thèse - Université Toulouse III

THÈSE
En vue de l'obtention du
DOCTORAT DE L’UNIVERSITÉ DE TOULOUSE
Délivré par l'Université Toulouse III - Paul Sabatier
Discipline ou spécialité : Ecologie Comportementale
Présentée et soutenue par
Jérémie CORNUAU
Le 04-12-12
Titre :
Signaux multiples et choix du partenaire chez le triton palmé Lissotriton helveticus
JURY
Thierry Lengagne (Chargé de recherche, Rapporteur)
Bruno Faivre (Professeur, Rapporteur)
Claude Miaud (Directeur EPHE, Examinateur)
Christophe Thébaud (Professeur, Examinateur)
Dirk Schmeller (Ingénieur de Recherche, Directeur de thèse)
Adeline Loyau (Post Doctorante, Directeur de thèse)
Ecole doctorale : SEVAB
Unité de recherche : Station d'Ecologie Experimentale du CNRS à Moulis USR 2936
Directeur(s) de Thèse : Adeline Loyau, Dirk S. Schmeller
Rapporteurs : Thierry Lengagne (Chargé de recherche) & Bruno Faivre (Professeur)
● Les sabots de Bethmale
"Le soir de Noël, le fiancé offre à sa fiancée une paire de sabots à longues pointes, habillée
de cuir et richement décorée de clous dorés dessinant un cœur. Il offre aussi une quenouille
rouge et un fuseau, le tout fabriqué avec tout son amour. La tradition veut que plus la pointe
des sabots est longue, plus l’amour est ardent..."
Autrefois le Couserans 2012 (St Girons/Ariège/France, Photo : Audrey Tourat). Les hommes
et les femmes portent des sabots de Bethmale dont la longueur reflète l’amour du bien-aimé.
REMERCIEMENTS
Août 2012, après une marche difficile entre brouillard et pluie, et accompagné de deux amis,
j’arrive en haut de la Pic Rouge de Bassiès. Juste avant le sommet, nous passons au-dessus
des intempéries accueillis par un soleil réconfortant. Je place ma pierre en haut du petit édifice
construit au fur et à mesure des passages de randonneurs. Je ne sais pas si « l’après thèse » me
procurera autant de plaisir que les pâtes chaudes qui m’ont accueilli au retour de ce périple.
Par contre ce qui est certain c’est que cette ascension marque la fin de ma thèse et l’heure
pour moi de remercier toutes les personnes qui m’ont permis de poser un premier grain de
sable dans le monde scientifique.
Je voudrais tout d’abord remercier Thierry Lengagne et Bruno Faivre d’avoir accepté de juger
le travail de trois ans de ma vie. Je voudrais également remercier Claude Miaud et Christophe
Thébaud, membres du jury, d’avoir accepté de partager les derniers moments de cette
aventure.
Mes remerciements vont également à l’Ecole Doctorale SEVAB et à son comité pour m’avoir
accordé un contrat doctorale.
Je tiens également à remercier Jean Clobert, directeur de la station d’Ecologie Expérimentale
de Moulis de m’avoir accueilli au sein de son établissement. Merci de m’avoir permis de
vivre la renaissance d’un laboratoire qui je l’espère continuera de grandir et accueillera
longtemps des embryons de chercheurs. Merci également d’avoir toujours laissé votre porte
ouverte.
Mes remerciements vont maintenant à Adeline et Dirk de m’avoir choisi pour cette thèse et de
m’avoir financé un tas de gadgets (étudiants compris) pour les expériences tritons. Merci
également de m’avoir accordé beaucoup de temps même dans les moments difficiles. Je
souhaite à ce sujet remercier la communauté féline de Cazaux de m’avoir prêté Adeline et
Dirk durant cette thèse. Je n’oublierai pas les nombreuses soupes chaudes à Bassiès après un
terrain glacial à la recherche de petites bêtes, et la gastronomie Cazausoise. Aussi je ne vous
remercierai jamais assez d’avoir montré à Audrey qu’un barbecue et une raclette se
conjuguent aussi en mode végétarien!
Parce qu’on ne remercie jamais assez les personnes qui nous ont formés, je voudrai ici
remercier tout ce qui au cours de ma formation m’a permis d’être ce que je suis aujourd’hui.
Merci donc à tout le personnel des écoles qui m’ont accueilli. Merci entre autre de m’avoir
laissé regarder les colombidés et autres bestioles par la fenêtre durant les maudites heures de
classe. Je tiens également à remercier tous ceux qui depuis les premiers cours sur « les
lumières de l’évolution » m’ont transmis leur savoir sur l’écologie comportementale. Merci à
Karine, Jérôme, Frank et F-X.
Je voudrai ici remercier tout le personnel de la Station d’Ecologie Expérimentale de Moulis
que j’ai croisé durant ces trois années de thèse. À Michelle de rester si longtemps le soir pour
veiller sur nous. À Sabine et les nombreuses visites de la grotte. À la dream team du Moulis
Football Club et à Fabien et Alexis fervent garant du beau jeu Moulisien. Cela a été un réel
plaisir de pouvoir jouer à un niveau « international ». À Michel pour le Moulis Tennis Club. À
Vincent pour le Moulis Marathon Club. À Olivier et Elodie, deux brillants naturalistes qui
m’ont beaucoup aidé durant cette thèse et qui ont rendu le « terrain » encore plus passionnant.
Une station en construction c’est forcement beaucoup de changements de bureau. Merci à
Jocelyne et Kim de m’avoir accueilli dans le bureau–secrétariat. Mes remerciements vont
également à tous les habitants de la salle thésard: Hamed, Sylvain l’habitant nomade, Audrey
mon soutient contre les galères administratives de fin de thèse, Julien et les discussions
scientifiques et comiques. Elvire danseuse étoile sur terrain de foot, Sophie une hirondelle qui
fait le printemps.
Merci à tous les stagiaires qui ont participés aux programmes NEWTS. À Margaux d’avoir
commencé avec moi cette aventure (merci aussi pour LUND). J’espère avoir un jour moi
aussi une vue sur l’océan. À Adelaïde d’avoir toujours su voir le Panda Roux qu’il y avait en
moi. Je ne peux m’empêcher de dire « Que vive la recherche à Moulis et que vive la
vie… ». A Romain, tueur de cloportes, amoureux de la cagouille et pourtant si bon avec les
tritons. A Géraldine, Thomas et Laurence, de m’avoir supporté et d’avoir regardé des vidéos
de tritons pendant des heures. Merci également à Fanny et les autres étudiants pour le terrain à
Bassiès.
Merci à Philippe et Dominique pour leur accueil à Bassiès aussi bien pour nous que pour nos
tritons. J’espère pouvoir revenir un jour (mais sans triton) !
J’ai ici une pensée pour tous mes amis que je n’ai pas assez vus suite à mon entrée au
monastère scientifique. J’espère pouvoir corriger cela une fois que « thèse » sera passée.
À Chonchon, p’tite Fred, Matthieu, Aurélia, Julien, Didie, Mylène, Nono et Gaëtan. Très bon
soutien en période de thèse.
À ma famille et les noëls réparateurs. À ma mère. Certainement le plus puissant des effets
maternels. C’est vraiment dommage que l’évolution ne sélectionne pas un peu plus les
personnes altruistes ! Tu étudie aussi des trucs dont tout le monde s’en fou... Tu te poses des
questions étranges le matin du genre « Y-a-t-il une opposition entre la philosophie des
lumières et la notion de hasard en génétique »… Il y a dans ta bibliothèque des livres sur
l’évolution et sur le comportement des animaux… Ce n’est peut être pas un hasard si j’en suis
là aujourd’hui !!! ☺
À mes deux frères, bien plus que des exemples pour moi, votre soutien m’a été précieux.
À Audrey, l’amour de ma vie. Si les tritons ne sont pas monogames c’est parce que tu n’as
pas d’équivalent dans leur monde. Je n’aurai jamais assez de mots pour te remercier de tout ce
que tu as fait pour moi. Des expériences tritons en passant par les révisions TOIEC jusqu’au
soutien pendant les périodes de stress intense, tu as toujours été présente pour moi. Cette thèse
et moi te devons énormément. En biologie évolutive on dit que “Nothing in biology makes
sense except in the light of evolution”. Je crois encore plus que “Nothing in my live makes
sense except in the light of your eyes” Merci pour tout, I love you…
PRÉAMBULE
Cette thèse traite de la théorie des signaux multiples dans le cadre du choix du partenaire
sexuel. La compréhension du « pourquoi » et du « comment » les individus utilisent plusieurs
signaux pour choisir leurs partenaires peut apporter des réponses intéressantes dans le cadre
de la conservation des espèces, de la gestion des espèces utilisées comme bien de
consommation par les Hommes, et de la réponse des organismes aux changements globaux
tels que les changements d’environnement, les nuisances sonores ou bien les maladies
émergentes. De plus, cela permet d’aborder des questions autour de l’utilisation de plusieurs
sources d’information et des mécanismes de prise de décision inhérente à toute type de
communication et donc transposable à beaucoup de situations rencontrées dans l’espèce
humaine. Finalement, et c’est certainement la cause qui m’anime le plus, la théorie des
signaux multiples est, à l’instar des sujets d’écologie comportementale, l’occasion
d’apprendre quelque chose sur les mécanismes évolutifs qui conduisent à l’élaboration des
comportements. Pour traiter ces questions autour des signaux multiples, j’ai utilisé un modèle
biologique tout aussi fascinant que les questions théoriques, le triton palmé, Lissotriton
helveticus. Comme pour la plupart des urodèles la parade des tritons a fasciné plus d’un
naturaliste. C’est pourquoi il existe un grand nombre de description des parades, plus ou
moins détaillé et plus ou moins anthropomorphique. Pour la plupart des gens, les tritons sont
méconnus voire insignifiants. Pourtant j’ai l’intime conviction que la « connaissance » peut
changer cette vision. En effet lorsqu’ils sont mis devant le fait accompli que dans des zones
humides, il existe un petit animal qui réalise des parades complexes pour séduire « sa
femelle »; les gens, dans un premier lieu un brin amusés, peuvent aussi devenir plus réceptifs
au problème de l’influence de l’homme sur son environnement.
Cette thèse comporte 5 articles dont je suis le premier auteur, et est subdivisée en quatre
grands chapitres. Le premier chapitre sert d’introduction. Il est composé d’une courte
introduction sur la sélection sexuelle, puis d’un article de synthèse sur les signaux multiples
dans le cadre du choix du partenaire [article 1]. Le deuxième chapitre est composé de deux
articles visant à comprendre le choix des femelles sur plusieurs signaux [article 2 et 3]. Dans
le troisième chapitre, j’ai testé la condition dépendance de signaux multiples [article 4 et 5].
Le quatrième et dernier chapitre est une discussion générale des travaux réalisés durant la
thèse suivi de perspectives.
SOMMAIRE
REMERCIEMENTS .................................................................................................................. 2
PREAMBULE............................................................................................................................ 4
SOMMAIRE .............................................................................................................................. 5
I. INTRODUCTION ................................................................................................................. 7
I. 1. Sélection sexuelle .......................................................................................................... 7
I. 2. Le Choix du partenaire sexuel ....................................................................................... 9
I. 3. Vers un modèle plus dynamique du choix du partenaire sexuel.................................. 12
I. 4. Signaux multiples......................................................................................................... 15
I. 5. Objectifs de la thèse ..................................................................................................... 16
II. SIGNAUX MULTIPLES CHEZ LE TRITON PALMÉ..................................................... 22
II. 1. Etat de l’art de la théorie des signaux multiples ........................................................ 22
II. 2. Signaux multiples et accès à la reproduction chez les tritons palmés ........................ 24
II. 3. Etude de la parade du triton........................................................................................ 25
III. SIGNAUX MULTIPLES, SÉLECTION SUR LE CONTENU ET HÉTÉROGÉNÉITÉ
DE L’ENVIRONNEMENT ..................................................................................................... 27
III. 1. Introduction ............................................................................................................... 27
III. 2. Condition dépendance de signaux multiples ............................................................. 28
III. 3. Effet de l’hétérogénéité de l’environnement sur l’expression de signaux multiples 29
IV. CONCLUSION GÉNÉRALE............................................................................................ 32
IV. 1. Choix des femelles sur critères multiples ................................................................. 32
IV. 2. Prise en compte de l’hétérogénéité de l’environnement ........................................... 35
IV. 3. Paradoxe du lek et conséquences sur les processus de sélection .............................. 37
IV. 4. Conséquences au niveau populationnel .................................................................... 38
IV. 5. Conséquences pour la biologie de la conservation ................................................... 40
IV. 6. Perspectives............................................................................................................... 42
BIBLIOGRAPHIE ................................................................................................................... 45
ARTICLES............................................................................................................................... 55
Article 1............................................................................................................................... 56
Cornuau JH, Rat M, Schmeller DS, Loyau A. 2012. Complex love decisions: why and how
animals use several signals in mate choice. En préparation.
Article 2............................................................................................................................. 100
Cornuau JH, Rat M, Schmeller DS, Loyau A. 2012. Multiple signals in the palmate newt:
ornaments help when courting. Behavioral Ecology and Sociobiology, 66:1045-1055.
Article 3............................................................................................................................. 112
Cornuau JH, Courtoix EA, Jolly T, Schmeller DS, Loyau A. It takes two to tango : Do both
male and female identities influence complex courtship display in a newt species? En
préparation.
Article 4............................................................................................................................. 138
Cornuau JH, Pigeault R, Schmeller DS, Loyau A. Condition-dependance of multiple sexual
traits in the palmate newt (Lissotriton helveticus). En préparation.
Article 5............................................................................................................................. 174
Cornuau JH, Sibeaux A, Tourat A, Schmeller DS, Loyau A. Impacts of varying
environmental conditions sexual traits and consequences for mate choice in the Palmate newt.
En préparation.
SUMMARY ........................................................................................................................... 214
RESUME................................................................................................................................ 215
I. Introduction.
I. 1. Sélection sexuelle.
Pour les individus pratiquant une reproduction sexuée, la capacité à transmettre une
copie de leur génome dépend fortement de la capacité à trouver un partenaire sexuel. La
sélection exercée sur les individus pour l’accès à la reproduction est appelée sélection
sexuelle (Darwin 1871). A l’instar de la sélection naturelle dont elle peut être vue comme une
sous-catégorie, la sélection sexuelle est un processus de tri entre variants phénotypiques. La
spécificité de ce que l’on regroupe sous le terme de sélection sexuelle, est que le tri est
effectué en fonction de l’accès différentiel aux partenaires sexuels (Danchin et al. 2008). La
sélection sexuelle est ainsi une sélection sociale, c'est-à-dire basée sur des interactions intraspécifiques et qui utilise un système de communication du type « émetteur-receveur » (Lyon
& Montgomerie 2012, Box 1, Figure 1).
Box 1 : Communication sexuelle
La communication sexuelle se fait à partir d’indices (cues) appelés signaux
s’ils ont évolué pour la communication (Candolin 2003). Les signaux sont émis par
l’émetteur (le plus souvent mâle) et traduit par le receveur (le plus souvent
femelle). Un signal peut être défini comme « une structure ou une action de
l’émetteur qui est sélectionnée pour ses effets sur le comportement du receveur via
son système nerveux » (Bro-Jørgensen 2010). Il est important de rappeler que les
deux protagonistes agissent pour leurs « propre bien » c'est-à-dire optimiser leur
propre fitness.
"Influencer le receiver”
receveur"
“Influencing
Signal
Emetteur
“Information
extraction”
"Extraire de l’information"
Receveur
Figure 1. Représentation d’une communication entre un mâle (émetteur) et une
femelle (receveur).
Trois conditions sont nécessaires pour enclencher un mécanisme de sélection sexuelle
(Danchin et al. 2008). La première requiert de la variation sur un trait sexuel. La deuxième
repose sur le fait que cette variation du trait sexuel soit liée/se traduise par une variation sur
l’aptitude phénotypique (fitness) c'est-à-dire sur la capacité d’un individu à produire plus de
descendants matures par rapport aux autres individus. La troisième condition est que le trait
sexuel et/ou l’aptitude phénotypique soit héritable c'est-à-dire transmissible à la descendance.
Pour les espèces sexuées, une des principales différences entre les mâles et les
femelles est l’investissement dans les gamètes. En effet, les mâles produisent de petits
gamètes, considérés comme peu coûteux, contenant principalement le matériel génétique
(spermatozoïdes). Au contraire, les femelles produisent une plus faible quantité de gros
gamètes plus coûteux composés également de substance nutritive (ovocytes). Cette
anisogamie dans la taille des gamètes qui conduit à des taux potentiels de reproduction
différents, fait que, les femelles investissent généralement davantage que les mâles dans la
descendance (Bateman 1948, Trivers 1972, mais voir Clutton-Brock 2009). Ainsi, pour une
même quantité d’énergie, un mâle peut produire beaucoup plus de gamètes qu’une femelle. Il
existe donc à un moment donné dans la population une grande quantité de gamètes mâles
contre une faible quantité de gamètes femelles. Les femelles étant la ressource limitante, leur
succès reproducteur va dépendre principalement de la qualité du partenaire sexuel (Box 2).
Ainsi, nous pouvons nous attendre à ce que la sélection favorise les femelles ayant la capacité
à choisir les mâles de meilleures qualités (partie B). A l’inverse le succès reproducteur des
mâles va dépendre principalement de l’accès aux femelles réceptives. Ainsi, les mâles entrent
généralement en compétition pour accéder aux femelles et investissent donc fortement dans la
production de traits sexuels leurs facilitant cet accès. Deux grands types de stratégies
existent pour accéder aux femelles et sont appelées sélection intra- et inter-sexuelle. La
sélection intra-sexuelle, ou compétition intra-sexuelle, repose sur une compétition directe
entre mâles pour l’accès aux femelles et conduit à l’évolution de caractères sexuels
secondaires appelés dans ce cas « armements ». La sélection inter-sexuelle repose sur la
capacité d’un mâle à être choisi par une femelle et conduit à l’évolution des caractères sexuels
secondaires préférés par les femelles (ornements). Il existe de nombreux liens entre les
armements et les ornements et faire la distinction entre la sélection intra- et inter-sexuelle
n’est pas toujours aisée. En effet les femelles peuvent choisir (inter) les mâles ayant la
capacité de gagner des combats (intra) allant même jusqu'à solliciter les combats (Berglund et
al. 1996). Néanmoins il existe aujourd’hui un grand nombre de preuves empiriques
d’évolution de caractères sexuels secondaires uniquement causée par le choix du partenaire
sexuel effectué par les femelles (Andersson 1994, Danchin et al. 2008). Dans cette thèse nous
avons surtout abordé l’évolution des caractères sexuels liés aux choix des femelles.
Box 2 : La qualité du partenaire sexuel
L’expression "qualité" d’un individu paraît au premier abord suffisamment claire pour que
nous puissions nous affranchir de la définir. Cependant une lecture rapide de la littérature
montre que ce terme est utilisé pour désigner des choses très différentes et peut donc rendre
le concept parfois ambigu (Bergerons et al. 2011, Lailvaux & Kasumovic 2011). Ainsi,
dans cette thèse, nous avons choisi de définir la qualité d’un individu comme « un axe de
variation hétérogène entre les individus qui est positivement corrélé avec la fitness »
(Wilson & Nussey 2010). Lorsque la qualité d’un mâle est d’ordre génétique nous parlons
de bons gènes (good genes). Cependant, la qualité d’un mâle peut être d’ordre nongénétique, telle que la possession d’un territoire de bonne qualité. Un individu de meilleure
qualité est donc un individu qui peut avoir une meilleure condition corporelle, être avantagé
dans l’accès aux ressources, avoir acquis de meilleures ressources protéiques ou lipidiques,
posséder une meilleure résistance aux parasites, une meilleure compatibilité génétique, un
meilleur territoire, ou encore avoir une haute fertilité. Lorsque les qualités permettent un
bénéfice pour les femelles s’exprimant seulement dans leur progéniture on parle de
bénéfice indirect et lorsque les bénéfices s’expriment lors de la reproduction en cours nous
parlons de bénéfice direct.
I. 2. Le choix du partenaire sexuel.
Le choix du partenaire sexuel est un « comportement où un individu influence la
probabilité de se reproduire avec un individu particulier, plutôt qu’avec d’autres individus,
suivant un ou plusieurs traits chez l’individu du sexe opposé » (Bateson 1983, Bradbury &
Andersson 1987). L’appariement et/ou l’accouplement entre deux individus ne sont donc pas
aléatoires. Ainsi, le choix du partenaire repose sur des règles de décision, sur des préférences
internes à chaque individu et sur des contraintes environnementales telle que la disponibilité
de différentes options (Wagner 1998).
Plusieurs hypothèses ont été développées pour expliquer l’évolution des préférences
sexuelles (Jones & Ratterman 2009, Tableau 1). Ces hypothèses peuvent être classées en
fonction de l’information potentiellement contenue dans le trait des mâles et des bénéfices que
les femelles peuvent espérer d’un tel choix (Jones & Ratterman 2009). En effet, le trait
exprimé par les mâles peut être vu comme un "badge" signalant une information spécifique
sur la qualité du mâle pour les femelles. Ce badge doit être résistant à la tricherie et donc être
un signal honnête de la qualité du mâle (Maynard Smith & Harper 2003). La fiabilité du trait
peut être maintenue par des contraintes, notamment par le coût trop important de la tricherie
ou encore par le coût de la production et/ou de la maintenance du trait (Searcy & Nowicki
2005). Par exemple, la taille des individus peut être un bon indice de la capacité de croissance
des mâles car seuls les mâles ayant une bonne capacité de croissance ont pu effectivement
grandir. Les ornements des mâles sont généralement coûteux à produire et donc seuls les
mâles de bonne qualité (Box 2) sont capables de les produire et de les maintenir. Ce principe
est appelé « principe du Handicap » et indique que l’honnêteté du signal (et donc sa
résistance à la tricherie) est scellée par le coût du signal (Zahavi 1975). Par exemple chez les
Fou à pieds bleus Sulanebouxii, seuls les mâles de bonne qualité, c'est-à-dire ayant eut
récemment accès à du poisson frais, peuvent maintenir la coloration bleue de leurs pattes et
donc être attirants pour les femelles (Velando et al. 2006).
D’autres formes d’information peuvent être extraites par les femelles sans pour autant
être coûteuses pour les mâles. De nombreux exemples récents montrent que les femelles
peuvent baser leurs choix sur des critères de compatibilité génétique (Mays & Hill 2004),
et/ou comportementale (Schuett et al. 2010). Par exemple, chez l’épinoche à trois épines
Gasterosteus aculeatus, les femelles utilisent l’odeur des mâles pour choisir un partenaire
permettant de maximiser la diversité génétique de leurs progénitures (Aeschlimann et al.
2003, Milinski et al. 2005). De même, voir un mâle s’accoupler avec une femelle peut aussi
être considéré comme un signal attestant de la qualité de ce mâle (copiage du choix de
partenaire, Danchin et al. 2011). Dans ce cas, les femelles utilisent de l’information sociale
qui, sans forcement être coûteuse pour le mâle, donnent aux femelles observatrices une
indication indirecte sur la qualité des mâles, telle que cette qualité est perçue par les autres
femelles (Witte & Ryan 1998, 2002).
La préférence des femelles peut aussi avoir évolué sans réelle information véhiculée
par le trait et sans bénéfice direct pour les femelles. Un modèle classique est le trait de
Fisher (Fisher 1915, 1930, Lande 1981, Kirkpatrick 1982). Ce modèle invoque une
préférence chez les femelles héritable de mère en fille et un trait phénotypique chez les mâles
héritable de père en fils. Dans ce modèle, les femelles exprimant une préférence pour le trait
du mâle engendreront des filles qui exprimeront la même préférence que leurs mères et des
fils qui exprimeront le même trait phénotypique que leur père et qui seront donc préférés à
leur tour. Ce modèle repose sur une corrélation génétique entre le trait des mâles et la
préférence de la femelle. Il permet d’expliquer le maintien d’une préférence chez les femelles
et même son renforcement, mais n’explique pas l’apparition de la préférence chez les femelles
(Jones & Ratterman 2009).
L’hypothèse du biais sensoriel permet d’expliquer l’apparition d’une préférence chez
les femelles pour un trait chez les mâles. En effet, dans ce modèle la préférence des femelles
existerait avant l’apparition du trait chez les mâles (Basolo 1990, Ryan & Rand 1990, Fuller
et al. 2005, Kokko et al. 2003). Cette préférence pourrait être d’origine non sexuelle et
maintenue par la sélection utilitaire. Un exemple connu est la préférence exercée par les
femelles guppys Poecilia reticulata pour la coloration orangée des mâles (Rodd et al. 2002).
Rodd et al. (2002) ont en effet montré, en utilisant plusieurs populations de guppy, que la
force d’attraction des femelles pour la coloration orangée dans un contexte non sexuel (ici la
nourriture) explique 94% de la variation inter-population de la préférence sexuelle des
femelles pour cette coloration.
Un dernier type de modèle, basé sur le conflit sexuel, peut expliquer l’évolution des
préférences des femelles (Hollande & Rice 1998, Cameron et al. 2003, Parker 2006). Les
intérêts des mâles et des femelles divergent souvent lorsqu’il s’agit de reproduction (voir box
1). Or, la sélection sexuelle favorise les mâles ayant la capacité d’accéder à la reproduction.
Ainsi, toute mutation qui permettrait à un mâle d’être avantagé dans l’accès à la reproduction
(par exemple en utilisant un biais sensoriel), lui procurerait une meilleure descendance et
donc la mutation serait sélectionnée, même si celle-ci n’apporte aucun bénéfice à la femelle.
Cependant, si cela induit une reproduction suboptimale de la femelle, il est attendu que toute
mutation provoquant une résistance des femelles pour le trait sera sélectionnée. Suivant le
modèle de sélection antagoniste, il s’en suit une nouvelle sélection sur l’habilité des mâles à
séduire les femelles (Hollande & Rice 1998).
Il existe donc une multitude de théories expliquant l’évolution de la préférence des
femelles (Tableau 1). Toutes ces théories ne sont pas mutuellement exclusives (Kokko et al.
2003). Ceci est particulièrement vrai pour les traits de Fisher ou les biais sensoriels qui
peuvent agir conjointement avec toutes les autres théories (Jones & Ratterman 2009).
Tableau 1. Exemples de modèles expliquant l’évolution de la préférence des femelles. Les
modèles sont souvent classés selon le potentiel informatif du trait pour la femelle. Adapté de
Jones & Ratterman (2009).
Mécanisme d’évolution de
la préférence des femelles
Trait informatif
Bénéfice direct
Particularités
Références
Le bénéfice s’exprime lors de
la reproduction en cours
Nakatsuru & Kramer 1982
Le bénéfice s’exprime
uniquement dans la
progéniture
Welch et al. 1998
Déséquilibre de liaison entre
la préférence des femelles et
le trait chez les mâles
Rowe 2001
Biais sensoriel
La préférence des femelles
précède l’apparition du trait
chez les mâles
Basolo 1990
Conflit sexuel
Evolution d’une résistance
des femelles contre des traits
manipulateurs chez les mâles
Demary & Lewis 2008
Bénéfice indirect
Trait non-informatif
Processus de Fisher
I. 3. Vers un modèle plus dynamique du choix du partenaire sexuel ?
L’approche de classification de l’évolution des préférences des femelles pour un trait
chez les mâles peut avoir l’inconvénient d’admettre de manière implicite que la
communication sexuelle est robuste aux variations spatiale et temporelle (Jones & Ratterman
2009). En effet, les études expérimentales et les modèles théoriques ont eu tendance à
considérer les préférences sexuelles comme fixes (Wagner 1998). Or, comme tout trait
phénotypique, le choix du partenaire et l’expression des traits sexuels peuvent être
expliqués par des gènes, par l’environnement et par l’interaction entre les gènes et
l’environnement (Greenfield & Rodriguez 2004). En effet, les gènes peuvent s’exprimer
différemment dans des environnements différents ; ce phénomène est connu sous le nom de
plasticité phénotypique (Schlichting & Pigliucci 1998). L’expression d’un génotype suivant
un gradient d’environnement est appelé norme de réaction (Schlichting & Pigliucci 1998).
Lorsque les normes de réaction de différents génotypes ne sont pas parallèles, une interaction
gène-environnement se produit (GEI, Fig. 2, Greenfield & Rodriguez 2004).
a)
e
py
to 1
né
h
P c)
1
b)
2
1
2
d)
2
1
Environnement
2
Figure 2. Expression du phénotype (trait sexuel, choix du partenaire) dans différentes
conditions environnementales. Le trait plein représente un génotype A, le trait en tiret
représente un génotype B. a) Les génotypes A et B ont des niveaux d’expression qui ne
diffèrent pas en fonction de l’environnement (phénotype = génotype), b) Les génotypes A et
B ont des niveaux d’expression qui diffèrent en fonction de l’environnement (plasticité) mais
la norme de réaction est parallèle (phénotype = génotype + environnement). c) et d) Les
génotypes A et B ont des niveaux d’expression qui diffèrent en fonction de l’environnement
et les normes de réaction ne sont pas parallèles (phénotype = génotype + environnement +
génotype × environnement). En c) l’expression du génotype A est toujours supérieure à celui
de B mais contrairement à la situation d) où les normes de réaction se croisent.
Ce phénomène couramment étudié pour des traits soumis à la sélection utilitaire a fait
l’objet de rares études dans le cadre du choix du partenaire (Cornwallis & Uller 2010). Étant
donné que la plupart des modèles d’évolution de la préférence pour un partenaire se focalise
sur le choix pour un trait plus ou moins informatif (Jones & Ratterman 2009), des études plus
récentes se sont focalisées sur l’effet de l’hétérogénéité de l’environnement sur le choix du
partenaire en lui-même et sur la condition dépendance des traits sexuels (Cotton et al. 2006).
Ces études montrent que le choix des femelles peut varier rapidement dans sa sélectivité ainsi
que dans sa direction selon l’environnement et donc affecter grandement le régime de
sélection (Jennions & Petrie 1997). Plusieurs sources environnementales peuvent influencer le
choix des femelles. On distingue des facteurs externes telles que la qualité de l’habitat, la
prédation, la densité et la sex-ratio et des facteurs internes tels que l’âge de la femelle, son
expérience, sa condition physique, sa personnalité et son statut social (Jennions & Petrie
1997, Cotton et al. 2006). Un exemple classique est la variation dans le choix causée par une
variation de la réceptivité des femelles. Par exemple, chez le triton ponctué Lissotriton
vulgaris, la sélectivité des femelles est très faible lorsqu’elles ne se sont pas encore
reproduites et leur choix apparait comme aléatoire suivant la qualité du mâle (Gabor &
Halliday 1997). En revanche, après une première reproduction, les femelles deviennent plus
sélectives et montrent une préférence pour les mâles de meilleure qualité c'est-à-dire les mâles
ayant une plus grande condition corporelle (Gabor & Halliday 1997). En effet, il parait plus
avantageux de se reproduire avec un mâle sans avoir fait un choix au préalable que de ne pas
se reproduire (Jennions & Petrie 2000). Par contre, il devient avantageux pour les femelles en
terme de fitness d’être de plus en plus sélectives à mesure que les épisodes de reproduction se
succèdent (Jennions & Petrie 2000).
Des études récentes suggèrent également un fort effet de l’hétérogénéité de
l’environnement sur la condition-dépendance des ornements (Robinson et al. 2007, 2012,
Scordato et al. 2012). Il a notamment été montré, chez le Gobemouche à collier Ficedula
albicollis, que les femelles en couple avec un mâle exprimant une forte ornementation
(coloration blanche connue pour être dépendante de la condition et soumise à la sélection
sexuelle) avaient une meilleure fitness durant les périodes sèches (Robinson et al. 2012).
Cependant cette relation était inversée en période humide. Ainsi les femelles en couple avec
des mâles fortement ornementés avaient une fitness plus faible que les femelles en couple
avec des mâles moins ornementés (Robinson et al. 2012). Ces exemples montrent que
l’honnêteté d’un signal est relative à l’environnement et amène des questionnements sur le
caractère adaptatif du choix des femelles en fonction des environnements. Ces questions
seront abordées dans les articles 1 et 5.
Bien que la prise en compte des effets de l’environnement apparaisse comme
essentielle pour la compréhension des mécanismes de sélection sexuelle, peu d’études
incluent ce facteur dans la compréhension du choix du partenaire (Bussière et al. 2008,
Cornwallis & Uller 2010). Il convient donc de l’inclure dans de futures études (article 1,
article 5).
1. 4. Signaux multiples.
Les exemples que nous venons de développer dans les parties précédentes de
l’introduction font appel à une préférence des femelles pour un trait chez les mâles. Dans la
partie suivante nous avons intégré le fait que les femelles expriment souvent des
préférences multiples et que les mâles possèdent plusieurs traits potentiellement
sélectionnés par les femelles. Cependant, toutes les théories développées précédemment pour
expliquer l’évolution d’une seule préférence, ainsi que l’effet de l’hétérogénéité de
l’environnement sur le choix et l’expression des traits sexuels demeurent valables dans un
contexte de préférences multiples.
La possibilité que la communication sexuelle soit basée sur plusieurs traits, résultant
en plusieurs critères de choix du partenaire, a reçu une attention particulière en sélection
sexuelle (Guilfort & Dawkins 1991, Møller & Pomiankowski 1993). En effet, des
observations ont montré que les mâles exhibaient de nombreux ornements et que les femelles
pouvaient exprimer des préférences pour plusieurs traits (Guilfort & Dawkins 1991, Møller &
Pomiankowski 1993). On parle ainsi de signaux multiples, signaux complexes, ou signaux à
multi-composants (Candolin 2003). Les recherches sur les signaux multiples dans le cadre du
choix de partenaires se sont intensifiées (Candolin 2003, Hebets & Papaj 2005) et continuent
d’être un axe de recherche important en sélection sexuelle (Lozano 2009, Bro-Jørgensen
2010). Ces recherches se concentrent principalement sur deux grands types de questions :
(1) Pourquoi les individus utilisent-ils des signaux multiples dans la communication
sexuelle ?
(2) Comment utilisent-ils et hiérarchisent-ils les multiples signaux ?
La première question vise à comprendre les mécanismes évolutifs qui permettent
l’apparition et le maintien de l’utilisation de plusieurs signaux. La seconde vise à comprendre
les règles de décision utilisées par les femelles lorsque plusieurs signaux sont disponibles.
Dans cette thèse, nous avons réalisé une synthèse sur les signaux multiples dans le cadre
du choix du partenaire. Ces signaux multiples sont également utilisés dans le cadre plus
large de la sélection sociale, tel que la communication parent-enfant (Jacob et al. 2011), les
receveurs multiples (Pryke et al. 2001, Andersson et al. 2002), la compétition intra-sexuelle
(Chaine & Lyon 2008) ou la dominance (Chaine et al. 2011). Cependant, nous avons choisi de
nous restreindre spécifiquement au choix du partenaire.
Au cours de ce travail bibliographique, nous avons synthétisé les facteurs
ultimes et proximaux du choix du partenaire basés sur des signaux multiples en utilisant des
exemples récents. Nous avons également mis en lumière la nécessité d’inclure certains
signaux (notamment l’information sociale et la compatibilité) jusque-là peu considérés dans le
cadre théorique des signaux multiples. Ensuite, nous avons développé deux grands axes
d’avenir pour l’étude des signaux multiples. Le premier est la prise en compte de
l’hétérogénéité de l’environnement sur les signaux multiples. Le second est la nécessité de
coupler les théories développées sur les signaux multiples avec les connaissances apportées
par l’écologie cognitive afin de mieux comprendre les prises de décision basées sur des
signaux complexes. Cette synthèse permet d’avoir une vision générale de la théorie des
signaux multiples tant sur les recherches passées et actuelles, que sur ses futurs
développements.
Pour plus d’informations sur les signaux multiples, je vous invite à lire ce
travail de synthèse que vous trouverez dans l’article 1 “Complex love decisions: why and how
animals use several signals in mate choice?”.
I. 5. Objectifs de la thèse.
L’objectif général de cette thèse était l’étude des signaux multiples dans le cadre
du choix du partenaire sexuel. En effet, si les facteurs ultimes et proximaux de l’utilisation
de signaux multiples sont maintenant bien étudiés, il reste encore à apporter les preuves
expérimentales sur des taxons variés (article 1). De plus, bien qu’il soit admis que
l’hétérogénéité de l’environnement puisse avoir un effet important sur les signaux multiples et
éventuellement expliquer leur évolution, les preuves expérimentales demeurent encore
relativement faibles (article 1).
Nous avons choisi le triton palmé Lissotriton helveticus (Box 3) comme modèle
biologique à notre étude sur les signaux multiples dans le cadre du choix du partenaire.
Cette espèce rassemble les qualités adéquates pour notre étude. En effet les mâles possèdent
de nombreux caractères sexuels secondaires tels que des palmures au niveau des pattes
arrières, une crête dorsale, un filament caudal, une coloration ventrale orangée, ainsi
que des comportements de parade complexes (Halliday 1975, Griffiths & Mylotte 1988,
Figures 3, 4 et 5). Chez cette espèce de triton, les interactions de compétition directe entre les
mâles semblent très faibles (Wells 2007), même si une compétition par exploitation n’est pas
à exclure. La présence de ces traits complexes et la faible compétition entre les mâles
suggèrent un rôle actif du choix des femelles dans l’évolution de ces traits sexuels multiples
(article 1).
Dans une première partie nous avons étudié l’effet des signaux multiples du mâle
sur le choix des femelles chez le triton palmé (article 2 et 3). Nous avons tout d’abord
examiné quels traits sexuels avaient le potentiel pour être sélectionnés par les femelles, et ceci
en nous focalisant à la fois sur les traits sexuels morphologiques et des traits
comportementaux des mâles (article 2). Dans le but de mieux comprendre l’importance des
traits comportementaux identifiés grâce à l’étude rapportée dans l’article 2, nous avons
examiné s’ils étaient répétables et s’ils étaient liés à des caractéristiques phénotypiques
(article 3).
Comme nous l’avons expliqué dans l’introduction, les traits sexuels des mâles peuvent
être révélateurs de leur qualité. Cette condition-dépendance des traits sexuels est primordiale
pour distinguer les hypothèses d’évolution des préférences multiples (article 1). Dans une
deuxième partie nous avons donc exploré le rôle des signaux multiples des mâles en tant
que signaux de qualité individuelle chez le triton palmé (article 4 et 5). Nous avons
également testé l’effet de l’hétérogénéité de l’environnement sur l’honnêteté des traits
sexuels et les conséquences que cela pouvait avoir sur le choix des femelles (article 5).
Box 3 : Le Triton palmé
Le triton palmé Lissotriton helveticus est un amphibien de la famille des
Salamandridae. Cette espèce est largement répandue en France autant en basse altitude
qu’en montagne (observation jusqu'à 2400 mètres). Cette espèce est également présente en
Allemagne, Grande-Bretagne, Suisse, Belgique, Luxembourg, ainsi que dans le nord de
l’Espagne et du Portugal. Le triton palmé est une espèce protégée, classée comme
« considérations mineures » par l’IUCN. Les tritons palmés font partis des plus petits tritons
d’Europe puisque la taille totale des mâles ne dépasse que rarement 8 cm pour les mâles et
10 cm pour les femelles. Ils requièrent peu d’espace lorsqu’ils sont maintenus en captivité,
ce qui en fait un modèle intéressant en laboratoire. Les tritons palmés peuvent vivre jusqu'à
8 ans à 11 ans dans la nature (Amat et al. 2010).
Il existe deux grandes phases de vie du triton durant l’année. Durant la phase dite
terrestre, le triton vit à terre, proche des zones humides et dépend de la présence de couvert
boisé. La phase dite aquatique, correspond à la période de reproduction. Lorsqu’il est en
phase aquatique, le triton palmé vit dans des milieux aquatiques stagnants ou à très faible
courant tels que des petites flaques d’eau, des mares peu profondes, ou des lacs (Denoël &
Lehmann 2006). La migration prénuptiale marque la fin de la phase terrestre et le début de
la phase aquatique. Les mâles se dirigent vers leur point d’eau et s’ornent de caractères
sexuels secondaires, inexistants en période terrestre, tels que les palmures, le filament
caudal, et la crête dorsale (Figure 5). C’est également en phase aquatique que les mâles
expriment des comportements de parade envers les femelles (Figure 3 et 4). La
reproduction se fait par transfert de spermatophore que le mâle place sur le sol et que la
femelle prend au niveau de son cloaque. La femelle peut prendre plusieurs spermatophores
de plusieurs mâles différents au cours de la saison de reproduction. Il est important de noter
qu’il n’existe pas de comportement d’amplexus chez le triton palmé et qu’il n’existe pas
non plus de comportement agressif physique du mâle envers la femelle (Wells 2007). En
revanche, les mâles passent une grande partie de leur phase aquatique à parader devant les
femelles et à les suivre. Les femelles pondent des œufs (jusqu'à 400) dans l’eau en
enroulant chaque œuf individuellement dans une feuille. Ce geste, important pour la survie
des œufs, constitue le seul soin parental que la progéniture reçoit (Miaud 1990). A la fin de
la saison de reproduction, les mâles et les femelles retournent en phase terrestre. Une fois le
développement de l’œuf achevé (après environ 1 mois), les larves de triton croissent dans
l’eau, durant environ 2 mois, avant de gagner la terre. Les individus reviendront dans l’eau
une fois devenus sexuellement mature c'est-à-dire pas avant l’âge de 3 à 4 ans. reniflement
Le mâle se place devant la femelle
Coup de fouet
Vague
Orientation
poursuite
Parade
« statique »
éventail
éventail
Parade
« de retrait »
Coup de fouet
Devancer
Trembler
Phase du transfert
de spermatophore
Touche queue
Dépôt
Avancer encore
Appât distal, Queue frémissante
interrompre
repousser
Figure 3. Représentation des séquences principales du comportement de cour chez le triton
palmé Lissotriton helveticus. Le mâle est représenté en noir et la femelle en blanc. Eventail =
fan, coup de fouet = whip, trembler = quiver. D’après Arntzen & Sparreboom (1989) et
Denoël (1999).
Figure 4. Trois comportements principaux de parade chez le triton palmé Lissotriton
helvetivus. En haut, le comportement de vague (wave). Au milieu le comportement de coup de
fouet (whip). En bas le comportement d’éventail (fan). D’après Halliday (1977) et Wells
(2007).
Figure 5. Traits morphologiques du mâle triton palmé Lissotriton helveticus. En haut sont
représentées les extensions de la peau (crête, filament, palmure). En bas sont représentés les
patterns de coloration ventrale. (Photographies : Jérémie Cornuau).
II/ Signaux multiples chez le triton palmé.
II. I. Etat de l’art de la théorie des signaux multiples.
La théorie des signaux multiples stipule que plusieurs caractères sexuels secondaires sont
importants pour expliquer le succès reproducteur des mâles (article 1). L’expression de ces
traits peut être plus ou moins corrélée et l’influence d’un trait par rapport à l’autre peut être
différente suivant la présence ou non d’autres traits (article 1). Pour de nombreuses espèces,
le succès des mâles dépend d’une combinaison de traits comportementaux (parade) et de traits
morphologiques (Tableau 2). Par exemple, chez la rainette arboricole Hyla arborea, la
couleur et le chant des mâles expliquent le choix des femelles et les deux traits semblent avoir
la même importance (Richardson & Lengagne 2010, Richardson et al. 2010). A l’inverse chez
l’épinoche à cinq épines Culaea inconstans, alors que la couleur nuptiale et la taille des mâles
peuvent être tous deux des critères de choix, la parade est le critère le plus important pour les
femelles (Ward & McLennan 2008).
Tableau 2. Liste non exhaustive d’espèces pouvant utiliser à la fois des traits morphologiques
et des traits comportementaux au cours du choix du partenaire sexuel. Les trais indiqués en
gras sont les traits prédominants dans le choix des femelles.
Espèce
Grillons des
champs
Araignée Loup
Rainette
arboricole
Lézard à
collerette
commun
Guppy
Traits morphologiques
Traits comportementaux
Références
Gryllus
campestris
Schizocosa
uetzi
Hyla arborea
Taille de la harpe
Taux de gazouillement
Scheuber et al. 2004
Couleur des pattes
Schamble et al. 2009
Coloration du sac vocal
Fréquence de coups de
patte
Chant
Crotaphytus
collaris
Taille et couleur
corporelle
Comportements
territoriaux
Bairs et al. 2008
Poecilia
Coloration
Sigmoïde
reticulata
Epinoche à
Gasterosteus
Taille et coloration
Nage en zigzag
trois épines
aculeatus
corporelle
Gobie
Rhinogobius
Nageoire dorsale*
Nage*
brunneus
Epinoche à
Culaea
Taille et coloration
Intensité de parade
cinq épines
inconstans
corporelle
Junco ardoisé
Junco
Couleur de la queue
Chant
hyemalis
Colin de
Callipeplaga
Coloration corporelle
Parade
Gambel
mbelii
Siffleur doré
Pachycephala Coloration de la gorge
Chant
pectorialis
*l’importance donnée à chaque trait dépend de la condition de la femelle.
Richardson & Lengagne 2010
Kodric-Brown & Nicoletto 2001
Künzler & Bakker 2001
Suk & Choe 2008
Ward & McLennan 2009
Hill et al. 1999
Hagelin & Ligon 2001
Van Dongen & Mulder 2008
De nombreuses études se sont focalisées sur les signaux multiples chez les anoures
(Poole & Murphy 2007, Akre & Ryan 2010, Richardson & Lengagne 2010, Richardson et al.
2010, Taylor et al. 2011), alors que des études équivalentes sont rares chez les urodèles. Ainsi
à notre connaissance la seule étude suggérant l’implication potentielle de signaux multiples
chez un urodèle a été conduite chez le triton palmé Lissotriton helveticus (Haerty et al. 2007).
Pourtant, il est généralement admis que chez les urodèles les comportements de parade
ainsi que les traits morphologiques et certainement la combinaison des deux influencent
grandement le choix des femelles (Wells 2007). Parmi les traits morphologiques, les
extensions de la peau telle que la crête dorsale semblent affecter le choix des femelles chez de
nombreuses espèces de tritons (Wells 2007). Ainsi il a été montré chez le triton crêté Triturus
cristatus et le triton ponctué Lissotriton vulgaris que les mâles possédant une large crête
étaient avantagés dans l’accès aux femelles par rapport aux mâles possédant une crête moins
développée (Green 1991, Gabor & Halliday 1997). La taille du mâle peut également être un
critère de choix pour les femelles (Haerty et al. 2007). Enfin la coloration du mâle pourrait
avoir une importance chez les tritons (Denoël & Dollen 2010, Secondi et al. 2012), ce qui n’a
été jusque-là que peu explorée chez les amphibiens (Richardson & Lengagne 2010,
Richardson et al. 2010). Les comportements de parade pourraient également être des éléments
clefs du choix des femelles (Wells 2007). En effet, chez le Pléthodonte nord américain
Desmognathus ocoee, les mâles ayant des fréquences de parade élevée ont un succès plus
important dans l’accès aux femelles par rapport aux males à faible fréquence de parade
(Vinnedge & Verrell 1998). En revanche à notre connaissance aucune étude n’a étudié
l’influence de la combinaison de la parade et des traits morphologiques sur l’accès à la
reproduction chez les urodèles.
Comme nous l’avons précédemment décrit, les tritons palmés mâles possèdent des traits
morphologiques et comportementaux potentiellement importants dans le choix des femelles
(Haerty et al. 2007, Wells 2007, Figure 3, 4, 5). Nous avons réalisé des expériences,
synthétisées sous la forme de deux articles (article 2 et 3), dont le but était de mieux
appréhender le rôle des traits morphologiques et comportementaux dans le cadre du
choix du partenaire chez le triton palmé.
II. 2. Signaux multiples et accès à la reproduction chez les tritons palmés. [article 2]
Haerty et al. (2007) ont mesuré le choix des femelles de triton palmé pour le filament
et pour la taille, deux traits fortement indépendants l’un de l’autre. Leurs résultats montrent
que les femelles passaient d’avantage de temps dans le compartiment contenant des mâles de
petite taille et possédant un filament plus développé (Haerty et al. 2007). Cependant, le
protocole utilisé dans cette étude ne permettait pas aux mâles de parader librement et cela
avait pour conséquence de retirer à l’appréciation des femelles un trait potentiellement
important pour elles. Afin de tester l’importance des signaux multiples dans le choix du
partenaire chez le triton palmé, nous avons pris en compte à la fois l’importance du
filament mais également d’autres traits tels que la coloration ventrale, la taille corporelle
et les comportements de parade (article 2). Nous avons utilisé un protocole expérimental
ouvert, c'est-à-dire que les individus interagissaient librement, et les femelles avaient le choix
entre deux mâles qui différaient pour la taille de leur filament (un grand versus un petit
filament). Nos prédictions étaient un meilleur accès à la reproduction pour les mâles
possédant un grand filament, une fréquence de parade forte, une coloration orangée intense et
une taille réduite. Afin de tester l’importance du filament seul, nous avons réalisé une seconde
expérience où nous avons expérimentalement inversé la taille relative des filaments des mâles
proposés au choix des femelles. Ainsi, les mâles à grand filament étaient devenus des mâles à
petit filament. Nos prédictions étaient une diminution du succès reproducteur des mâles dont
la longueur du filament avait été modifiée.
Les résultats que nous avons obtenus sont détaillés dans l’article 2. Ils montrent que
l’accès des mâles à la reproduction est fortement influencé par la taille du filament. En effet
les mâles à grand filament avaient un meilleur accès à la reproduction. De plus, lorsque le
filament avait été réduit, le succès des mâles l’avait également été. En revanche, une inversion
de la taille relative du filament n’avait pas complètement inversé le succès des mâles. Ce
résultat suggère soit que d’autres traits corrélés au filament sont potentiellement importants,
soit que sous un certain seuil de longueur de filament, la taille du filament n’a plus
d’importance dans l’accès à la reproduction. Nos résultats ont également montré que la parade
est un élément déterminant pour expliquer l’accès à la reproduction. En effet, les mâles qui
avaient une activité de parade plus importante avaient un meilleur accès à la reproduction.
Ainsi nous montrons pour la première fois chez un urodèle l’importance conjointe des
traits morphologiques et comportementaux dans le cadre du choix de partenaire.
II. 3. Etude de la parade du triton palmé. [article 3]
Dans l’étude précédente, nous avons montré que l’accès à la reproduction des mâles était
partiellement lié à la variation dans leur temps de parade (article 2). Bien que moins étudiée,
la variation individuelle dans le temps de parade n’en est pas moins importante (Bell et al.
2009). La question est alors de savoir si les comportements de parade sont constants dans le
temps et donc répétables entre les individus. De nombreuses études ont montré que les
comportements de parade des mâles sont globalement répétables mais cette répétabilité reste
souvent assez faible, une grande partie de la variation restant inexpliquée (Bell et al. 2009).
Des études récentes mettent en avant que cette faible constance des comportements de parade
pourrait être due à une forte labilité en fonction des situations et notamment des
caractéristiques des femelles (Ruiz et al. 2008, Lehtonen et al. 2011). En effet, alors qu’un
triton palmé mâle ne peut pas ajuster la taille de son filament en fonction de la femelle qu’il
rencontre, il peut ajuster son comportement de parade. Ainsi, un mâle donné pourrait choisir
de parader peu pour une femelle qu’il juge de mauvaise qualité afin, par exemple, de limiter
ses dépenses énergétiques. Cependant peu d’études se sont intéressées à l’importance relative
de l’identité des mâles et des femelles sur la variation des comportements de parade
(Lehtonen et al. 2011).
A notre connaissance une seule étude a étudié la répétabilité des comportements de
parade chez les tritons (Michalak 1996, voir Wells 2007 et Bell et al. 2009). Cette étude a
montré que, globalement, les comportements des mâles ne sont pas répétables (Michalak
1996). Nous avons donc examiné l’importance relative de l’identité des mâles et des
femelles et nous avons testé l’influence relative des caractéristiques du mâle et de la
femelle sur la variation dans les comportements de parade tels que les éléments de la
parade statique, les comportements trembler (quiver) et touche queue (touch tail) (Figures 3
et 4). Pour cela nous avons mis en place un protocole expérimental où le comportement de
chaque individu (mâle et femelle) était mesuré trois fois, avec un intervalle d’un jour puis de
quatre jours. Nous avons mis en évidence que le temps passé en parade statique était en partie
expliqué par l’identité du mâle et pas du tout expliqué par l’identité de la femelle. Les
comportements de trembler (quiver) semblaient être expliqués à la fois par l’identité du mâle
et de la femelle. Enfin les comportements de touche queue (touch tail) étaient uniquement
expliqués par l’identité de la femelle. Nous n’avons trouvé aucun lien entre les
comportements et les traits morphologiques, et ceci à la fois pour les mâles et les femelles.
Notamment, le temps de parade n’était pas lié à la taille du filament du mâle. De même, nous
n’avons pas trouvé de lien entre la constance dans les comportements de parade et les traits
morphologiques des mâles : les mâles de grande taille n’étaient pas plus répétables que les
mâles de petite taille. Contrairement à ce que les travaux de Michalak (1996) suggéraient,
nous avons montré pour la première fois chez un urodèle que les comportements de la
parade sont significativement répétables. Nous montrons également l’importance de
prendre en compte les caractéristiques des mâles et des femelles pour comprendre
l’expression des comportements de parade.
III. Signaux multiples, sélection sur le contenu et hétérogénéité de
l’environnement chez le triton palmé.
III. 1. Introduction.
Les signaux multiples, ainsi que les potentielles interactions entre les différents
signaux s’étudient en évaluant la réponse des femelles pour chaque signal pris séparément
ainsi que la combinaison de plusieurs signaux (Partan & Marler 1999, 2005, article 1). Bien
que les résultats de telles études soient nécessaires et extrêmement utiles pour comprendre
l’importance relative de chaque signal, ils ne renseignent pas directement sur l’information
véhiculée par les signaux (Hebet & Papaj 2005, tableau 1, article 1). Or, une grande partie
des hypothèses expliquant l’utilisation de signaux multiples reposent sur l’information
extraite par les femelles des traits des mâles (article 1). Møller & Pomiankowski (1993) ont
émis trois grandes hypothèses permettant d’expliquer l’évolution des signaux multiples qui
sont les signaux non-informatifs (les signaux ne sont pas liés à la condition des mâles), les
messages redondants (les signaux contiennent la même information sur la condition) et les
messages multiples (les signaux renseignent sur des aspects différents de la condition) (article
1). Une manière de tester le contenu informatif des signaux est d’évaluer leur conditiondépendance (Cotton et al. 2004). Nous avons réalisé des expériences, synthétisées sous la
forme de deux articles (article 4 et 5), dont le but était de mieux appréhender le rôle des
traits morphologiques et comportementaux en tant que signaux de qualité individuelle
chez le triton palmé.
III. 2. Condition dépendance des signaux multiples. [Article 4].
Dans cette expérience nous avons testé les hypothèses de Møller & Pomiankowski (1993)
sur l’évolution du filament, des palmures, de la crête et de la parade chez le triton
palmé. Pour tester ces hypothèses, nous nous sommes basés sur deux grands types de qualité
du mâle qui sont le statut immunitaire et la condition corporelle, un aspect peu étudié pour la
classe des urodèles. Si l’on se réfère à la synthèse de Cotton et al. (2004) sur la condition
dépendance, la seule preuve expérimentale de condition dépendance chez les amphibiens est
une expérience réalisée par Green (1991) chez le triton ponctué Lissotriton vulgaris. Dans
cette expérience Green (1991) a montré, en utilisant 14 tritons mâles, que les tritons du groupe
soumis à un stress de nourriture avaient une crête moins développée que le groupe contrôle de
tritons nourris. Il a aussi montré une relation positive entre la condition corporelle et la taille
de la crête sur 70 mâles capturés dans la nature (Green 1991). A ce jour et à notre
connaissance, il n’existe en revanche aucune étude ayant utilisé la réponse à un challenge
immunitaire comme indice de la qualité des mâles chez les urodèles.
Nous avons donc soumis des mâles à un challenge immunitaire afin de voir si leurs
traits sexuels étaient corrélés à leur statut immunitaire. Pour cela, nous avons injecté des
fragments de bactéries (LPS) connues pour activer le système immunitaire chez une grande
variété d’animaux. Nous avons également testé si les traits sexuels co-varient avec la
condition corporelle des mâles. Lors de cette expérience, nous n’avons mesuré aucun effet du
challenge immunitaire sur l’expression des traits sexuels. Une des explications possible à ce
résultat, et que ce protocole ne permet pas de vérifier, est que le traitement n’a pas activé le
système immunitaire des tritons. Cependant avec un protocole similaire d’injection, des
expériences précédentes ont montré que le système immunitaire des anoures était activé,
même si ce type de preuve n’existe pas chez les urodèles.
Nous avons mesuré une co-variation positive entre trois caractères sexuels (la taille du
filament, la surface de palmure, l’indice de développement de la crête), ainsi qu’une covariation positive de ces trois traits avec l’indice de condition corporelle des mâles. En
revanche la parade ne semblait aucunement liée à la condition corporelle du mâle.
Globalement nos résultats suggèrent que les traits morphologiques (filament, palmure,
crête) sont des signaux redondants de la qualité du mâle, renseignant sur la condition
corporelle des mâles. De son côté, la parade semble être un trait non informatif sur la
condition corporelle du mâle.
III. 3. Effet de l’hétérogénéité de l’environnement sur l’expression de signaux multiples
[Article 5].
Bien qu’elle soit encore relativement peu étudiée, l’hétérogénéité de l’environnement
peut avoir des effets importants sur la sélection sexuelle (Greenfield & Rodriguez 2004,
Cornwallis & Uller 2010). En particulier, l’hétérogénéité de l’environnement peut être un
facteur expliquant l’évolution du choix des femelles pour des signaux multiples (article 1,
Bro-Jørgensen 2010). Les signaux multiples pourraient ainsi permettre aux femelles de choisir
les meilleurs mâles dans des environnements fluctuants (article 1). En effet l’hétérogénéité de
l’environnement pourrait avoir un effet sur l’honnêteté des signaux, effet qui pourrait être
différent en fonction de la labilité des traits (Bro-Jørgensen 2010). Les traits phénotypiques
condition-dépendants indiquent la qualité des mâles au moment où ils sont produits. Lorsque
les traits sont relativement statiques il peut alors exister un écart important entre l’expression
du trait et la qualité de l’individu au moment de l’évaluation du trait. Par exemple alors que la
qualité des individus peut varier rapidement dans le temps et l’espace, l’expression de certains
traits morphologiques reste constante (Figure 6, Bro-Jørgensen 2010). Dans ce cas les traits
morphologiques indiqueraient la qualité du mâle uniquement au moment de leurs productions.
Lorsque l’environnement change les traits morphologiques peuvent ainsi devenir des signaux
non fiables de la qualité des mâles (Figure 6, Robinson et al. 2012). Dans ces cas, les
femelles devraient utiliser en priorité des signaux plus flexibles comme certains traits
comportementaux qui indiquent la qualité présente du mâle (Figure 6). Cependant ces traits
flexibles peuvent également être plus sensibles à un ajustement bref des mâles (notamment
en cas de variation dans la "motivation"). En effet les mâles pourraient investir fortement dans
l’expression de ces traits indépendamment de leur qualité afin d’accéder à la reproduction. Il
existe très peu de preuves empiriques de ces hypothèses (Bro-Jørgensen 2010 mais voir
Scheuber et al. 2003a,b, Whattam & Bertram 2011) particulièrement dans le cadre de
changements d’environnement (Candolin & Wong 2012).
Nous avons ici testé cette hypothèse chez le triton palmé, une espèce où à la fois les
traits morphologiques et comportementaux sont importants pour expliquer l’accès à la
reproduction (article 2). Pour cela, nous avons soumis des mâles à quatre traitements
différents suivant un plan factoriel. Nous avons créé une hétérogénéité de l’environnement en
faisant varier la disponibilité en nourriture. Les mâles ont été soumis à un traitement de quatre
semaines avec deux traitements de nourriture (présence ou absence) suivi d’une semaine de
traitement de nourriture (présence ou absence).
1
Environnement
2
b)
Expression du trait
Qualité du mâle
Expression du trait
Qualité du mâle
a)
1
Environnement
2
Figure 6. Expression du phénotype (trait sexuel et qualité associée au trait) sur des
traits multiples a-trait statique, b-trait dynamique. Le trait plein représente une qualité I
associé à un trait I, le trait en tiret représente une qualité II associé à un trait II. Dans les deux
cas a et b la qualité des mâles change suivant l’environnement. En a- l’expression du trait ne
suit pas la qualité du mâle (signaux statiques). En b- l’expression du trait suit la qualité du
mâle (signaux dynamiques).
Notre première prédiction était que lorsque la disponibilité en nourriture varie
rapidement (changement d’environnement) les traits comportementaux de parade devraient
indiquer la qualité du mâle dans le nouvel environnement et non la qualité du mâle dans son
précédent environnement. A l’inverse, les traits morphologiques devraient refléter la
condition environnementale lors de leur production du fait de leur faible labilité. Notre
seconde prédiction était que dans les environnements stables, le succès des mâles devrait être
expliqué par les traits morphologiques dû à un choix de la femelle pour ces traits qui seraient
alors plus informatifs tandis que dans les environnements fluctuants les traits
comportementaux devraient être favorisés.
En accord avec notre première prédiction, nos résultats montraient que les traits
morphologiques étaient relativement fixes et pouvaient indiquer la qualité passée du mâle
mais ne prédisaient pas sa qualité présente. Ceci était vrai pour des changements relativement
brefs. Par contre sur des pas de temps plus importants, les traits morphologiques semblaient
être plus flexibles et pourraient constituer de bons indicateurs de la qualité du mâle. Le
comportement de parade "trembler" (quiver) était relativement flexible et influencé par la
condition présente du mâle. Nous avions trouvé que les comportements de parade statique
étaient constants dans le temps (répétables) dans des conditions stables de laboratoire (article
3). Contrairement à notre première prédiction, les comportements de parade statiques n’ont
pas été impactés par la variation de la disponibilité en nourriture et semblaient donc
relativement fixes. L’ensemble de ces éléments suggère que les traits comportementaux
pourraient être fixés génétiquement et peu coûteux à produire. En accord avec notre deuxième
prédiction, nous avons montré que les traits morphologiques étaient contre sélectionnés en
milieu fluctuant, mais curieusement n’étaient pas sélectionnés en environnement stable. Les
traits comportementaux étaient sélectionnés quelque soit l’environnement. Globalement nos
résultats montrent que l’hétérogénéité de l’environnement peut avoir des impacts sur le
choix du partenaire pour des signaux multiples en impactant la condition dépendance
des traits.
IV. Conclusion générale
L’objectif général de cette thèse était l’étude des signaux multiples dans le cadre du
choix du partenaire sexuel. Dans une première partie, nous avons réalisé une synthèse sur les
signaux multiples dans le cadre du choix du partenaire. Cette synthèse nous a servi à établir
nos hypothèses de travail (article 1). Dans une deuxième partie, nous avons étudié comment
les ornements du mâle pouvaient influencer le choix des femelles chez le triton palmé
(articles 2 et 3). Enfin dans une troisième partie, nous avons étudié le rôle des signaux
multiples en tant que signaux de qualité individuelle (articles 4 et 5).
IV. 1. Choix des femelles sur critères multiples
Il apparait que, chez le triton palmé, l’accès à la reproduction est en grande partie expliqué
par des traits morphologiques telle que la longueur du filament et des paramètres
comportementaux tels que le temps passé en parade et le nombre de "trembler" (articles 2 et
5). Nos travaux de thèse contribuent à étayer l’hypothèse selon laquelle ces deux types de
traits contribuent grandement à l’accès à la reproduction chez les tritons (Wells 2007). Bien
que la parade semblait fixe pour un individu donné (article 3 mais voir article 5), elle n’était
pas révélatrice de la qualité du mâle évaluée par la condition corporelle (article 4 et 5). Les
expressions des traits morphologiques (longueur du filament, surface de palmure et surface de
la crête) étaient positivement corrélées entre elles (articles 2, 4 et 5). De plus les traits
morphologiques co-variaient positivement avec la qualité du mâle toujours mesurée par la
condition corporelle (articles 4 et 5). Cela confirme l’hypothèse d’une condition dépendance
des ornements chez les tritons en ajoutant un nouvel exemple avec une nouvelle espèce. En
effet, il n’existait auparavant que deux exemples : le triton crêté Triturus cristatus (Baker
1992) et le triton vulgaire Lissotriton vulgaris (Green 1991). Globalement chez le triton palmé
l’accès à la reproduction est expliqué par des traits multiples composés de traits
morphologiques et comportementaux et seuls les traits morphologiques sont révélateurs de la
condition du mâle (Figure 7).
TRAIT
INFORMATION
crête
palmure
condition corporelle
filament
taille corporelle
*
?
coloration
parade
Figure 7. Association entre les traits potentiellement utilisés par les femelles pour choisir
leurs partenaires sexuels et l’information contenue dans ces traits. Les flèches en tiret continu
représentent les traits qui influencent le choix des femelles. Les flèches en tiret représentent
les traits dont l’influence sur le choix n’est pas avérée. * D’après Haerty et al. (2007).
Cette première conclusion de nos travaux montre que les signaux multiples peuvent être
vus comme une mosaïque de traits regroupant à la fois des signaux de type non fiables,
redondants et multiples, le tout au sein d’une même espèce (Figure 7, Doucet &
Montgomerie 2003). Cela montre que les différentes hypothèses expliquant l’évolution des
signaux multiples ne sont pas mutuellement exclusives (article 1). Les travaux sur les signaux
multiples chez le triton palmé étant encore très minces, et cette thèse étant le début d’un projet
sur les signaux multiples, il convient maintenant de les compléter par l’ajout d’autres signaux
potentiellement sélectionnés par les femelles (développés plus en détail dans la partie
perspective).
Nos résultats peuvent également être interprétés dans le cadre du conflit sexuel. En effet
les bénéfices divergent souvent entre les mâles et les femelles lorsqu’il s’agit de reproduction
(Box 1). Alors que les mâles sont sélectionnés pour accéder aux femelles, les femelles sont
sélectionnées pour choisir les meilleurs mâles (Font & Carazo 2010). Il est possible que la
parade ait évolué comme moyen utilisé par les mâles pour accéder aux femelles alors que les
ornements (comme le filament) aient évolué comme moyen utilisé par les femelles pour
choisir le meilleur mâle (articles 2, 5, Figure 8). Bien que le conflit sexuel puissent expliquer
l’existence de signaux multiples (Holland & Rice 1998, Lozano 2009) les preuves sont
relativement minces (Candolin 2003). Chez les tritons la complexité de la parade semble avoir
co-évolué avec le degré d’expression des ornements (Wiens et al. 2011). Cependant les traits
comportementaux ne sont peut être pas sans lien avec la qualité du mâle (Figure 8). En effet
il convient maintenant de tester quels autres types d’information peuvent être contenus dans
les signaux (en dehors de la condition corporelle). La parade et les ornements pourraient être
liés à la qualité immunitaire du mâle, les réserves en spermatophores, l’âge, les conditions
durant l’ontogénèse… etc. (article 4). Cela permettrait de compléter la "carte du choix du
partenaire" pour des signaux multiples élaborée au cours de cette thèse (Figure 7).
Mâle « motivé »: une information sur la qualité ?
Traits
comportementaux
« influencer la femelle », « manipulation »
morphologiques
« Extraction d’information »
Figure 8. Interprétation de l’effet des traits comportementaux et morphologiques sur le choix
des femelles en lien avec le conflit sexuel.
Les colorations font parties des traits souvent utilisés par les femelles dans le cadre du
choix du partenaire et elles sont largement utilisées dans le cadre des signaux multiples
(article 1). L’examen d’un rôle de la coloration comme un critère du choix du partenaire chez
les amphibiens connait d’ailleurs un certain succès ces dernières années (Rosenthal et al.
2004, Vasquez & Pfennig 2007, Maan & Cumming 2009, Gomez et al. 2009, 2010, 2011a,b,
Doucet & Mennill 2010, Richardson et al. 2010, Sztatecnsy et al. 2010). Chez les amphibiens,
la coloration orangée est généralement produite par des pigments caroténoïdiques (Richardson
et al. 2009) ou des ptérines. Il est reconnu que ces deux pigments (caroténoïdes et ptérines)
jouent un rôle important dans les fonctions immunitaires, et que leur fonction antioxydante
permet une protection des cellules contre les radicaux-libres. Or, les ptérines sont synthétisées
par l’organisme tandis que les animaux ne peuvent pas synthétiser les caroténoïdes et doivent
donc les trouver dans leur alimentation. La disponibilité en caroténoïdes n’étant pas infinie,
les mâles font face à un compromis entre une allocation pour des signaux colorés ou une
allocation pour le bien être de leur organisme (Baeta et al. 2007). Il a donc été proposé que les
mâles pouvant se permettre d’allouer une forte quantité de caroténoïdes dans leur trait sexuel
devaient être des mâles de bonne qualité (Faivre et al. 2003). Dès lors, les femelles devraient
baser leur choix sur des mâles très colorés (Hill 2006). Nos résultats montrent au contraire
que la coloration n’est pas un critère important chez le triton palmé et ce résultat est confirmé
par d’autres études (Secondi et al. 2012, Théry communication personnelle, article 2). Durant
cette thèse nous avons réalisé une autre expérience, non présentée dans ce manuscrit, visant à
comprendre plus finement le rôle potentiel de la coloration. Dans un dispositif tel que celui
décrit dans l’article 2, nous avions proposé à des femelles le choix entre des mâles très orangé
et des mâles blanchâtres. Les résultats de cette seconde expérience ne nous permettent pas de
proposer une conclusion car aucun des protagonistes ne semblait réceptif, nous n’avons
mesuré aucune prise de spermatophore et nous avons observé seulement un très faible nombre
d’événements de parade. Même si nos premiers résultats ne suggèrent pas un rôle
prédominant de la coloration (article 2), il conviendrait peut être de réaliser une expérience
manipulant l’apport en caroténoïdes chez les mâles afin d’explorer l’impact de cette
manipulation sur leur coloration et le choix des femelles. En effet, un apport d’antioxydants
sous forme de caroténoïdes pourrait améliorer l’état de santé général des individus et ceci
pourrait être perçu par les femelles, même en l’absence d’impact visible sur la coloration
individuelle, par des indices olfactifs par exemple.
IV. 2. Prise en compte de l’hétérogénéité de l’environnement
La prise en compte de l’effet de l’hétérogénéité de l’environnement sur la sélection sexuelle
est relativement récente, particulièrement dans le cadre des signaux multiples (Cornwallis &
Uller 2010, Candolin & Wong 2012, article 1). Les conclusions développées dans le
paragraphe précédent ainsi que la Figure 7 doivent être interprétées dans un cadre dynamique
car le choix des femelles et la condition dépendance des traits sexuels peuvent varier aussi
bien en direction qu’en intensité (articles 1, 2 et 5). Ainsi le choix des femelles semblaient
potentiellement variable. Alors que les résultats des expériences présentées dans l’article 2
montrent que le succès des mâles dépendait grandement de la taille de leur filament, les
résultats de l’expérience réalisée pour l’article 5 montrent que le filament ne prédisait pas ou
prédisait inversement le succès des mâles. L’ensemble de ces éléments suggère que le choix
des femelles peut varier spatialement et/ou temporellement. Ainsi, plusieurs paramètres de
l’environnement pourraient causer cette variation, telles que la prédation, la disponibilité des
mâles, la sex ratio opérationnelle ou la qualité de l’habitat (Ah-King 2010). Le choix du
partenaire pourrait également varier suivant des facteurs internes propres à la femelle tels que
sa taille, son statut parasitaire, sa condition, son âge ou son expérience passée (Ah-King
2010). Ces paramètres influant le choix du partenaire ont souvent été identifiés sur la base
d’un critère unique, mais ont rarement été pris dans un contexte de signaux multiples (article
1).
Dans cette thèse nous avons également montré que lors d’un changement rapide de la
qualité de l’environnement (comme la disponibilité en nourriture), les traits morphologiques
pouvaient perdre leurs liens avec la condition corporelle du mâle. Nous montrons ainsi, à
travers les résultats présentés dans l’article 5, l’importance de l’environnement sur un élément
phare en sélection sexuelle : la condition dépendance des traits sexuels. L’article 5 donne des
résultats contrastés quant à l’effet de l’hétérogénéité de l’environnement sur la condition
dépendance des traits sexuels. En effet sur une échelle aussi courte qu’une semaine, les
ornements peuvent perdre leur lien avec la condition. Cependant sur une échelle plus longue
d’un mois, il semble que le lien entre traits sexuels et qualité du mâle puissent être rétabli.
Cela met en avant l’importance de l’échelle temporelle dans l’étude de la sélection
sexuelle (Cornwallis & Uller 2010).
Dans la continuité de l’article 5, il serait intéressant de reproduire une expérience
similaire à celle que nous avons réalisée mais où les traitements expérimentaux viseraient à la
fois les mâles et les femelles. Ainsi les femelles seraient également assignées à des
environnements différents et variables (contrairement à l’article 5 où seuls les mâles
subissaient le traitement expérimental). Cette expérience permettrait de comprendre en quoi
l’hétérogénéité de l’environnement affecte également le choix des femelles. Les tritons vivent
dans des habitats très différents au cours de l’année (terrestre puis aquatique). Ces habitats
peuvent présenter des sources de stress et des pressions de sélection très variables pour les
tritons en termes de qualité/quantité de nourriture et autres types de stress. Dans notre
expérience, nous avons constaté que les conditions initiales (proches de la phase terrestre)
pouvaient influencer l’expression des traits sexuels (article 5). Il serait dès lors très intéressant
de tester l’effet de la phase terrestre ainsi que de la phase aquatique sur l’expression des traits
sexuels, la condition dépendance des traits sexuels et le choix des femelles (Figure 9).
Nourriture +
Nourriture +
Nourriture -
Nourriture -
Nourriture +
Nourriture -
Mesure du choix
des femelles
Phase aquatique
Mesure des
traits des mâles
Phase terrestre
Figure 9. Design expérimental pour l’étude de l’effet de l’hétérogénéité de l’environnement
sur le choix des femelles et la condition dépendance des traits sexuels chez les mâles tritons
palmés.
IV. 3. Paradoxe du lek et conséquences sur les processus de sélection
La prise en compte de l’effet de l’hétérogénéité de l’environnement sur le choix du
partenaire peut avoir des conséquences importantes sur le maintien de la variation
phénotypique et de la variabilité génétique observées dans la nature (Greenfield et al. 2012).
Or, la variation sur un trait est une des trois conditions nécessaire pour qu’il y ait sélection
sexuelle et donc évolution des ornements (introduction partie a). Le maintien de la variation
est source de nombreux débats notamment concernant l’évolution de la préférence des
femelles pour des bénéfices indirects et entourant le « paradoxe du lek » (Kokko et al. 2003).
Le paradoxe du lek provient de la situation où les femelles choisissent leur(s) partenaire(s)
uniquement sur la base d’un trait unique corrélé à la qualité génétique de ceux-ci, où les
bénéfices des femelles sont indirects et où la force de préférence co-varie avec la quantité de
variation génétique entre les mâles. Pour une espèce répondant à ces critères, plus la
préférence des femelles est forte, plus le bénéfice est important en terme de fitness, mais plus
la variation en terme de qualité génétique sera faible à la génération suivante (Kokko et al.
2003, Tomkins et al. 2004, Bussière et al. 2008). Il en découle que la sélectivité est diminuée
au fur et à mesure des générations successives. Au final, la variation génétique qui favorise
la préférence des femelles est diminuée par cette préférence (Tomkins et al. 2004) et
devrait tendre à disparaître, d’où le paradoxe. La variation dans le choix des femelles tout
comme la variation dans l’honnêteté du signal peut réintroduire de la variation et contribuer à
résoudre le paradoxe (Bussière et al. 2008). En effet, selon l’environnement, les femelles vont
être plus ou moins sélectives et donc choisir les mâles de plus ou moins bonne qualité
(Greenfield & Rodriguez 2004). De plus, l’honnêteté des traits peut varier selon les
environnements, ce qui conduit les femelles à plus ou moins se tromper dans la quête du mâle
de meilleure qualité (Greenfield & Rodriguez 2004). En conséquence, l’hétérogénéité de
l’environnement réduit la manière dont le choix des femelles peut éroder la variation. Il
pourrait être intéressant d’examiner si les populations naturelles faisant face à des
environnements fluctuants possèdent des variations génétiques plus importantes que les
populations établies en milieu stable.
Dans cette thèse, nous avons établi que l’honnêteté des traits peut être plus ou moins
forte suivant les environnements et que les femelles ne choisissent pas forcement toujours les
mâles de meilleure qualité (articles 1 et 5). Nous avons mesuré que, sur une échelle d’une
semaine, les changements dans les conditions environnementales pouvaient impacter la
qualité des mâles sans impacter les traits sexuels, diminuant ainsi la condition dépendance et
donc l’honnêteté des ornements des mâles (article 5). En conséquence, nos expériences
suggèrent que, chez le triton palmé, la variation peut être maintenue par les variations dans le
choix des femelles ainsi que par les variations dans l’honnêteté des traits. Sur une échelle de
temps d’un mois, il semble que l’environnement puisse moduler la qualité des mâles sans
pour autant changer la condition dépendance des traits (article 5). En d’autres termes, même
si les femelles utilisent toujours le même trait sexuel pour faire leur choix et que celui-ci est
condition dépendant, la variation peut être maintenue car ce ne sont pas les mêmes individus
qui sont sélectionnés selon l’environnement.
IV. 4. Conséquences au niveau populationnel
La prise en compte de l’effet de l’hétérogénéité de l’environnement sur le choix du
partenaire peut avoir des conséquences au niveau populationnel. En effet, la variabilité du
choix des femelles et la variabilité de l’honnêteté des ornements (article 5) montrent que l’on
peut passer rapidement d’un modèle d’évolution de la préférence des femelles à un autre
(Tableau 1). Par exemple, le fait qu’un trait puisse être condition dépendant dans un
environnement et pas dans un autre (article 5) montre que l’on peut passer d’un modèle de
trait dit "informatif" à un modèle de trait dit "non-informatif" (Tableau 1). Or, ces modèles
ne reposent pas sur les mêmes hypothèses et n’ont pas non plus les mêmes conséquences
au niveau populationnel (Jones & Ratterman 2009). Il est couramment admis que la
sélection sexuelle a un coût pour la population car l’investissement dans les traits sexuels peut
se faire au détriment de la survie (Doherty et al. 2003). En effet l’énergie investie dans les
ornements ne peut être allouée pour d’autres traits et les ornements peuvent augmenter les
risques de prédation (Andersson 1994). Cependant, suivant les modèles d’évolution de la
préférence des femelles (Jones & Ratterman 2009), la sélection sexuelle pourrait aussi fournir
des bénéfices au niveau populationnel (Candolin & Wong 2012). Les modèles reposant sur
des traits dits informatifs peuvent avoir pour effet d’augmenter la fréquence des individus de
bonne qualité à l’intérieur de la population, et ce par le choix des femelles, ce qui peut avoir
pour conséquence d’augmenter la viabilité des populations (Møller & Alatalo 1999,
Jarzebowska & Radwan 2010, Candolin & Wong 2012). De plus, le coût supposé des traits
sexuels (notamment selon le principe du Handicap) et le choix des femelles peuvent permettre
l’élimination des individus les moins bien adaptés à l’environnement, laissant plus de
ressources aux individus restants (Candolin & Wong 2012). Dans nos expériences, les traits
morphologiques semblent être de tels traits (article 4 et 5).
Au contraire, les modèles basés sur des traits dits non-informatifs prédisent des
conséquences différentes à l’échelle de la population car ils ne stipulent pas que les femelles
choisissent les mâles de meilleure qualité. Les traits comportementaux chez le triton palmé
semblent être non-informatifs (articles 4, 5). Certains modèles, tel que le conflit sexuel,
(chapitre IV. 1) dans lesquels les mâles et les femelles ont des intérêts reproductifs divergents,
où certains traits sexuels mâles imposent un coût accru aux femelles et où certains gènes sont
favorables seulement à l’un des deux sexes pourraient même avoir des conséquences
négatives sur la population (Candolin & Wong 2012). En effet, ce qui est favorable au niveau
individuel ne l’est pas forcement pour la population. Or les mâles et les femelles sont
sélectionnés pour maximiser leur propre succès reproducteur, et par exemple pour influencer
la femelle contre le choix du meilleur mâle (Box 1, Figure 1 et 8). En favorisant l’utilisation
de traits non-informatifs attractifs pour les femelles (dans notre cas les comportements de
parade), la sélection sexuelle peut empêcher les femelles d’utiliser les meilleurs critères pour
choisir leur partenaire (dans notre cas les traits morphologiques). Ceci pourrait conduire à une
tragédie des communs où les bénéfices individuels conduisent à des conséquences tragiques
pour la population (Rankin et al. 2011). Cependant les conséquences populationnelles de la
sélection sexuelle restent encore sujettes à caution (Candolin & Heuschele 2008). En effet ces
conséquences dépendent grandement des modèles d’évolution de la préférence des femelles
dont les frontières semblent floues au vu de nos résultats et des récents travaux sur l’effet de
l’hétérogénéité de l’environnement sur la sélection sexuelle (Cornwallis & Uller 2010,
articles 1 et 5).
IV. 5. Conséquences pour la biologie de la conservation
Une question d’actualité en biologie de la conservation est l’adaptation des animaux aux
changements environnementaux. Nos résultats montrent une certaine résistance des tritons
aux pressions de l’environnement car même exposés à un environnement défavorable, les
tritons semblent pouvoir se reproduire (article 5). Cependant, nos résultats montrent que des
changements environnementaux peuvent affecter les processus de sélection sexuelle,
notamment la fiabilité des traits (article 5). Cela pourrait rendre le choix du partenaire mal
adaptatif (article 5) pouvant conduire à des problèmes au niveau populationnel (chapitre IV. 3
et IV. 4). Chez les épinoches à trois épines Gasterosteus aculeatus, la pollution entraîne une
diminution de la qualité de l’eau qui elle-même engendre une visibilité réduite. Cela a pour
effet de diminuer la compétition entre les mâles et l’honnêteté des signaux comportementaux
(Wong et al. 2007). Pour qu’un choix qui était adaptatif dans un environnement donné
continue d’être adaptatif dans un nouvel environnement, il faut que les femelles basent leurs
choix sur un critère de la qualité du mâle qui demeure fiable dans ce nouvel environnement.
Dans notre expérience le trait sélectionné par les femelles (i.e., le comportement de parade) ne
semble pas indiquer la condition du mâle (article 2, 4 et 5). Un changement d’environnement
pourrait donc avoir des conséquences négatives pour la population (Candolin & Wong 2012).
Cependant une autre possibilité est que l’honnêteté du trait s’ajuste rapidement au
nouvel environnement par plasticité. Par exemple, dans notre expérience, bien que la
condition dépendance des traits morphologiques puisse diminuer suite à un changement
d’environnement rapide, elle semble pouvoir se rétablir sur un temps un peu plus long (article
5). Cela contraste avec les résultats obtenus chez le mouton Ovis aries et chez le Gobemouche
à collier Ficedula albicollis, où les ornements ne co-variaient pas avec la qualité du mâle
(Robinson et al. 2007, 2012). Nos résultats demandent cependant à être confirmés par une
étude à plus long terme (Figure 9) et également par des mesures en milieu naturel.
Les
maladies
émergentes
peuvent
être
comptées
parmi
les
changements
environnementaux qui impactent les populations (Daszak et al. 2000, Smith et al. 2009, Fisher
et al. 2012). Chez les amphibiens, le champignon pathogène Batrachochytrium dendrobatidis
est responsable d’une maladie infectieuse émergente, la chytridiomycose, susceptible de
modifier la dynamique des populations (Fisher et al. 2012). Depuis sa découverte en 1998, la
chytridiomycose a été identifiée comme l’une des causes du déclin mondial des populations
d’amphibiens (Fisher et al. 2012). Les résultats de cette thèse peuvent apporter des pistes de
réflexion importante sur ce sujet. Par exemple, nous montrons que le choix des femelles
tritons est, sous certaines conditions, basé sur des traits reflétant la qualité du mâle (article 2,
4 et 5). Or, comme nous l’avons décrit précédemment le choix du partenaire pourrait agir
comme un effet de purge en éliminant les génotypes mal-adaptés (chapitre IV. 4). Nos
résultats laissent penser que les ornements reflètent la qualité du mâle chez le triton palmé
(articles 4 et 5). Ils pourraient donc potentiellement refléter la résistance à la chytridiomycose.
Les individus n’étant pas tous résistants de la même façon à la maladie (Kilpatrick et al.
2010), les génotypes résistants pourraient être favorisés par le choix des femelles ce qui peut
avoir des effets positifs pour la population (Candolin & Heuschele 2010, Rankin et al. 2011).
Cependant nous avons clairement montré que, chez cette espèce, le choix du partenaire est
également basé sur des traits non informatifs (i.e., le comportement parade, articles 2 et 5), ce
qui limiterait fortement un éventuel effet de purge (Candolin & Heuschele 2010). En effet,
nos expériences ont révélé que les mâles de moins bonne qualité pouvaient accéder à la
reproduction aussi bien que les mâles de meilleure qualité (article 5). Des expériences doivent
donc maintenant établir le lien entre chytridiomycose, qualité des mâles, expression des traits
sexuels et succès reproducteur.
Nos résultats montrent également que l’hétérogénéité de l’environnement peut
impacter la condition dépendance des traits et l’importance des critères morphologiques dans
l’accès au femelles (article 5). Une conséquence est que l’hétérogénéité de l’environnement
réduit la manière dont le choix des femelles peut éroder la variation (chapitre IV. 3). Or la
variation est une composante essentielle de l’adaptation à des changements environnementaux
par sélection naturelle. Dans le cadre de la chytridiomycose, il a été montré que les
populations présentant une variation génétique plus importante étaient plus à même de résister
à la maladie (Luquet et al. 2012). Il est donc possible que les populations faisant face à des
environnements fluctuants résistent mieux à l’arrivée d’une maladie émergente telle que la
chytridiomycose.
Enfin, les amphibiens sont des espèces menacées notamment par les changements
environnementaux et les des maladies émergentes (Stuart et al. 2004, Fisher et al. 2012). Une
attention particulière doit donc être attribuée aux populations naturelles, notamment par un
suivi précis de leurs abondances et de leurs qualités. Ceci peut être réalisé à travers des suivis
de population ou des études d’impact lors de changement d’origine anthropique. Les résultats
de cette thèse suggèrent à travers la condition dépendance des traits morphologiques (article 4
et 5) que des paramètres tels que les ornements peuvent être pris en compte pour juger
de la qualité d’une population (Hill 1995). Par exemple, le suivi des ornements des mâles a
été utilisé comme indicateur de la qualité des mâles dans le cadre de pollution lié aux marées
noires (Pérez et al. 2010). Pérez et al. (2010) ont en effet mesuré que la pollution liée aux
marées noires avait des impacts sublétaux sur les mâles pouvant être mesurés à travers
l’expression des ornements. Chez les tritons palmés, il a été montré que l’expression des
ornements était liée à la qualité de l’environnement en termes de turbidité (Secondi et al.
2007), concentrations en nitrates (Secondi et al. 2009) et disponibilité en ressources
alimentaires (article 5). Des suivis, comprenant la mesure des ornements comme indicateur
d’effet sublétal, pourraient être très utiles dans le cadre des études sur l’impact de la
chytridiomycose sur les populations d’amphibiens. Ceci est également vrai pour les études
d’impacts réalisées dans le cadre des suivis de population suite à des pressions d’origine
humaine.
IV. 6. Perspectives
Il existe de nombreuses perspectives à cette thèse. Certaines perspectives ont déjà été
développées dans les chapitres précédents. Par exemple il conviendrait de compléter la carte
du choix des femelles en ajoutant des traits potentiellement préférés par les femelles et les
informations potentiellement véhiculées par ces traits (Figure 7). En outre, il serait nécessaire
de poursuivre le travail sur l’effet de l’hétérogénéité de l’environnement sur la sélection
sexuelle (chapitre IV. 1 à 5, Figure 9). J’ai développé ici sous forme d’une liste quelques
autres perspectives pouvant faire suite à ce travail de thèse.
Les critères relatifs, telle que la compatibilité génétique, peuvent être extrêmement
importants pour expliquer le choix des femelles. En effet, deux études montrent que
les femelles exerceraient un choix pour des individus les moins apparentés chez le
triton alpestre Ichthyosaura alpestris et le triton ponctué Lissotriton vulgaris (Garner
& Schmidt 2003, Jehle et al. 2007). Or, nous ignorons ce qu’il en est chez le triton
palmé. De plus, le rôle de l’information chimique semble important chez les urodèles
et nous savons que la compatibilité génétique peut être évaluée en jugeant des odeurs
(Denoël 1999, Aeschlimann et al. 2003, Milinski et al. 2005, Houck 2009). Un axe de
recherche très intéressant pourrait être d’examiner l’existence d’une signature
individuelle des composés chimiques des mâles. Une première étape pourrait être de
réaliser un échantillonnage, sur différentes populations de tritons palmés, de composés
chimiques afin de voir s’il existe un effet population, sexe, et pourquoi pas individuel
sur la variation des composés chimiques. Cette technique prometteuse a déjà été
utilisée sur des modèles oiseaux et mammifères (Bonadonna et al. 2007, Scordato et
al. 2007) et pourrait apporter des réponses pertinentes quant aux choix des femelles
sur des critères chimiques.
Enfin, l’effet de l’information sociale sur le choix du partenaire n’a jamais été testé
chez les amphibiens. Pourtant que ce soit pour les anoures formant des cœurs ou les
urodèles tels que le triton palmé, les rencontres entre mâles et femelles se déroulent
souvent sur des sites où les femelles ont l’opportunité d’observer le choix d’autres
femelles et donc de collecter des informations sociales qui pourraient influencer leurs
choix.
Les théories sur le choix du partenaire font généralement le présupposé que les
femelles sont capables de classer les différentes options présentées sur une échelle de
valeur. Il est attendu que les femelles soient rationnelles dans leur choix. Or ce
présupposé n’a fait l’objet que de peu d’études dans le contexte du choix du partenaire
(Ryan et al. 2007). Le choix pour la taille du filament chez le triton palmé peut être un
moyen de tester ce présupposé. Pour cela l’étude de la répétabilité, de la transitivité et
de la répétabilité de la transitivité du choix peut être mise en place dans un design
similaire à l’article 2.
La théorie des signaux multiples, comme toute théorie évolutive, repose sur le
caractère adaptatif (en terme de fitness) de l’utilisation des signaux multiples par
rapport à l’utilisation d’un signal unique de communication (article 1). Or ce caractère
adaptatif est rarement testé et démontré. Dans cette thèse, nous n’avons pas réalisé de
mesure directe de la fitness (nombre de descendants viables et fertiles) de nos tritons.
Ceci pourrait être réalisé avec les tritons, ou de manière plus réaliste avec des animaux
à cycle de vie plus court.
Un volet très important dans le cadre de la théorie des signaux multiples est l’effet de
chaque signal pris indépendamment sur le choix de la femelle par rapport à l’effet de
l’ensemble des signaux combinés (article 1). Nous nous sommes approchés d’une telle
démarche dans l’article 2 mais les difficultés que nous avons rencontrées dans la
manipulation expérimentale du phénotype des individus font qu’il est difficile de tester
l’interaction des différents signaux sur le choix des femelles. Pourtant une telle
approche est cruciale pour comprendre comment les femelles jugent les traits
multiples tels que le filament, la crête, les palmures, la taille ou la parade.
Dans cette thèse, nous avons souvent abordé la notion de qualité des individus.
Comme nous l’avons dit, cette notion est relativement floue (Box 2). Dans cette thèse
nous avons utilisé l’indice de condition corporelle comme proxy de la qualité des
mâles. Cet indice semble d’ailleurs fiable comme indicateur de la disponibilité en
ressource alimentaire (article 5). Bien que cet indice soit couramment utilisé
notamment chez les amphibiens, il conviendrait de tester de manière plus approfondie
si un mâle en meilleure condition corporelle est effectivement un mâle de meilleure
qualité en termes de survie ou de fitness par exemple.
De même il conviendrait de tester la co-variation entre les traits sexuels et la qualité du
mâle en utilisant d’autre proxy de la qualité du mâle. Nous avons essayé d’utiliser
l’activation du système immunitaire sans réussite (article 4). En effet nous ne pouvons
pas affirmer que le système immunitaire de nos tritons a bien été affecté. De plus, nous
avons utilisé un antigène sans grande réalité évolutive. L’utilisation direct d’un
pathogène tels que la chytridiomycose, l’amphibiocystidium ou les bactéries
responsables des phénomènes de « red leg » pourraient être une piste de recherche très
intéressante.
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ARTICLES
Article 1………………………………………………………………………………..
Cornuau JH, Rat M, Schmeller DS, Loyau A. Complex love decisions: why and how
animals use several signals in mate choice. En préparation.
Article 2…………………………………………………………………………………
Cornuau JH, Rat M, Schmeller DS, Loyau A. 2012. Multiple signals in the palmate newt:
ornaments help when courting. Behavioral Ecology and Sociobiology, 66:1045-1055.
Article 3…………………………………………………………………………………
Cornuau JH, Courtoix EA, Jolly T, Schmeller DS, Loyau A. It takes two to tango : Do both
male and female identities influence complex courtship display in a newt species? En
préparation.
Article 4…………………………………………………………………………………
Cornuau JH, Pigeault R, Schmeller DS, Loyau A. Condition-dependance of multiple sexual
traits in the palmate newt (Lissotriton helveticus). En préparation.
Article 5…………………………………………………………………………………
Cornuau JH, Sibeaux A, Tourat A, Schmeller DS, Loyau A. Impacts of varying
environmental conditions on sexual traits and consequences for mate choice in the Palmate
newt. En préparation.
ARTICLE 1
Complex love decisions: why and how animals use
several signals in mate choice.
Cornuau JH, Rat M, Schmeller DS, Loyau A.
En préparation
1
Complex love decisions: why and how animals use several signals in mate choice?
2
3
Jérémie H. Cornuaua,*, Margaux Rata,b, Dirk S. Schmellera,c, Adeline Loyaua,c
4
5
a
Station d’Ecologie Expérimentale du CNRS à Moulis, 09200 Saint Girons, France.
6
b
Percy FitzPatrick Institute, DST/NRF centre of Excellence, University of Cape Town,
7
7701 Rondebosch, South Africa.
8
c
9
Biology, Permoser Strasse 15, 04138 Leipzig, Germany, both senior authors
Helmholtz Center of Environmental Research – UFZ, Department of Conservation
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* Correspondence: J.H. Cornuau, Station d’Ecologie Expérimentale du CNRS à Moulis,
12
09200 Saint Girons, France.
13
E-mail address: [email protected] (J.H. Cornuau)
14
15
Short title: Multiple signals and mate choice
16
1
17
Abstract:
18
Ten years after the first review about the multiple signal theory, this area of research
19
continues to be flourishing. Here we proposed to revisit and add current research on the
20
different hypotheses that explain the used of multiple signals focusing on mate choice
21
decision. We first proposed that compatibility and social information need to be more
22
included in the multiple signal theory. Then, we used recent examples that now give
23
experimental support to previous hypothesis, develop in previous reviews, in order to
24
understand why and how female used multiple signals to make their choice. Afterwards,
25
we highlighted current research, particularly the influence of heterogeneous environment
26
to explain the used of multiples signals in mate choice. We particularly focus on the
27
necessity to take account of both external and internal environment to explain why and
28
how female make their choice. Next we pointed conceptual issue which make different
29
hypothesis little distinguishable. We showed with example that the previous
30
categorizations of the hypothesis that explain the used of multiple signals are often more
31
blurred than previously described. Finally we discussed the necessity to incorporated
32
recent advance in cognitive ecology in the multiple signals theory. Indeed we think that
33
the multiple signals theory cannot be fully understood without a description of their
34
cognitive consequence. Globally this review, in supplement to previous review, provide a
35
comprehensible framework for scientist that want investigate why and how animal used
36
multiples signals in mate choice decision.
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Keywords: multiple signals, complex signals, multimodal, mate choice, animal
41
communication, information processing.
2
42
Introduction
43
Despite considerable advances over the last thirty years, the questions of why and
44
how animals make decisions about with whom to mate continue to puzzle behavioural
45
ecologists. Mate choice represents any pattern of behaviour, shown by members of one
46
sex, which leads to their tendency to mate non-randomly with respect to one or more
47
varying traits in members of the opposite sex (Halliday 1983, Heisler et al. 1987, Fig. 1).
48
As any other decision mechanism, mate choice involves costs in terms of signal
49
assessment, sorting and processing (Mery & Kawecki 2005). If costs associated to each
50
signal are additive (Roberts et al. 2007), overall costs may be higher when mate choice
51
involves multiple signals. In this case, selection should favour only one signal providing
52
the highest fitness benefits, i.e. an honest signal with a low assessment cost (Schluter and
53
Price 1993; Iwasa and Pomiankowski 1994, Fawcett & Johnstone 2003, but see
54
Johnstone 1995). However, it is now well established that females often base their choice
55
on multiple signals, and theories explaining the concomitant use of multiple signals for
56
mate choice are continuing to flourish (Guilford & Dawkins 1991, Møller &
57
Pomiankowski 1993, Rowe 1999, Candolin 2003, Hebets and Papaj 2005, Partan &
58
Marler 2005, Lozano 2009, Bro-Jørgensen 2010). These theories provide a strong
59
evolutionary framework allowing a better understanding of sexual preferences. They may
60
even contribute to resolve ongoing discussions about the lack of empirical evidence
61
and/or the apparent discrepancies sometimes found in studies of mate choice
62
(Roughgarden & Akçay 2010, Carranza 2010, Clutton-Brock 2010, Shuker 2010),
63
because where ones may see inconsistencies between studies, others see spatial and
64
temporal flexibility in mate choice in which a single, but different, signal is used each
65
year (Loyau et al. 2008, Chaine & Lyon 2008, Bro-Jørgensen 2010).
3
66
In this review, we propose to examine and discuss recent research on the issue of
67
multiple signalling in the context of mate choice. First, we point out the importance of
68
recently identified cues of mate choice, such as cues containing social information, and
69
we propose that social cues should be included in multiple signalling theories as any
70
other kind of signal. Second, we review different hypotheses put forward to explain the
71
evolutionary pressures underlying the evolution and maintenance of multiple signals in
72
mate choice. We particularly focused on recent theory that includes dynamic process of
73
selection. Third, we integrate multiple signals theory in the light of cognitive ecology.
74
Our aim is to provide a general and integrative framework for research on multiple
75
signals theory in the context of mate choice. For convenience, we will mostly refer to
76
female choice for male traits or signals, although mate choice occurs in both males and
77
females (Clutton-Brock 2007).
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79
SEXUAL SIGNALS USED IN MATE CHOICE
80
Since Darwin (1871), considerable efforts have been invested to identify traits and
81
signals used for mate choice and to understand how these traits and signals have been
82
selected and maintained by evolution (Andersson 1994, Gibson & Langen 1996,
83
Andersson & Simmons 2006). Various types of traits have been recognized, including (i)
84
morphological ornaments such as an elongated tail or vivid colours, (ii) behavioural traits
85
such as elaborate courtship displays or songs, and (iii) extended phenotypes like nest
86
construction (Andersson 1994, Schaedelin & Taborsky 2009, Byers et al. 2010, Cornuau
87
et al. 2012). Note that each of these traits may be a multi-component trait that can be
88
further unbundled into multiple signals, even though this level of complexity has been
89
poorly studied so far (examples for coloration: Grether et al. 2004, extended phenotypes:
90
Schaedelin & Taborsky 2009). Morphological traits, behavioural traits and extended
4
91
phenotypes are commonly included in the multiple signals framework, whereas choice
92
for mate compatibility (or heterozygosity) and social information are less considered.
93
Although, the consideration of relatedness, genetic heterozygosity and/or compatibility
94
have recently increased, as witnessed by several theoretical reviews (Zeh & Zeh 2003,
95
Neff & Pitcher 2005, Puurtinen et al. 2005, Mays et al. 2008, Roberts & Little 2008,
96
Puurtinen et al. 2009) the integration of this cue in a multiple cue framework has rarely
97
been done (Mays & Hill 2004). Only few studies of mate choice investigated the impact
98
of several signals including compatibility cues on mate choice decision (Mays & Hill
99
2004). These studies focus particularly on the potential conflict between choice for
100
compatible partner or choice for the most ornamented partner. Indeed it is expected that
101
the most compatible partner is on average not the most ornamented partner (Mays & Hill
102
2004). Thus it’s expected that animal should trade-off between this two traits. For
103
example in mice, although both mate choice for genetic compatibility and ornamental
104
quality occurs, genetic quality seems prefer only when available partner were similar in
105
ornament (Roberts & Gosling 2003). In the cichlid Pelvicachromis taeniatus females give
106
more importance to genetic compatibility than in ornament whereas the opposite was
107
found for males (Thünken et al. 2012). These two experiments show how compatibility
108
can be included in multiple signals theory.
109
110
Individuals can also gather social information by observing conspecifics interacting
111
with each others and use this information to make more accurate adaptive decisions
112
(McGregor 1993, Otter et al. 1999, Mennill et al. 2002, Danchin et al. 2004, Valone
113
2007). The use of social information in the context of mate choice can be broadly divided
114
into “eavesdropping” and “mate choice copying”. Females can “eavesdrop” on male-male
115
competitive interactions (such as song contests) to assess male quality and compare
5
116
potential partners (McGregor 1993, Otter et al. 1999, Mennill et al. 2002, Desjardins et
117
al. 2010). Females can also observe and then “copy” the choice of other females for a
118
given male or phenotype (Valone 2007). It is thought that copying or eavesdropper
119
individuals obtain information more easily and at lower costs, as it reduces the time they
120
spend looking for a mate (Templeton & Giraldeau 1996). Only few studies of mate
121
choice investigated the impact of several signals including social cues (Dugatkin 1996,
122
Dugatkin 1998). It is still unknown whether individuals would favour one type of
123
information (e.g. collected through eavesdropping) at the expense of another one (e.g.
124
observation of mate choice) and how choosy individuals deal with receiving
125
contradictory social information. So far, most research on social cues which considered
126
several signals, dealt with the respective roles played by private (non-social) versus
127
public (social) cues. For example, in the zebra finch Taeniopygia guttata, private
128
information (mate attractiveness manipulated using tarsus-band colours) can offset mate
129
choice copying (Drullion & Dubois 2008). This example demonstrates that social cues
130
should definitively be considered into multiple signals theories. The authors further stress
131
the importance of neural mechanisms and brain functions implied by mating choice, since
132
using social cues for mate choice is likely to require cognitive abilities such as learning
133
and memory.
134
135
FROM SEVERAL SIGNALS TO MULTIPLE SIGNALING
136
Møller & Pomiankowski (1993) pioneered the formulation of verbal models that
137
explain the used of multiple signals, by proposing three hypotheses based on the
138
information content in complex signals (content-based hypotheses sensus Guilford &
139
Dawkins 1991, Hebets & Papaj 2005, Table 1). First, the multiple message hypothesis
140
states that each trait provides particular information on the sender. Assessing several
6
141
signals thus provides several pieces of information about various aspects of the sender’s
142
location, species, sex, and quality (reviewed in Hebets & Papaj 2005). For example in the
143
field cricket Gryllus assimilis, song pulse rate honestly reflects juvenile condition
144
whereas dominant frequency reflects adult condition (Whattam & Bertram 2011).
145
Secondly, the redundant signal hypothesis (also called back-up signals hypothesis)
146
postulates that each signal provides similar information on the sender but, because each
147
signal may contain a certain degree of error or female assessment of each signal is error-
148
prone, the use of several signals decreases this error (Møller & Pomiankowski 1993,
149
Johnstone 1996). In the barking treefrog, Hyla gratiosa, Poole & Murphy (2007) found
150
that three parameters in male call give information about male size and that the
151
probability for a female to choose the largest male is higher when she can assess together
152
the three parameters, rather than each parameter separately. Alternatively, the unreliable
153
hypothesis (Møller & Pomiankowski 1993) proposed that multiple traits may not inform
154
about male quality. Either they have lost their connection to quality or they have evolved
155
through a runaway process or a receiver bias (Fisher 1930, Ryan 1990).
156
157
In addition to selection on the content, multiple signals could be also explained by a
158
selection on the transmission, reception or information processing by the receiver (the
159
“efficacy-based hypothesis”, Guilford and Dawkins 1991, Hebets & Papaj 2005, Table 1,
160
Fig. 1). For instance, amplifiers are signals that exist solely because they increase the
161
value of other signals (Hasson 1997, Harper et al. 2006). Abdominal patches of the
162
jumping spider Plexippus paykulli provide an example of amplifier because they
163
highlight the abdominal width linked to body condition (Taylor et al. 2000). In agreement
164
with “the amplifier hypothesis”, Rowe (1999) brought into light that the way the receiver
165
perceives and processes signals can explain the evolution of multiple signalling, as
7
166
several signals can be more effective to catch the receiver’s attention than a single one.
167
This hypothesis is based on the efficiency of the signal on the receiver psychology.
168
Multiple signals can affect receiver psychology in several ways acting on their potential
169
of detectability, discriminability or memorability (Rowe 1999). For example multimodal
170
signalling of male wolf spiders in the genus Schizocosa increases their detection by
171
females (Uetz et al. 2009). In the tree frog Hyla arborea, it was demonstrated that the
172
ability of female to discriminate attractive calls (and so good quality mates) increased
173
when the number of call components was high (Richardson & Lengagne 2010). Recently,
174
Akre & Ryan (2010) tested whether the complexity of the signal (3 chucks vs. 1 chuck)
175
can influence the memorability of female tùngara frog (Physalaemus pustulosus). Using a
176
dichotomous mate choice design, they showed that females remember the position of the
177
male only when he produces 3 chucks.
178
179
Overall, efficacy-based and content-based hypotheses all assume that using several
180
signals is better than a single one. However the adaptive function of multiple signals is
181
often untested (but see Lancaster et al. 2009, Rundus et al. 2010). Notably, only few
182
studies examined whether senders and receivers using multiple signals have better fitness
183
than individuals using only one signal. Though, this is of crucial importance for
184
understanding multiple signals evolution.
185
186
187
COMPLEX CHOICE IN VARIABLE ENVIRONMENT
188
Evolutionary processes are dynamic in time and space, and so are the morphological
189
and behavioural phenotypes resulting from them. The expression of phenotypes is often
190
plastic and depends of genes, environmental condition experienced by the individuals and
8
191
the interaction between genotype and environment (GEI, see Greenfield & Rodriguez
192
2004). In a recent meta-analysis on the temporal dynamics of selection on 89 studies,
193
Siepielski et al. (2009) argued that the strength of selection, including selection acting on
194
mate choice, can vary from year to year and suggested that this phenomenon is very
195
common in nature (but see Morrissey & Hadfield 2012). Thus, the rules of thumb used by
196
animals to make their choice should be flexible and context-dependent to finely track the
197
temporal and spatial changes in trait expression and remain adaptive in any condition
198
(Qvarnström 2001, Cotton et al. 2006, Cornwallis & Uller 2010). This point of view is a
199
major advance in the study of mate choice because it leaves a static vision of adaptive
200
preference for a dynamic vision (Bro-Jørgensen 2010). An elegant demonstration of this
201
idea was performed by Chaine & Lyon (2008) in the lark bunting Calamospiza
202
melanocorys. Female preference was dramatically flexible over a 5-year period and even
203
reversible across years in the direction of the preference for a given trait. Importantly,
204
changes in female preference were adaptive as they allowed the females to maximize
205
their fitness outcome. Chaine & Lyon (2008) concluded that variation in the physical or
206
social environment may therefore explain the existence of multiple signals. Unexpected
207
variation in mate choice may be more common than previously recognised, since it could
208
also occur along finer time scales, such as a reproductive season or even over one day
209
(Oh & Badyaev 2006, Jacot et al. 2008).
210
211
Bro-Jørgensen (2010) called “fluctuating environments hypothesis” the hypothesis
212
that adaptively explains the presence of multiple signals by fluctuations in ecological
213
conditions (Table 1). Multiples signals have evolve to maximize fitness of senders and/or
214
receivers in various fluctuating contexts by affecting both the information content
215
(content-based selection), and the transmission (efficacy-based selection) of the signal
9
216
(Bro-Jørgensen 2010). The environmental heterogeneity could have profound effects on
217
signal transmission. For example if one signal A is adapted to one specific environment
218
E1, and one signal B is adapted in another environment E2, senders and receivers who
219
use both the signal A and B have better success whatever the environment E1 or E2
220
(“Multiple sensory environments” sensus Candolin 2003). For example in the three-
221
spined stickleback, Gasterosteus aculeatus, female based their choice on visual signals in
222
clear water, while olfactory signal was used in turbid water (Heuschele et al. 2009).
223
Female that used both visual and olfactory signal could maximise their fitness whatever
224
the environment. This environmental variation (turbidity of water can change quickly)
225
can explain why visual and olfactory are both selected by mate choice in this species
226
(Heuschele et al. 2009).
227
228
The environmental heterogeneity could have also profound effect on the information
229
content of the signal (Greenfield & Rodriguez 2004, Lindström et al. 2009). For example
230
acoustic signals indicate male condition in field crickets Gryllus camperstris, but these
231
signals are more reliable in mornings and afternoons than evenings (Jacot et al. 2008). In
232
the collard flycatchers Ficedula albicollis conspicuous white forehead patch signals male
233
quality during dry summer conditions whereas the opposite was found in wetter years
234
(Robinson et al. 2012). According to the fluctuating environments hypothesis it is
235
expected that females use another signal when signal is unreliable ie in evenings when
236
acoustic signals failed to indicate male condition in field crickets and in wetter years
237
when white forehead did not match with male quality in the collard flycatchers.
238
239
These examples described in the previous section show that senders and receivers
240
could maximise their fitness in various, fluctuating contexts using multiple signals. Yet,
10
241
the rule(s) used by the receivers to adapt their choice to varying environment remains an
242
open issue. Indeed, in the stickleback example (Heuschele et al. 2009), shifts in the
243
signals used by the receiver could result from a perception constraint (i.e. the female does
244
not receive both signals because she cannot see in turbid water) or from an adaptation of
245
the receiver to external information (i.e. the female perceives both signals but prioritize
246
one of them according to environment condition). In the sand gobies Pomatoschistus
247
minutus, females seem able to adjust their choice according to external information.
248
Females adapt their decision rule for male size according to the intensity of male-male
249
competition (Lehtonen & Lindström 2009). When male-male competition is high,
250
females prefer big males because they benefit from the production of offspring able to
251
win competition, but not when competition is low. Note that according to the fluctuating
252
environments hypothesis it is expected that when male-male competition is low, females
253
should base their choice on another signal such as nest quality (Lehtonen et al. 2007).
254
Future research needs to investigate the rule used by females to adapt their mate choice
255
according to varying environments. According to previous models receivers are expected
256
to prioritize signals that are more reliable and easier to evaluate in each given
257
environment (Schluter & Price 1993, Iwasa & Pomiankowski 1994). To identify the most
258
reliable signal, one possibility is that receivers prospect several potential mates and base
259
their choice on the signal with the highest variance. Another assumption is that receivers
260
should use flexible signals in flexible environments and more static signals in less
261
flexible environments (Bro-Jørgensen 2010).
262
263
In addition to variation in external environment (ecological, social), the receiver
264
himself can be a source of variation (“receiver variability” sensus Hebets & Papaj 2005,
265
Fig. 1). While the classical view states that mate choice is concordant among receivers in
11
266
a population, recent work shows that preference is not always absolute in a population
267
(Jennions & Petrie 1997, Mays & Hill 2004). Indeed variation in mate choice among
268
females is common, even in fixed environmental conditions (reviewed by Jennions &
269
Petrie 1997), and could be largely explained by female heterogeneity (Bakker et al. 1999,
270
Kodric-Brown & Nicoletto 2001, Forstmeier & Birkhead 2004, Burley & Foster 2006,
271
Ilmonen et al. 2009, Hebets et al. 2008, Baugh & Ryan 2009, see also the “perceptual
272
variability hypothesis” in Hebets & Papaj 2005). This inter-individual variability could
273
also explain the evolution of multiple signals (Coleman et al. 2004, Suk & Choe 2008).
274
Indeed, we can expect that in one population in which 50% of the females assess an
275
ornament A and 50% assess an ornament B, males exhibiting both A and B ornaments
276
have a higher probability to find a sexual partner than males with only one of the A and B
277
ornaments. Experimental evidence of this paradigm was established in the satin
278
bowerbird Ptilonorhynchus violaceus in which an internal feature (age of females) can
279
drive the evolution of complex male displays such as blue decoration and display
280
intensity (Coleman et al. 2004). However evidences are scarce (but see Suk & Choe
281
2008). While it is now clear that animals have different personalities that influence their
282
decision rule in various contexts such as dispersal (Cote et al. 2010), foraging tactic
283
(David et al. 2011) or information use (Kurvers et al. 2010), only few studies investigated
284
a link between personality and mate choice (but see: Schuett et al. 2010). One future line
285
of research would be to explore how individual personality influences mate choice and
286
whether the coexistence of multiple personalities in a population of receivers can favour
287
the evolution of multiple signals in senders.
288
289
290
12
291
EMPIRICAL TESTS AND CONCEPTUAL ISSUES OF MULTIPLE SIGNALS
292
The number of hypotheses put forward to explain the evolution of multiple signals
293
offers great potential for testing them empirically (Hebets & Papaj 2005). However,
294
researchers may be confronted to a conceptual issue: the difficulty to empirically and
295
theoretically disentangle between some hypotheses (Johnstone 1996, Kokko 2001, Kokko
296
et al. 2002, Van Doorn & Weissing 2004). The distinction is not always obvious between
297
hypotheses differing on the content of the information conveyed by the signals. Signals
298
can be “fisherian” or condition-dependant. However, Kokko and colleagues (2002)
299
showed that the two apparently distinct processes (“fisherian” and good genes) are
300
actually the two ends of the same continuum in a model of preference for traits that
301
indicate indirect benefits. In agreement, Marcias Garcia & Ramirez (2005) demonstrated
302
that male signals exploiting receiver biases can become honest condition-dependant
303
signals.
304
305
The multiple messages and redundant message hypotheses are commonly mixed up
306
in many empirical studies (Candolin 2003, Jawor et al. 2004, Van Doorn & Weissing
307
2004). A first reason is that two definitions of redundant signals coexist. One definition is
308
based on the content-based information that receivers can glean about senders (Møller &
309
Pomiankowski 1993), whereas the second definition is based on the effect of the signals
310
on the receiver behaviour (Partan & Marler 1999, Partan & Marler 1995). According to
311
Partan & Marler (1999), signals are redundant or non-redundant if receivers exhibit
312
respectively similar or dissimilar responses to isolated signals. A second reason is that it
313
is difficult to empirically distinguish between the multiple messages and redundant
314
message, because information on individual condition can be either considered as
315
identical or as a different kind of information, depending on the authors and the accuracy
13
316
of the method and/or experiment (Møller & Pomiankowski 1993, Johnstone 1996, Van
317
Doorn & Weissing 2004). Specifically, two traits can signal parasitic resistance (i.e.
318
redundant messages), but one trait can signal resistance against ecto-parasites and the
319
other one can signal resistance against endo-parasites (i.e. multiple messages) (e.g. Jawor
320
et al. 2004). However, it is important to point out that validation of the redundant
321
message hypothesis do not require only correlations between several traits and one index
322
of sender quality but also an experimental confirmation that the probability to choose a
323
high quality mate increases with the number of traits used, as defined by Møller &
324
Pomiankowski (1993) (see e.g. Poole & Murphy 2007).
325
326
A unifying view of multiple signals theories is to consider that all these theories are
327
not necessarily mutually exclusive and that multiple signals may constitute a mosaic of
328
various types of signals. In the Satin bowerbird, Ptilonorhynchus violaceus, different
329
signals (bower quality and ultraviolet plumage coloration) indicate different aspects of
330
condition (respectively ecto-parasite load and feather growth). In that sense they support
331
the multiple message hypothesis. Thought, these signals also indicate the same aspect of
332
condition (body size, redundant signal hypothesis) (Doucet & Montgomerie 2003). Male
333
bower and plumage in this species provide both multiple information and redundant
334
information on the sender’s quality. Multiple other scenarios are conceivable: let’s
335
suppose a situation in which three signals A, B and C convey two types of information a
336
and b (i.e. multiple messages and redundant message), transmission of A, B and C
337
altogether could be favoured by a sensory bias, which in turn would allow a better
338
memorability of a and b information by the receiver (i.e. receiver psychology). As these
339
mosaics of signals may be the norm rather than an exception, this point of view should
14
340
therefore be integrated into future mathematical models investigating the evolution of
341
multiple signalling.
342
343
344
HOW INDIVIDUALS CHOOSE THEIR MATE(S) WHEN FACING MULTIPLE
345
SIGNALS?
346
One important proximate question still largely unsolved is how receivers use several
347
signals to choose their partner(s). It is still unclear how signals are perceived and
348
processed, and more generally what are the rules explaining mate choice when several
349
signals come to the receiver’s brain. For example, when an individual uses a pool-
350
comparison tactic with multiple signals, it implies that this individual receives several
351
kind of information about each potential partner and treats all information to finally
352
assign one value to each partner (Bateson & Healy 2005). In a threshold-criterion tactic
353
with multiple signals, each signal contributes (to a various extent) to reach the threshold
354
of the behavioural answer. This perspective adds a new level of complexity to the rule of
355
choice. How do prospective individuals assign one general value to each potential partner
356
when they received many signals? What is the thumb of rule used by receivers? Several
357
decision processes have been theoretically proposed, and empirically identified to some
358
extent.
359
360
-When animal use priority rules:
361
In priority rule systems, the receiver evaluates the multiple signals one by one, in a
362
hierarchical order, and one signal B is assessed only if another signal A has exceeded a
363
certain threshold, or when the choosy individual cannot discriminate between potential
364
mates only using the signal A (Scheuber et al. 2004, Table 2). This ruling system has been
15
365
named as hierarchical, sequential or priority system (Wittenberger 1983, Scheuber et al.
366
2004). One trait could be prioritized according to assessment cost or the abundance of
367
desirable partners (Fawcett & Johnstone 2003). In mice and humans, both complementary
368
genes and good genes are used for mate choice, but complementary genes are evaluated
369
only when potential partners share the same quality in terms of good genes (Roberts &
370
Gosling 2003, Saxton et al. 2009). Hierarchical rule is also known for private and social
371
information. Witte & Ryan (1998) found that the Sailfin Molly Poecilia latipinna use
372
social information only when there is no difference in private information (in terms of
373
male sizes).
374
375
-When individuals use weighting rules:
376
Individuals can evaluate a potential mate thanks to a combination of several signals in
377
which one signal does not affect the value of another signal via an additive assessment
378
process (Table 2, “simultaneous hypothesis”, Burke & Murphy 2007). In other words, the
379
strength of the preference increases linearly with the addition of signals and there is no
380
interaction between them. When the signals A and B are perceived together, the strength
381
of the resulting preference is equal to the sum of the preference when A is perceived
382
alone plus the preference when B is perceived alone (“A+B”= “A” + “B”). To our
383
knowledge, only few studies have clearly demonstrated this pattern of rule. An example
384
of additive equal preference with two signals is provided by the butterfly Bicyclus
385
anynana, in which the individuals seem to devote as much importance to visual as to
386
chemical signals in mate choice (A=B, Costanzo & Monteiro 2007). In the stickleback,
387
Gasterosteus aculeatus, females can use redness, courtship and body size to evaluate
388
males (Künzler & Bakker 2001). Using virtual stickleback, Künzler & Bakker (2001)
389
found that adding signals increases female preference. The preference for
16
390
“red+courtship+body size” exceeds the preference for “red+courtship” that exceeds the
391
preference for “red” male (A+B+C>A+B>A), without one signal influencing the weight of
392
other signals (Künzler & Bakker 2001).
393
394
Contrary to additive assessment process, multiplicative one occurs when the strength
395
of the preference is higher than a simple sum of signals (Table 2). Preference increases
396
non-linearly with the number of signals used. Namely, the strength of preference when
397
two signals A and B are present is higher than the sum of the preference when A is
398
perceived alone plus the preference when B is perceived alone (“A×B”>“A”+“B”). A
399
recent empirical study in the Sand Goby, Pomatoschistus minutes, reveals multiplicative
400
assessment process with male size and nest size as signals (Lehtonen et al. 2007). In this
401
species female choice was poorly explained by male size and nest size alone but strongly
402
explained by the interaction between them (Lehtonen et al. 2007). Amplifiers represent a
403
special kind of multiplicative assessment process. An amplifier is a signal that increases
404
the attractiveness of another signal (Hansson 1997, Rowe 1999, Harper et al. 2006), acts
405
as an “attention grabber” (Rowe 1999, “alerting signal”: Brø-Jorgensen 2010), improves
406
detection or discrimination, that changes the way the receiver processes signals (Hebets
407
& Papaj 2005). In a larger sense, multiplicative interaction includes also “emergence”,
408
which is defined by Partan & Marler (2005) as the combination of two signals that elicits
409
an entirely new result (A+B=C; see Rowe & Guilford 1996 for an empirical example
410
with aposematic signals). Emergence represents a small fraction of multiplicative
411
interaction in which only an important change in the answer, such as being chosen or
412
being rejected as a mate, represents an “entirely new result”. In this case the two signals
413
A and B do not elicit an answer alone but together (Table 2), as previously mentioned
414
with the sand goby experiment of Lehtonen and colleagues (2007).
17
415
-How to distinguish between decision processes?
416
Only few experimental designs offer the possibility to disentangle between the different
417
decision rule(s) used by animals during mate choice (Scheuber et al. 2004, Burke &
418
Murphy 2007). Moreover as explained in the section “complex choice in variable
419
environment”, the rule of thumb used by females to make their choice could be dependent
420
on the environmental conditions and/or internal features of the prospecting females. Thus
421
even the decision rule(s) should be envisaged in a dynamic context. Recent advances in
422
technology include robotic technology, audio, video recording and engineering. These
423
advances offer promising and exciting research perspectives in the study of mate choice
424
by providing the possibility to create new signals, control existing signals or design any
425
kind of signal variation and test the impact of each signal on the strength of preference
426
(e.g. Rosenthal et al. 2004, Poole & Murphy 2007, Taylor et al. 2008, Gomez et al. 2009).
427
In addition, robotic technology will also allow testing for the effects of internal and
428
external features on decision rule used by female, while controlling for signal variations.
429
430
431
TOWARD A NEUROBIOLOGICAL PROCESSING OF MULTIPLE SIGNAL
432
THEORY?
433
Complexity in signal expression is necessarily reflected in signal perception and
434
processing. This complexity likely explains why it is still unclear how choosing
435
individuals integrate and treat all multiple signals, potential interactions between signals,
436
and information on environmental conditions to make their choice (“information
437
processing” in Fig. 1). A rewarding area for future studies is cognitive ecology, i.e.
438
animal information processing that leads to decision-making with fitness consequences
439
(Dukas 1998). Here, cognition is considered in its broader sense, namely “the sum of
18
440
processes by which information is processed, stored, retrieved and used in a flexible and
441
adaptive sense. Such a definition refers therefore to implicit faculties like perception,
442
attention, representation, expectation, planning, learning, recognition, memory and
443
knowledge organization” (Giurfa 2003). This view contradicts the common misleading
444
image of animals as mainly directed by pre-programmed reflex mechanisms, but does not
445
imply conscious levels of decision making.
446
447
Earlier work on “receiver psychology” (Rowe 1999) has highlighted the importance
448
of considering neuronal processes and brain functions to understand the implication of
449
multiple signals in mate choice. Therefore recent advances in neurology open new
450
avenues to explore mate choice more accurately when animals are facing two or more
451
signals. Indeed, modern methods now allow to visualize brain regions that are activated
452
when performing certain tasks, such as attractiveness assessment and mate decision, or
453
while being stimulated by various stimuli including sexual signals. Two main types of
454
techniques that track neural activity are currently available and are increasingly being
455
used: Immediate Early Gene expression (IEG) and functional resonance magnetic
456
imaging (fMRI).
457
458
IEGs are genes that are dynamically regulated in the brain by neural activity. They
459
are rapidly expressed upon neural stimulation (usually 20-90 minutes) and function as
460
transcription factors or code for structural proteins. Classical experiments involve one
461
group of individuals which performs a behavioural task or is exposed to a stimulus, while
462
the control group is placed in control conditions. Because IEG induction does not require
463
preparatory procedures, individuals can virtually be exposed to any kind of stimulus,
464
allowing the exploration of a variety of behavioural contexts (Farivar et al. 2004). After
19
465
sacrifice, brain sections are marked to detect either mRNA or proteins, with a resolution
466
as precise as the cellular level (Guzowski et al. 2001, Farivar et al. 2004). Using IEG
467
expression, two studies identified the forebrain regions involved in the detection and
468
discrimination of preferred male songs. In the European starling (Sturnus vulgaris),
469
females exposed to preferred longer songs showed higher expression of the ZENK gene
470
in the ventral-medial neostriatum. Similarly, female canaries showed higher expression
471
level of the same gene but in the caudomedial mesopallium when they were exposed to
472
songs containing sexy syllables (Gentner et al. 2001, Leitner et al. 2005). These two
473
examples demonstrate that IEG techniques yield promising results when females are
474
exposed to single, “simple”, sexual stimuli; however these techniques can also be
475
rewarding in more complex contexts, such as varying social context, or when females use
476
complex social cues to choose their mates (Desjardins et al. 2010). Moreover, Farivar et
477
al. (2004) proposed a new procedure called “dual activity mapping” in which two
478
different stimuli A and B are successively applied to a given individual, and the neurons
479
that are activated by A only, B only, or both A and B can be identified. Although it has not
480
been used to investigate how multiple signals are processed so far, this new approach is
481
shows potential and surely will yield important results in the next few years.
482
483
In contrast to IEGs, neuroimaging has made it possible to visualize dynamic brain
484
function without invasion. Indeed, IEG techniques can only provide a post-mortem
485
picture of how the brain reacted to a specific stimulus or event, whereas neuroimaging
486
allows a direct observation of brain function at the time of stimulation and time series of
487
observations required for longitudinal studies. Neuroimaging comprises several
488
techniques, including electroencephalogram (EEG) signals analyzed in term of event-
489
related brain potentials (ERPs) (e.g. Schacht et al. 2008), positron emission tomography
20
490
(PET) (e.g. Bales et al. 2007) and functional resonance magnetic imaging (fMRI). Both
491
PET and fMRI measures change in blood flow, oxygen consumption and glucose uptake
492
that are directly related to neural activation. fMRI is now preferred to PET because it
493
provides a high-resolution three-dimension colored picture of the brain and does not
494
entail the injection of radioactive substances that may lead to overexposure to radiation
495
(Logothesis 2008). Investigations of the brain regions activated by sexually attractive
496
stimuli have mainly been undertaken in humans so far. It is largely admitted that human
497
mate choice is reciprocal, based on multiple signals, including facial and body
498
attractiveness
499
information, and that internal information can modulate the strength of preference given
500
to each signal (Little et al. 2008, Currie & Little 2009, Saxton et al. 2009, Lass-
501
Hennemann et al. 2010). Yet physical attractiveness plays an important role in both men
502
and women mate choice, and asking experimental subjects to watch and rank photos
503
according to their attractiveness is a simple procedure. Nakamura and colleagues (1998)
504
used fMRI and identified higher activity in the left frontal regions of men brain when
505
subjects assessed a woman face as attractive. Similarly, Rupp and colleagues (2009a,b)
506
examined the brain regions associated with women’s sexual decision making with fMRI
507
while women were watching photos of men’s faces presented as potential sexual partners.
508
The researchers found a stronger activation in a number of brain regions, namely the
509
anterior cingulated cortex, posterior cingulate cortex, midbrain, parietal sulcus, superior
510
temporal gyrus, precentral gyrus, and inferior parietal lobule. In both men and women,
511
PETs revealed a higher activity in the caudate nucleus and other parts of the brain reward
512
system linked to attractive female bodies (Holliday et al. 2011). In general, most brain
513
regions that were identified by these studies are known to be involved in the brain reward
physical
attractiveness,
self-similarity, sexual
21
dimorphism
social
514
system and it is likely that an observer’s preference for an attractive photo is mediated by
515
its reward value (Fisher et al. 2006).
516
517
Clearly, behavioural ecology coupled to neurobiology has only begun to establish
518
relationships between gene expression, brain function and male sexual traits, and the
519
powerful IEG and fMRI techniques have still a lot to contribute to the understanding of
520
mate choice. The experiments described above call for future research into the effect of
521
multiple signals on brain function. More interestingly we can expect that the results of
522
such studies may provide answers on how each signal is processed, which interactions
523
occur (additive, multiplicative, hierarchical) and finally what are the rules of thumb used
524
to make a choice. More precisely we can expect that when animal use hierarchical rule (B
525
is used only after evaluation of A), the neurons processing information of A suppress the
526
neurons processing information of B. Conversely when animal use multiplicative
527
interaction, we can expect that neurons processing information of A and B activate each
528
other to increase neural response which exceeds the simple sum of response when A is
529
perceived alone plus the preference when B is perceived alone (“A×B” > “A”+“B”). We
530
can predict more connections between neurons processing information of A and B in
531
multiplicative interaction that in additive interaction.
532
533
Organisms with small brains may serve as prime model systems for identifying
534
neuronal processes and circuitry, and neural substrates involved in mate preferences for
535
multiple signals (Dickson 2008). These organisms have indeed fewer neurons and
536
simpler brain architecture than large-brained species, making research easier. Moreover
537
artificial neural network analyses typically show that the minimum number of neurons
538
necessary to perform a variety of cognitive tasks is exceedingly small. Drosophila
22
539
appears to be a great model because this species shows complex mate choice with
540
multiple signals, mating rule is affected by internal and external features, while having
541
well-known simple brain architecture (Dickson 2008). On the other hand, several
542
vertebrate species might be good candidates to study cognitive ecology: anurans such as
543
the túngara frog, fishes such as poeciliid species or human (Fisher et al. 2006, Wilczynski
544
& Ryan 2010, Cummings 2012).
545
546
Advances in the field of neurobiology will provide new insights about the proximate
547
causes of multiple signalling, allowing a better understanding on how individuals choose
548
their mate(s). Despite tremendous advances in the field of cognitive ecology, we are still
549
far from unravelling how multiple signals emitted in the context of sexual communication
550
can elicit answers such as pair-bonding or mating (Fig. 1). The field of cognitive ecology
551
is currently undergoing major advances (Dikson 2008, Wilczynski & Ryan 2010). The
552
association between neurobiology and behavioural ecology could provide powerful
553
results and better understanding of multiple signal theory. Future research should
554
investigate how receiver brain varies with the attractiveness of conspecifics senders
555
including multiple and multimodal signals (Fisher et al. 2006, Dickson 2008, Wilczynski
556
& Ryan 2010). Moreover more studies should aim at exploring receiver variability in
557
perception and information processing at the neural level (Hebets & Papaj 2005).
558
559
560
CONCLUSION
561
Since first interrogations about the use of multiple signals, it has become clear that
562
mate choice is by far more complex than a simple relation between one trait and one
563
preference. An adaptive reproductive decision commonly requires the detection and
23
564
processing of multiple, and sometimes multimodal, signals. The senders should convey
565
adaptive signals that allow them to reproduce with the receivers and the receivers
566
integrate all these signals to make an appropriate decision (behaviour) to choose the best
567
senders. This decision has a great influence on fitness of the two protagonists and natural
568
selection has selected various sender and receiver strategies using multiple signals.
569
Recent research works have revealed a large variability in the kind of signals used by
570
receivers but less conventional signals and cues (such as social cues) should be taken into
571
account more frequently in multiple signals theory.
572
573
Many theories have been developed to explain the evolution and maintenance of
574
multiple signals. These different theories are frequently considered separately, yet recent
575
empirical results strongly suggest that multiple signals can be the result of multiple
576
evolutionary pressures, and therefore should be more integrated in a common framework.
577
Importantly, recent studies highlighted the importance to take into account both internal
578
characteristics and environmental conditions that may influence the production,
579
transmission, reception and processing of multiple signals. This internal and external
580
environmental heterogeneity could explain the use of multiple cues and the use of
581
different decisions rules to process multiples signals. The use of robot technology, new
582
advances in cognitive ecology can help research on multiple signals and the
583
understanding of how signals are perceived by individuals, are processed by brains, how
584
these signals interact and lastly how internal and external information affect signal
585
processing, all in a dynamical world. This knowledge will allow understanding the
586
evolution of mate choice using multiple signals and surely will provide a better and more
587
realistic estimate of the strength of sexual selection.
588
24
589
Acknowledgements
590
This work was supported by the Ministère de la Recherche (PhD fellowship to JC and
591
two CNRS grants to AL and DS). This work was supported by the "Laboratoire
592
d’Excellence (LABEX)" entitled TULIP (ANR -10-LABX-41).
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Table 1. Existent hypotheses proposed to explain the presence of multiple signals.
Hypothesis
Multiple signals
Example
Multiple message
Reflect different information about condition
Whattam & Bertram 2011
Redundant message
Reflect the same information about condition
Poole & Murphy 2007
Ureliable signals
No reflect condition
MØller & Pomiankowski 1993
Amplifiers
Amplify other signal
Taylor et al. 2000
Detectability
Increase detectability of potential mate
Rowe 1999
Discriminability
Increase discriminability between potential mate
Richardson & Lengagne 2010
Memory
Are more efficient to allow memorability
Akre & Ryan 2010
Fluctuating
environments Using several signals sender could “seduce” receiver according
(external feature)
Heuschele et al. 2009
receiver external feature
Receiver variation (internal Using several signals sender could “seduce” receiver according Coleman et al. 2004
feature)
receiver internal feature
943
944
945
40
946
Table 2. Different types of treatment of several signals by the receiver.
Strength of preference
Interaction
Without interaction
A
B
with interaction
Example
A*B
Hierarchical
Witte & Ryan 1998
Additive
Künzler & Bakker 2001
Multiplicative
Castellano & Rosso 2007
Amplifier
Harper et al. 2006
Emergent
Lehtonen et al. 2007
947
948
949
950
951
952
953
41
External feature3
predation, social
environment, environment
Manipulation
Internal feature3
personality, self condition,
age, experiment
production / content
signals
production
signal
design
Sender
transmission
efficacy
954
receiver
information
processing1 *
decision rule
choice2
reception
Information extraction
955
Figure 1. Schematic view of sexual communication with multiple signals. Conventionally, mate choice implies active sampling of potential
956
mates or assessment of varying traits, but mating biases can sometimes result from passive acceptance of mates (see Kokko et al. 2003). Varying
957
traits that directly affect mating decision are also called “cues”. Traits or “cues” which have been modified by natural selection for the purpose of
958
communication are called “signals” (Candolin 2003). In communication terminology, signals are emitted by a sender and processed by a
42
959
receiver. The receiver perceives and processes signals before adjusting its behaviour according to their information content or their stimulating
960
power and their decision rule. Selection favours senders whose signals affect the behaviour of receivers to their own advantage but also favours
961
receivers who are able to extract useful information from the senders (Font & Carazo 2010). 1-Information processing/decision rule could be
962
hierarchical, additive or multiplicative (see text), 2-Correspondance to behaviour (interest or not, copulated or not, pair bond or not), 3-external
963
and internal information which could modulate signal production, signal design and information processing by changing the assessment of
964
signals.
43
ARTICLE 2
Multiple signals in the palmate newt: ornaments
help when courting.
Cornuau JH, Rat M, Schmeller DS, Loyau A. 2012.
Behavioral Ecology and Sociobiology, 66:1045-1055.
Behav Ecol Sociobiol (2012) 66:1045–1055
DOI 10.1007/s00265-012-1355-y
ORIGINAL PAPER
Multiple signals in the palmate newt: ornaments help
when courting
Jérémie H. Cornuau & Margaux Rat &
Dirk S. Schmeller & Adeline Loyau
Received: 12 December 2011 / Revised: 28 March 2012 / Accepted: 29 March 2012 / Published online: 18 April 2012
# Springer-Verlag 2012
Abstract There is increasing evidence that female mate
choice is often based on the assessment of multiple male
traits, involving both morphology and behavior. We investigated female mate choice for multiple male traits in the
palmate newt, Lissotriton helveticus, including male tail
filament length, hind foot web size, crest development, body
size, ventral coloration, and courtship display activity.
Observations of courtship display in the field revealed that
females spent more time in front of males with longer tail
filaments. Laboratory experiments revealed a more detailed
relationship between filament length and courtship display.
We found that females took more sperm masses from males
with both longer filaments and greater display activity.
Experimental shortening of the tail filament length substantially decreased the number of male sperm masses transferred. However, when we experimentally reversed relative
filament length between two males in mating trials, male
mating success was explained by courtship activity and not
by filament length. Our results show that female palmate
newts value multiple traits during mate choice, including both
morphological ornaments and reproductive behaviors in
males. Our results further suggest that, when filament length
Communicated by K. McGraw
Dirk S. Schmeller and Adeline Loyau share senior authorship in this
study.
Electronic supplementary material The online version of this article
(doi:10.1007/s00265-012-1355-y) contains supplementary material,
which is available to authorized users.
J. H. Cornuau (*) : M. Rat : D. S. Schmeller : A. Loyau
Station d’Ecologie Expérimentale du CNRS USR 2936,
2-4 Route du CNRS,
09200 Moulis, France
e-mail: [email protected]
is below a certain threshold, females may value the information content of courtship activity over that of filament length.
Keywords Sexual selection . Sexual communication .
Courtship . Filament . Amphibian . Lissotriton helveticus
Introduction
In many species, males express complex courtship displays
involving elaborate ornaments combined with conspicuous
behaviors. The evolution and maintenance of such morphological and behavioral traits are commonly explained by
their signaling role in intersexual communication (Møller
and Pomiankowski 1993; Candolin 2003; Bro-Jørgensen
2010). Multiple signals that potentially could be used for
mate choice were empirically identified before the first
theoretical explanations had been proposed. Indeed, theoretical models of sexual selection generally predict that females
should evolve a preference for a single signal because of the
costs of assessing multiple signals (Schluter and Price 1993;
Johnstone 1996; Fawcett and Johnstone 2003; but see van
Doorn and Weissing 2004). However, the idea that females do
use multiple signals to choose their mate is supported by an
increasing number of empirical studies, leading to a growing
interest in the evolution and maintenance of such signals
(Candolin 2003; Hebets and Papaj 2005; Bro-Jørgensen 2010).
Several hypotheses have been put forward to explain why
and how females use numerous signals: multiple messages
(different signals convey information on different properties
or temporal aspects of male qualities), redundant signal
hypothesis (different signals convey the same information),
unreliable signal hypothesis (signals not linked to quality),
or receiver psychology (several signals are better detected
than a single one, or a signal amplifies another signal;
1046
Guilford and Dawkins 1991; Møller and Pomiankowski
1993; Rowe 1999; Hebets and Papaj 2005). Disentangling
these hypotheses mainly requires unraveling the information
content of multiple signals (Candolin 2003). To date, less
work has been undertaken to examine the relative use of
each signal, their prioritization, and how signals are processed
by choosy females (Witte and Ryan 1998; Künzler and Bakker
2001; Candolin 2003; Scheuber et al. 2004).
Recently, it was proposed that a fluctuating environment
is likely to drive the evolution of multiple signals because
few signals may be sufficiently flexible to remain reliable
when the environment changes (Chaine and Lyon 2008;
Bro-Jørgensen 2010; Cornwallis and Uller 2010). Morphological and behavioral signals commonly differ in their
temporal flexibility. Some morphological signals, such as
an elongated tail or elaborate plumage, are relatively fixed
(static sensu Hill et al. 1999) since they cannot be extensively
modified on a short time scale by the signaler. Morphological
signals are generally produced once per year before or at the
beginning of the breeding season and remain unmodified until
the next year (Hill et al. 1999; Loyau et al. 2005a, b; Baird et
al. 2007; van Dongen and Mulder 2008). Morphological
signals are thus expected to better reflect genetic quality or
long-term viability (Kokko et al. 1999; Scheuber et al. 2004).
However, if the bearer’s quality or the environmental conditions change between production and assessment, morphological signals may become unrepresentative of the signaler’s
quality (Bro-Jørgensen 2010). On the contrary, behavioral
signals such as vigorous displays or song rates can be finely
tuned by the signaler depending on the signaler’s current
quality, motivation, or environmental conditions. Behavioral
signals are typically more labile (dynamic; sensu Hill et al.
1999) than morphological ones and thus are expected to
accurately reflect signaler condition at the time of assessment
(Hill et al. 1999; Loyau et al. 2005a; Baird et al. 2007; van
Dongen and Mulder 2008).
Given that individual quality and environmental conditions may vary on a short time scale, it has been predicted
that females should use a mixture of static morphological
and dynamic behavioral signals to adaptively choose their
mates (Bro-Jørgensen 2010). Females are further expected
to differ in the degree to which they pay attention to these
two types of signals during mate choice. This potential
difference can only be assessed when both signals are contradictory, e.g., when a male exhibits an ornament of high
quality while expressing poor courtship behaviors or vice
versa. However, it is still disputed how females deal with
such contradictory information (Hill et al. 1999; Loyau et al.
2005a; Baird et al. 2007; van Dongen and Mulder 2008).
One can predict that females should value the information
content of behavioral signals over morphological signals
because behavioral signals provide more accurate information on current male condition (Hill et al. 1999; Loyau et al.
Behav Ecol Sociobiol (2012) 66:1045–1055
2005a; Baird et al. 2007; Bro-Jørgensen 2010). This is
particularly the case when females prefer mating with
healthy individuals not only to obtain indirect benefits, in
terms of good genes for their offspring or more viable
sperm, but also to avoid contracting infectious diseases,
since a recent decline in male condition could indicate a
challenged immune system (Sheldon 1993; Loyau et al.
2005a; Chargé et al. 2010). On the contrary, it has been
suggested that the expression of dynamic (behavioral) signals
is sensitive to very short term, motivational influences, social
circumstances, or stochastic environmental factors, and thus
these signals may not be as valuable to conspecifics as fixed
signals (Green et al. 2000; van Dongen and Mulder 2008).
We wished to test this set of predictions in the palmate
newt, Lissotriton helveticus, an amphibian with strong sexual dimorphism (Griffiths and Mylotte 1988). Males are
smaller and thinner than females. Males express a yellowto-dark-orange ventral coloration whose role remains unclear. During the reproductive period, males exhibit both
morphological and behavioral traits that may be assessed by
females when choosing a mate. Morphological male traits
that appear to have a sexual function are the hind foot web, a
caudal filament, and a low dorsal caudal crest. In the crested
newt Triturus cristatus and the smooth newt Lissotriton
vulgaris, females prefer males with high crests (Hedlund
1990a; Green 1991; Gabor and Halliday 1997; Malmgren
and Enghag 2008). In the palmate newt, Haerty et al. (2007)
investigated female visual preference for filament length
and body size and found that females spent more time close
to males with longer filaments and smaller bodies. In addition to morphological traits, male L. helveticus express a
conspicuous courtship behavior called “fan display”, which
mainly consists of displaying the tail and the filament to the
female in a rapid vibrating fan movement (Halliday 1975a).
This display behavior is very variable between individuals
(Halliday 1975a, b; 1976). If the female is receptive to the
displaying male, she touches his tail with her snout, which
elicits spermatophore deposition by the male. The female
can then pick up the sperm mass in her cloaca.
We used an approach combining: (1) a correlative study
in the field; (2) a correlative study in the laboratory; and (3)
a manipulative study of a morphological signal in the laboratory. We first examined the impact of tail filament length
on the maximum time spent by the female watching a male
fan display in the field. We then examined whether female
palmate newts use multiple morphological and behavioral traits
to choose their mates, focusing particularly on the role played
by both filament length and courtship activity, while controlling
statistically for potential additional morphological signals (including crest development, hind foot web, body size, and
coloration). Finally, we manipulated filament length of pairs
of males so that the male with the shorter filament became the
male with the relatively longer filament, while courtship
Behav Ecol Sociobiol (2012) 66:1045–1055
activity was not manipulated. We predicted that, if females only
value filament length, female preference should be reversed.
Materials and methods
Correlative study in the field
Our study was designed to investigate whether females
spent more time watching courtship displays by males with
longer tail filaments. In amphibians, female preference has
rarely been observed in the wild, and such observations are
likely to provide valuable insights into the evolutionary
processes involved in sexual selection and are complementary to laboratory experiments.
Our behavioral observations of newts were conducted in
two small ponds near the Refuge des Etangs de Bassiès in
the Pyrenean Mountains (Ariège, France), at 1,655 m above
sea level, between 30 June and 09 July 2010, during the
peak of the reproductive season. These study ponds are ideal
for behavioral observations because they are shallow with
crystal clear water, were only a few meters apart, and had
little vegetation and few rocks. The behavioral observations
were performed for 5 days between 07:00 am and 07:00 pm.
The average male courtship fan display lasted 237.5±25.5 s
and was not significantly different between observation days
(Kruskal–Wallis tests χ²01.95, df04, P00.75), between
morning and afternoon (Wilcoxon rank sum test W0150,
P00.39), and between the two ponds (W0121, P00.62).
Reproductive behaviors of newts were well described by
Halliday (1975a). The male first approaches the female. He
then smells the female cloaca, follows her when she moves
away, and orients himself in front of the female. After this
orientation phase, courtship activity begins, defined by
“fan” movements of the male tail and filament in front of
the female. The female either stays still, seemingly watching
male fan display or moves away. When the female moves,
the male stops the fan movement. A new sequence of
orientation and fan display can then occur.
Sperm mass transfer is rarely observed in field conditions
(Hedlund 1990b). We used the time spent by females watching
courtship fan display as a proxy for female preference (Wagner 1998). Behavioral observations were conducted by one
observer (JC) who walked around the two ponds (at 1-m
distance) until seeing a male in either the orientation or displaying phase. During behavioral observations, we recorded
the time between the start of the male display and the end, due
to departure of the female or the male surfacing to breathe.
Taking a breath is a critical moment in courtship by male
newts, as they are likely to lose visual contact with the female
to whom they were displaying (JC, personal observation).
Therefore, males increase the time between breathing episodes when the females are receptive (Halliday and Sweatman
1047
1976; Halliday 1977). We obtained several displaying periods
for each male. We used length of the longest bout of the male
display to a female for statistical analysis. Males were caught
to measure snout–vent length (SVL, from the snout tip to the
posterior end of the cloaca) and filament length with a caliper
(accuracy, 0.01 mm). We recorded individually distinctive
features such as shape, black spots, or coloration by drawing
the male on paper. These drawings and the two measures
(SVL and filament length) allowed us to ensure that a given
male was not included twice in our data set. Each male was
then immediately released at the site of capture. A total of 33
males (24 and 9 per pond) were observed.
Laboratory experiments
Newts caught in the wild were maintained in captivity at the
Station d’Ecologie Expérimentale du CNRS à Moulis
(Ariège, France) at 18 °C (±0.5 °C) and a natural light/dark
cycle of 10:14 h (ZooMed ReptiSun 2.0 fluorescent bulb).
Unisex groups of ten individuals were placed in opaque
tanks (52×33.5×29.5 cm) with de-chlorinated water and
some plants collected in their native environment. The water
depth was about 5 cm, corresponding to about 9 l of water.
Each tank was provided with a shelter (a perforated clay
brick with 17 holes). The top of each brick was just above
the water level to allow newts to get out of the water. Newts
were fed ad libitum with chironomid larvae, daphnia, tubifex, and earthworms. Time between capture and release
back into the wild was less than a month.
Behavioral experiments were designed to offer two males
to a single female and were conducted in the animal housing
facility between 0800 and 1500 hours local time. Experimental tanks were divided into three compartments by two
removable transparent perforated Plexiglas separations, defining a central compartment (20×33.5×29.5 cm) and two
external compartments (16×33.5×29.5 cm). We followed a
protocol used by Haerty et al. (2007) with the palmate newt,
to be able to compare our results with the previous results
(data not shown). The experiment comprised four steps. In
step 1, a focal female was placed in the central compartment
where she could move freely for 5 min, allowing the female
to explore her new environment. In step 2, the experimentalist placed the female in the center of her compartment in a
circular opaque PVC tube for 5 min, and a male was placed
in each external compartment. The tube was then removed
so that the two males and the female could move freely in
their compartments and explore their new environment for
15 min (step 3). Finally, in step 4, separations were removed
and the three individuals could interact freely for 40 min. At
the end of the experiment, we checked for the presence of
sperm mass in the tank and we examined the female’s cloaca
for sperm mass transfer. Each individual was used only once
in the experiment and the experimental tank was thoroughly
1048
Behav Ecol Sociobiol (2012) 66:1045–1055
cleaned with tap water between trials. Four trials were
performed simultaneously in four experimental tanks. Each
trial was recorded using a video camera (Panasonic HDCTM60, full HD, 1080p) placed above the experimental tank,
totaling 65.3 h of video observation.
Morphological traits were measured immediately after
the experiment. We recorded body mass (accuracy,
0.01 g), SVL (snout–vent length), and filament length as
previously described using an electronic caliper. The crest is
small in this species, so we used tail size as an index of crest
development (Green 1991). Tail area and the left and right
hind foot web areas were measured by taking a photo on a
millimeter paper background (grid 1 mm²) with a digital
camera (Nikon D5000). Photo analysis was conducted with
ImageJ 1.43 (http://rsb.info.nih.gov/ij; developed by Wayne
Rasband; Abramoff et al. 2004). With a subsample of 60
males, we tested the reliability of two measurements with
ImageJ. Filament length, hind foot web area, and crest
development were all highly repeatable (respectively, r²0
0.99, r²00.98, and r²00.96). Ventral coloration was measured using a spectrometer (USB2000, Ocean Optics Inc.,
Dunedin, FL, USA) with a Xenon light source (PX-2) and a
R400-7-UV/VIS fiber optic cable and probe at a 45° angle
to the skin surface. Five spectrometer measures were taken
at the middle of the belly. We used Endler’s segment classification method on percent reflectance between 300 and
700 nm to obtain indexes of hue, chroma, and brightness
(Endler 1990). We tested the repeatability of these indexes
with Kendall’s coefficient of concordance (Loyau et al.
2007) with a subsample of 100 individuals. Hue, chroma,
and brightness were highly repeatable (respectively, W0
0.93, χ²0361, P<0.001; W00.95, χ²0471, P<0.001; and
W00.73, χ²0361, P<0.001).
The videos were analyzed with The Observer 7.0 software (Noldus Information Technology). For each male, we
recorded the time spent displaying the fan (courtship activity)
and the number of sperm masses transferred to the female.
Experiment 1: female preference of filament length
This experiment was designed to test whether palmate newt
females prefer males with longer tail filaments. In total, 76
males and 38 females were used to perform 38 replicate
trials. Each trial involved three individuals: one female, one
male with a long filament (M+), and one male with a shorter
filament (M−). The pair of competitor males was chosen so
that males significantly differed in filament length (paired
t test, t 014.78, df 037, P < 0.001) and this difference
remained stable over trials (Table 1). SVL, body mass,
hue, chroma, brightness, and tail area (index of crest development) did not significantly differ between M+ and M−
males (paired t test, all P>0.05). However, hind foot web
area and filament length were correlated (r00.44, df074, P<
0.001), and M+ males had more developed hind foot web
areas than M− males (paired t test, t02.8, df037, P00.008).
Experiment 2: manipulation of filament length
In this experiment, we manipulated filament length to test
whether a decrease in filament length decreased the number
of male sperm masses transferred. Manipulation of a trait
(phenotypic engineering) allowed us to avoid potentially confounding factors (Sinervo and Basolo 1996). Filament length
could not be elongated because of technical difficulties. Many
other studies have used only sexual trait reduction in their
experimental manipulation for similar reasons (e.g., Bischoff
et al. 1985; Petrie and Halliday 1994; Tomkins and Simmons
1998; Pryke and Andersson 2005). In total, 120 males and 60
females were used in experiment 2 to perform 60 replicate
trials. One week before the start of each experimental trial,
male filament length was measured to rank the males according to their filament length and to choose the pairs of male
competitors as in experiment 1. However, unlike experiment 1, male filaments were immediately cut after measurement, so that the male with the longer filament in the
pair of males became the male with the shorter filament
(Table 1). Both males in each trial had their filament length
shortened to control for a possible effect of the cut itself
(Table 1). Filament length was not measured immediately
after cutting to avoid further stress to the individuals. The
individuals were left un-manipulated until trial. Filament
length was measured a second time just after the trial, and
that measurement was used for statistical analyses. As in
experiment 1, females had the choice between a male with a
Table 1 Measures of filament length (millimeters) between experiments (means±SE)
Exp 1
M+ males
M− males
|M+ −M−|
6.39±0.10
4.40±0.19
1.99±0.14
Exp 2 (BS)
Before shortening
Exp 2 (AS)
After shortening
P value
6.25±0.12
4.46±0.09
1.79±0.09
2.02±0.07
3.75±0.09
1.74±0.09
0.001
0.001
0.31
Equalities
Exp 10exp 2 (BS)
Exp 10exp 2 (BS)
All
“|M+ −M− |” represents the difference in filament length between the males with longer filaments (M+ male) and the males with smaller filaments
(M− male) for a given experiment. P values correspond to the results of the linear model that explains filament length by experiment. Equalities
show that filament length was not significantly different between experiments (Tukey’s tests)
Behav Ecol Sociobiol (2012) 66:1045–1055
longer filament (M+ male) and a male with a shorter filament (M− male). The SVL, body mass, hue, chroma, brightness, and tail area did not differ between M+ and M− males
(paired t test, all P>0.05). Again, hind foot web area and
filament length (before cut) were positively correlated (r0
0.44, df0118, P<0.001), as a consequence M− males had
more developed hind foot web areas than M+ males (paired
t test, t03. 9, df059, P<0.001).
We performed a study involving five newts to ensure that
shortening the male filament would not result in distress. We
used the same design describe previously (see Fig. S1). We
did not observe any behavioral differences for a male before,
immediately after, or 1 week after shortening the filament
(Fig. S1). Moreover all males used in experiment 2 behaved
normally after filament shortening.
Statistical analysis
In the field experiment, the effect of male SVL and filament
length on the time a female spent watching male display
(log-transformed) was assessed with a model II regression
using an ordinary least squares method.
For the laboratory experiments, we calculated indexes of
hind foot web and crest developments as the residuals of a
regression of the square root of hind foot web area or tail
area on the SVL (Baker 1992). Because morphological traits
were strongly correlated, we performed a principal component analysis (PCA) on male traits (SVL, body mass, hue,
chroma, and brightness) using the dimdesc function of the
FactoMineR package in R (R Development Core Team
2010). We did not include filament length, crest development, and hind foot web size in the PCA to fully explore
their explanatory potential with model selection. Including
or not, filament length, crest development, and hind foot
web size in the PCA did not change the overall conclusions of the study. The PCA resulted in principal
components of body size (PCbody size, loading on SVL,
and body mass), of coloration (PCcoloration, loading on
hue, and chroma), and of brightness (PCbrightness, loading on brightness; Table S1).
The effects of sexual traits on sperm mass transfer were
assessed using generalized linear mixed models with the
lmer function of the lme4 package in R (R Development
Core Team 2010). Morphological traits (filament length, hind
foot web size, crest development, PCbody size, PCcoloration, and
PCbrightness) and the behavioral trait (courtship activity) were
set as fixed factors, and tank, day-of-trial, and trial identity
were included as random factors. To investigate the effects of
male traits on the number of sperm mass transferred to the
females, we used models with a Poisson distribution of error
terms and the log link function. We analyzed data and made
biological inferences using the information theoretic approach
that identifies the best set of models according to several
1049
competing hypotheses via information criteria (Burnham and
Anderson 2002; Garamszegi et al. 2009; Burnham et al. 2011;
Grueber et al. 2011). We evaluated a set of candidate models
transferred to combinations of all morphological and behavioral variables and all interaction terms using Akaike’s Information Criterion corrected for small sample size (AICc;
Burnham and Anderson 2002).We used the stdz.model and
top.models functions of the arm and MuMIn packages in R to
calculate AICc, AICc weight, and other parameters needed for
the analysis (Grueber et al. 2011). We present only models that
were well supported by the data (models with a ΔAICc <2,
Burnham and Anderson 2002). Because several equally
likely models were identified and no model had
w >0.90, we model-averaged parameter estimates (“θ”)
and the associated variances from the 95 % confidence
interval (CI) set of candidate models using the model.avg
function of the MuMIn package in R (Grueber et al. 2011).
We considered the effect of one variable as having an
important predictive value only when the 95 % CI did
not include zero (Garamszegi et al. 2009; D’Alba et al.
2010). We calculated the coefficient of determination
(percentage of deviance explained) of the best models
as follows: (deviance of the null model − deviance of
the model)/deviance of the null model. We additionally
used chi-square tests in experiment 1 and experiment 2
to compare the global sperm mass transfer of males
with longer and shorter filaments with and without cuts.
Results
Correlative study in the field
In our correlative study in the field, male size and filament
length were uncorrelated (N033, r00.16, P00.36). The
time spent by a female watching a male display was
explained by male filament length (N 033, r 00.42, P 0
0.02, Fig. 1) and not by male size (N033 r00.04, P00.81).
Laboratory experiments
During experiment 1, 89.5 % (34/38) of females accepted at
least one sperm mass (60.5 % of females accepted a sperm
mass from a M+ male, 18.4 % from a M− male, and 10.5 %
from both males). Among males, 71.1 % of M+ and 28.9 %
of M− males successfully transferred a sperm mass to a
female. The latency between the beginning of the experiment and the first courtship display did not differ significantly between M+ and M− males (Wilcoxon signed rank
test, V0392, N076, P00.98).
Four models were retained to explain the number of sperm
masses transferred in experiment 1, among which the best had
a coefficient of determination of 33.3 % (Table S2). Filament
100
200
300
400
500
600
Behav Ecol Sociobiol (2012) 66:1045–1055
0
Time spent by female watching male displays (s)
1050
0
2
4
6
Filament length (mm)
Fig. 1 Relationship between the time spent by a female watching male
display and male filament length (N033, y025.5x+50.15, r00.42, P0
0.02). The variable “Time spent watching” represents the length of the
longest bout of the male display to a female
length, hind foot web size, PCbody size, and courtship activity
(but not PCbrightness and crest development) were included in
at least one model (Table S2). The number of sperm masses
transferred to a given female was best explained by
both male filament length and courtship activity, with
females taking more sperm masses from males having
longer filaments and higher courtship activity (Table S2,
Table 2, Fig. 2).
In experiment 2, the reduction of filament length
decreased the number of sperm masses transferred. During the entire experiment, only 53.3 % (32/60) of
females accepted at least one sperm mass, and this
number was significantly smaller than in experiment 1
(χ 2 012.2, df 01, P 00.001). The number of sperm
masses transferred of M− males (after filament shortening) was significantly smaller compared to M+ males in
experiment 1 (Wilcoxon rank sum test, W 01,666.5, N0
98, P < 0.001, Fig. 3), while the number of sperm
masses transferred of M+ males (after filament shortening) was similar compared to M− males in experiment 1
(Wilcoxon rank sum test, W01,163, N 098, P00.831,
Fig. 3).
In experiment 2, the latency between the beginning of the
experiment and the first courtship did not differ between M+
and M− males (Wilcoxon signed rank test, W0832, N0120,
P 00.544). Five models were selected by AICc and all
contained courtship activity (Table S2). The remaining variables included in at least one model were hind foot web
size, filament length, and PCcoloration (but not PCbrightness and
crest development; Table S2). The top ranked model
explaining male mating success had a coefficient of determination equal to 26 %. Model-average parameter estimates
showed that the number of sperm masses transferred increased with courtship activity (Table 2, Fig. 4). However,
contrary to experiment 1, filament length had very little
influence on the number of sperm masses transferred
(Table 2).
Discussion
Our approach combining behavioral observations in the
field and in the laboratory showed that female palmate
newts value both a morphological and a behavioral trait
Table 2 Effects of morphological and behavioral sexual traits on the number of sperm mass transfers for experiment 1 (exp1) and experiment 2 (exp2)
Parameter
exp1 (no. of sperm mass transfers)
exp2 (no. of sperm mass transfers)
Estimate
Unconditional SE
Confidence interval
Relative importance
Intercept
Hind foot web
PCbody size
Filament length
−0.52
0.42
−0.36
1.46
0.18
0.25
0.26
0.44
(−0.87, −0.17)
(−0.08, 0.93)
(−0.88, 0.16)
(0.61, 2.32)
0.55
0.44
1
Courtship activity
Intercept
PCcoloration
Filament length
Hind foot web
Courtship activity
1.06
−1.53
−0.33
−0.13
−0.53
2.48
0.35
0.25
0.32
0.33
0.34
0.47
(0.38, 1.74)
(−2.02, −1.04)
(−0.96, 0.31)
(−0.78, 0.51)
(−1.2, 0.14)
(1.55, 3.41)
1
0.32
0.12
0.61
1
In exp 1 female had the choice between two males (respectively with long and short filament length). In exp 2, we reversed the relative length of
filament before trial. The bold values indicate the variables selected after model averaging (i.e., for which the 95 % confidence interval did not
include zero). Fixed effects present in the full models: filament length, hind foot web, crest development, PCbody size, PCcoloration, PCbrightness, and
courtship activity. For details on the PCA see Table S4
2.5
2.0
1.5
1.0
0.5
0.0
Number of sperm mass transfers
a
1051
3.0
Behav Ecol Sociobiol (2012) 66:1045–1055
1
2
3
4
5
6
7
2.5
2.0
1.5
1.0
0.5
0.0
Number of sperm mass transfers
b
3.0
Filament length (mm)
0
200
400
600
800
1000
Time in courtship (s)
Fig. 2 Relationship between the number of sperm masses transferred
and a filament length and b the time spent in courtship during experiment 1. The females had the choice between a male with a long
filament and a male with a short filament length. Filament length was
not manipulated
when choosing a mate: the length of the tail filament and
courtship display activity. It further suggests that, when filament length is experimentally reduced, females may value the
information content of courtship activity over filament length.
Female mate choice for males with long filaments
Direct observations in the field revealed that females spent
more time watching males that had longer filaments. Our
result is congruent with previous work suggesting that
filament elongation may be the consequence of female preference in this species (Haerty et al. 2007). In a second step,
we experimentally tested female preference for filament
length in the laboratory. In this experiment, males with
longer filaments transferred more sperm masses to females
than males with shorter filaments, as predicted by our observations in the wild. However, we could not reject the hypothesis that female preference was directed to an unknown
factor correlated with filament length (e.g., hind foot web
size). We therefore experimentally reduced filament length,
while other traits were not manipulated. This reduction
decreased the number of male sperm masses transferred
compared to what was observed in the previous experiment.
Altogether, our three experiments provided strong evidence
that female palmate newts value the development of a morphological ornament, the filament length, to choose their
mates. Several not mutually exclusive hypotheses can explain why female palmate newts evolved a preference for
males with long filaments. First, such a preference could
result from a sensory bias, so that a higher length of filaments catch a female’s attention better (Basolo 1990; Ryan
and Rand 1990), as filaments strongly resemble the worms
that represent a major food resource for (female) newts.
Filament length could also be a reliable indicator of male
condition, so that only males in good condition can produce
and maintain long filaments, as previously reported for
interactions between filament length and environmental
stress (Secondi et al. 2007, 2009).
In our study, we observed a pre-copulatory female preference for males with longer filament length. However,
female newts can accept many sperm masses from the same
male and from different males, likely to allow sperm competition and cryptic post-copulatory female choice (Jones et
al. 2002; Garner and Schmidt 2003; Jehle et al. 2007).
Females of the alpine newt Mesotriton alpestris and smooth
newt L. vulgaris show cryptic mate choice, by favoring
sperm of particular males over others after accepting sperm
masses (Garner and Schmidt 2003; Jehle et al. 2007). Further work is therefore needed to evaluate true fitness consequences of the preference we observed in terms of number
of offspring produced.
Female mate choice for males with high courtship
activity
Our results failed to support a direct role of coloration and/
or body size on female preference, although there is increasing evidence of the use of coloration for mate choice in
amphibians (Rosenthal et al. 2004; Vasquez and Pfennig
2007; Maan and Cumming 2009; Gomez et al. 2009; Doucet and Mennill 2010; Sztatecsny et al. 2010), including
newts (Davis and Grayson 2008). Male filament length
Fig. 3 Number of sperm
masses transferred during
experiments 1 and 2 (without or
with filament shortening). M+
male with longer filament
length, M− male with shorter
filament length, exp 1 without
filament shortening, and exp 2
after filament shortening. The M−
males from this experiment had
longer filaments before the cut
and the M+ had smaller filaments
before the cut (see Table 1)
Behav Ecol Sociobiol (2012) 66:1045–1055
Number of sperm mass transfers
1052
***
1.8
1.6
1.4
1.2
1
NS
0.8
0.6
0.4
0.2
0
M+ (exp 1)
was, however, not sufficient to explain all of the variation in
male sperm masses transfer in our study, and courtship
activity also strongly predicted male sperm mass transfer.
This result indicates that a male with a small filament can
acquire access to reproduction if this male has a high courtship activity and that a male with a long filament but with a
very low courtship activity has a low likelihood to breed.
The importance of courtship to explain reproductive success
raises two conclusions. First, males increased their likelihood to breed by increasing their courtship activity, and
second, females selected males with the higher courtship
activity. Newt courtship activity is well described (Halliday
1975a; 1976), yet its potential to contribute to female mate
choice has received surprisingly little attention (but see
Vinnedge and Verrell 1998). Females of many species prefer
males exhibiting vigorous courtship displays, and measurements of courtship energy expenditure show that this activity may be costly (Vehrencamp et al. 1989; Kotiaho et al.
1998; Usherwood 2008; Hasselquist and Bensch 2008;
Byers et al. 2010; but see Dearborn et al. 2005). Courtship
can thus reveal many aspects of male quality, such as the
ability to cope with an immune challenge (Loyau et al.
2005a), body condition (Holzer et al. 2003), ejaculate quality (Matthews et al. 1997; Weir and Grant 2010), or heterozygosity (Drayton et al. 2010).
Female mate choice for multiple traits
Our study demonstrates that female palmate newts value
multiple traits during mate choice. Why males produce
and females assess several traits, and not a single one despite
the associated costs, remains an open issue in evolutionary
ecology (Møller and Pomiankowski 1993; Candolin 2003;
Bro-Jørgensen 2010). During courtship display, males present
and agitate their filament in front of females, a behavior likely
improving the perception and facilitating the assessment of the
M-(exp 2)
M-(exp 1)
M+ (exp 2)
filament length (Rowe 1999). Amplifiers may entail costs by
increasing conspicuousness to predators, thereby potentially
revealing their ability to escape predators (“amplifying handicaps” Hasson 1990; 1997; Berglund 2000; Castellano
and Cermelli 2010). In line with this idea, male palmate
newts can suffer from a high rate of filament predation in
habitats with high density of odonates and other insect larvae
(JC, personal observation). Because ornamentation acts in
conjunction with visual display, it is not clear whether the
exhibition of an ornament during courtship should be considered as several signals or a multi-component signal, and
whether a visual display could be viewed as an amplifier of
the ornament (Hasson 1989; 1990; 1991; Taylor et al. 2000) or
whether the filament length may amplify the expression of the
behavior (Hebets and Uetz 2000).
Morphological ornamental traits, such as the filament,
and behavioral traits (e.g., the courtship) vary in their flexibility and may also vary in their reliability, depending on
the stability of the ecological and/or social environment
(Hill et al. 1999; Loyau et al. 2005a, b; Baird et al. 2007;
van Dongen and Mulder 2008; Bro-Jørgensen 2010). For
example in field crickets Gryllus campestris, females based
their mate choice according to carrier frequency (link to
harp size development) and chirp rate, which provide
reliable information about past and present condition
(Scheuber et al. 2003, 2004). Assessing both filament
length and courtship activity, female palmate newts
could therefore gather information about male past and
present conditions to adaptively mate with high-quality males
(multiple message hypothesis, Møller and Pomiankowski
1993). However, to date, experimental evidence about the
relative flexibility of filament length and courtship activity is
lacking in the palmate newt. In newts, morphological sexual
traits could indicate male body condition (Green 1991). Moreover, the link between behavioral sexual traits and current male
quality remains unresolved in newts (but see Halliday and
2.5
2.0
1.5
1.0
0.5
0.0
Number of sperm mass transfers
a
1053
3.0
Behav Ecol Sociobiol (2012) 66:1045–1055
1
2
3
4
5
2.5
2.0
1.5
1.0
0.5
0.0
Number of sperm mass transfers
b
3.0
Time in courtship (s)
0
200
400
600
800
1000
1200
Time in courtship (s)
Fig. 4 Relationship between the number of sperm masses transferred
and a filament length and b the time spent in courtship during experiment 2. The females had the choice between a male with a longer
filament length and a male with a shorter filament length. Filament length
was shortened before trial, so that, in the pair of males, the male with the
longer filament length became the male with the shorter filament
Houston 1978). Additional work with newts and other species
is needed to clarify if morphological and behavioral sexual
traits could give information about past and current male
condition.
Female prioritization of behavioral traits over
morphological ones?
While evidence is accumulating that females often use multiple traits to choose their mate, relatively few studies have
explored how these traits are processed and integrated.
Choosers may assess multiple traits altogether to get a
global idea of the overall quality of potential mates, or
choosers may value one piece of information over another,
depending on the degree to which the information conveyed
is error-prone or particularly useful (Hebets and Papaj
2005). Because morphological and behavioral traits strongly
differ in their temporal sensitivity to individual condition,
females may weigh morphological and behavioral traits
differently in the mate choice process. Our results show that
when filaments were experimentally reduced and their relative length was reversed, male mating success was
explained by courtship activity and not by filament length,
suggesting that, in that case, females base their mate choice
on courtship activity.
In this experiment, the difference in filament length
(2 mm) between the two males was comparable to that in
experiments without filament length manipulation. According to the Weber–Fechner law, this difference should be
easier to assess for smaller filament length than for longer
filaments (Shettleworth 1998). Recently Akre et al. (2011)
elegantly demonstrated the relevance of this law during the
mate choice process. The authors showed that, for the same
discrepancy in ornament size, females were better able to
detect the difference in two small ornaments than in two
large ornaments. Thus, there is little likelihood that, in our
experiment, female newts were not able to detect the difference in filament length after filament manipulation. Instead,
our manipulation may have reduced filament length below a
certain stimulation threshold, so that females may not have
been stimulated by either of the two males. Another
interpretation is that females may have ignored an ornament (the filament) as a cue for mate choice because
females detected a lack of concordance in the development of two ornaments (the filament length and the
hind foot web size) that are normally correlated. Indeed,
females may commonly use several signals to avoid
mistakes (Johnstone 1996). In a recent experiment in
the tree frog Hyla arborea, females were provided with
the choice between two conflicting sexual traits, attractive call and unattractive vocal sac coloration or unattractive call and attractive vocal sac coloration. This
trial resulted in random female mating with respect to
the acoustic and visual traits manipulated (Richardson et
al. 2010). Finally, our results are consistent with the
hypothesis that, when the morphological signals are
expressed below a threshold, females may value the
information content of behavioral traits over morphological
ones because behavioral traits provide more accurate and reliable information on current male condition (Hill et al. 1999;
Loyau et al. 2005a; Baird et al. 2007; Bro-Jørgensen 2010).
To conclude, we found that female palmate newts use
multiple signals to choose their mates. Hence, in that species,
1054
females value both a morphological trait (the filament) and a
behavioral trait (courtship activity). Future investigation
should establish whether these two traits that may differ in
their temporal flexibility provide different kinds of information to the female.
Acknowledgments We are grateful to Sandrine Plénet and Claude
Miaud for discussing the results; Bob Montgomerie, László Z. Garamszegi,
and Philipp Heeb for discussions, statistical advice, and comments on the
manuscript; Géraldine Domisse and Thomas Jolly for help in gathering data
from experiment 2; and Olivier Calvez for technical assistance. We are
grateful to Philippe and Dominique Dupui, keepers of the Refuge des
Etangs de Bassiès for their help. The catching permits were no. 200913 (Ariège) and no. 2009-12 (Haute Garonne). This work was supported
by the Ministère de la Recherche (PhD fellowship to JC and two CNRS
grants to AL and DS), the BioDiversa-project RACE, and the Observatoire Homme-Milieu Pyrénées Haut-Vicdessos.
Ethical standards The experiments comply with the current laws of
the country in which they were performed.
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ARTICLE 3
It takes two to tango : Do both male and female
identities influence complex courtship display in a
newt species?
Cornuau JH, Courtoix EA, Jolly T, Schmeller DS, Loyau A.
En préparation
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It takes two to tango: Do both male and female identities influence complex courtship
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display in a newt species?
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Jérémie H. Cornuaua,*, Elodie A Courtoixa, Thomas Jolly a, Dirk S. Schmellera,b, Adeline
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Loyaua,b
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a
Station d’Ecologie Expérimentale du CNRS à Moulis, 09200 Saint Girons, France.
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b
Department of Conservation Biology, Helmholtz Centre for Environmental Research – UFZ,
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Permoser Strasse 15, 04318Leipzig, Germany.
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* Correspondence: J.H. Cornuau, Station d’Ecologie Expérimentale du CNRS à Moulis,
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09200 Saint Girons, France.
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E-mail address: [email protected] (J.H. Cornuau)
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Keywords: repeatability, behavioural consistency, sexual selection, mate choice, Lissotriton
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helveticus, palmate newt
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Abstract In many species, females base their mate choice on male courtship display.
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Although courtship display is consistent in term of behavioral sequence and structure within a
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given species, there is commonly important variation in the intensity of courtship display
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between and within males. Interestingly, only a few studies have investigated the different
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factors that can affect both between and within variability in courtship display intensity.
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Female traits can be an important source of within male variation. Therein, it is unclear what
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part of the variation in courtship display can be explained by males or females traits. In this
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experiment we tested whether several phases of a complex courtship display could be
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explained by both male and female identities in the palmate newts Lissotriton helveticus.
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Overall, we found that both male and female identities influence complex courtship behavior
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but the relative influence of each sex depended on the courtship phase considered. Male
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identity explained variation in fan and quiver display whereas female identity explained
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variation in quiver and touch tail display. The time spent in fan display appeared repeatable
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between males and we found no evidence of an effect of female identity. Finally we did not
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find any link between courtship display, and behavioral consistency and morphological traits.
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Our results provide, to our knowledge, the first example of significant inter-variation of
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courtship display in newts showing their potential importance to signal male identity.
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Additional experiments are now needed to determine whether courtship display indicates any
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aspect of male quality.
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Extravagant courtship displays consist of series of complex stereotyped behaviours
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that have evolved for sexual communication (Andersson 1994, Wachtmeister 2001, Mowles
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& Ord 2012). Courtship display is largely assumed to be costly to the male in terms of time,
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energy and exposion to higher predation risks (Andersson 1994). Generally, only males in
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good condition or highly motivated can maintain high courtship display activity (Zahavi 1975,
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Bradbury & Vehrencamp 2011, but see Lehtonen 2012, Mowles & Ord 2012). Therefore
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courtship display could be used by females during mate choice as an honest signal of male
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quality, and consequently courtship display behaviours could affect the regime of sexual
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selection (Jaquiéry et al. 2009, Schneider & Lesmono 2009, Loyau & Lacroix 2010).
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Although courtship display is consistent in terms of behavioural sequence and structure within
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a given species, there is commonly important variation in the intensity of courtship display
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between males (Bradbury & Vehrencamp 2011). Accordingly, the influence of variation
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among males in courtship display intensity on female mate choice has been the subject of
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much research (e.g. Künzler & Bakker 2001, Loyau et al. 2005a,b, Ward & McLennan 2009,
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Shamble et al. 2009). Another important source of variation, yet far less explored, is the
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behavioural plasticity of courtship display that can lead to important variation within males
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(Bell et al. 2009). The outcome of sexual selection could be strongly affected by such
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variation, especially when a poor quality male could momentarily be able to express
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behavioural display comparable to that of a high quality male (Lindström et al. 2009).
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Interestingly only a few studies have investigated the different factors that can affect both
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between and within male variation in courtship display intensity (Bell et al. 2009).
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Environmental heterogeneity is one major source of variation within male. Such
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variation can occur in response to environmental pressure such as predation (Fowler-Finn &
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Hebets 2011), environmental noise (Lengagne & Slater 2002, Brumm & Slater 2006, Wilgers
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& Hebets 2011), or spatial and temporal partner availability (Lindström et al. 2009). Less well
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studied, although equally important, is the influence of male and female individual
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characteristics as a source of within male variation (Patricelli et al. 2002, 2006). For example
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male desert gobies spent more time in courtship display towards larger females (Wong &
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Svensson 2009). In the wolf spider Schizocosa rovneri males increase courtship display (i.e.
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number of body bounces) when they receive a specific positive female feedback cue
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(Sullivan-Beckers & Hebets 2011). In contrast males can increase courtship display after a
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negative female feedback in an attempt to catch the female attention, and males can discount
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courtship display after a positive feedback, as in the convict cichlid Amatitlania nigrofasciata
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(Santangelo 2005). Within male variation can also differ among males. Indeed, in the wolf
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spider Schizocosa the males reduce their courtship display in presence of predator odor but
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this response to predation is stronger for more ornamented male, showing that behavioral
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plasticity can also depend on male characteristics (Fowler-Finn & Hebets 2011). Although
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courtship display behaviours can be driven by both male and female individual characteristics,
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it is not yet clear which part of the display is influenced by which sex and to which extent
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(Ruiz et al. 2008, Lehtonen et al. 2011). In this study, we extended recent findings on the
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importance of courtship display on female mate choice in the palmate newt Lissotriton
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helveticus (Cornuau et al. 2012, Cornuau et al. unpublished), and we examined which factors
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influence between and within male variation of the courtship display, including both male and
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female individual characteristics. We have previously found that the courtship display was
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variable between males but was not explained by male body condition (Cornuau et al.
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submitted, Cornuau et al. unpublished).
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To investigate behavioural plasticity of courtship display a widely adopted approach is
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to assess, in a given population, the temporal variation between and within males by
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performing successive mate choice trials (Bell et al. 2009). An advantage to this approach is
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that it allows calculating the repeatability of courtship display (Bell et al. 2009). Repeatability
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is defined as the part of variation in a trait that is explained by differences between individuals
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(Bell et al. 2009). A highly repeatable behaviour (e.g. male courtship display) is repeatable
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when it shows high variation between males associated to low variation within males, in other
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words when individuals behave differently from each other while behaving consistently
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through time (Widemo & Saether 1999, Bell et al. 2009). In contrast, a low repeatability could
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mean that the behaviour is highly variable within a male, or that there is a low variation
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between males associated to a low variation within males (Widemo & Saether 1999).
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Although many studies have described the behavioural displays of newts (see Wells 2007),
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only one study has investigated the repeatability of newt display behaviour (Michalak 1996,
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see Bell et al. 2009), and so far no study have performed experiment to investigated the
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relative influence of male and female characteristics on behavioural display. The aim of this
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study was to 1- investigate the importance of both male and female characteristics on the
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elaboration of complex courtship displays, 2- investigate the influence of both male and
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female morphological features on behavioral consistency.
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METHODS
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Courtship display in the palmate newt
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The palmate newt is a suitable model species to investigate the influence of male and
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female characteristics on behavioural display because newts use complex, stereotyped,
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elaborated courtship display that is known to influence female mate choice (Cornuau et al.
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2012). The internal fertilization and the use of spermatophore in this species require a close
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coordination between males and females. The complex courtship display of palmate newts
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combines multimodal cues; including visual, chemical and tactile cues. As in other European
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newt species the courtship display is composed of four phases (Wells 2007). During the first
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phase, named orientation, the male follows and smells the female before moving to her front.
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The second and the third phases are static and retreat displays. During these two phases the
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male newt performs fan, whip and wave behaviours (Table 1). Fan behaviour represents the
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longest and the most frequent behaviour in palmate newt display. The last phase is the
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spermatophore transfer, in which the coordination between the male and the female is
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necessary to ensure spermatophore transfer from the male to the female. During this phase the
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male creep before the female and performs quiver behaviour (Table 1). This behaviour
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corresponds to an offer to deposit a spermatophore to the female. The female then touches the
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tail of the male so that he deposes a spermatophore on the ground. To transfer the
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spermatophore, the female follows the male until her cloaca is above the spermatophore,
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allowing the female to take it.
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Laboratory experiment
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All individuals were originally captured by dip netting in one pond near to Caumont,
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France, during the breeding season (04-03-2012). We collected 24 male and 24 female newts
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(catching permits no. 2009-13). This sample size was big enough to measure repeatability
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(Bell et al. 2009). Newts were brought to the animal facility at the Laboratoire d’Ecologie
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Expériementale du CNRS de Moulis (France). The day following capture, the individuals
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were individually marked with subcutaneous implants of colored visible elastomers (VIE,
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Northwest Marine Technology, Washington, Shaw Island, WA, USA) at the basis of the legs.
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Newts were maintained in by unisex groups of six in tanks one week before the start of the
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experiment (52×33.5×29.5 cm) with approximately half water collected in their native pond
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and half tape water. A clay brick perforated with holes was placed in each tank to ensure
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shelter. Newts were maintained at 18°C (±1) under fluorescent tubes (ReptiSun 2.0, ZooMed)
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to simulate natural light with a cycle of 12 hours light/ 12 hours dark. Newts were fed ad
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libitum by daily provision of living daphnia collected in a semi natural pond. Newts were
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released in their native ponds immediately after the experiment (04-19-2012). Their captive
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time represented a very small part of their breeding season (two weeks on approximately three
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month).
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Measurement of morphological traits
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In male palmate newts, morphological sexual traits are composed of one filament at
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the end of the tail, two hind foot webs and a small crest on the back (Cornuau et al. 2012).
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These ornaments are only expressed during the reproduction period which corresponds to the
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aquatic phase of newt life. Individuals were measured the day after being caught. We
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recorded body mass using scale (accuracy: 0.01 g). We used Snout-Vent-Length (SVL), from
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the snout tip to the posterior end of the cloaca as body size index. We measured SVL and
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filament length by taking photos of the individuals on a millimeter paper background (grid 1
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mm2). We obtained sizes using the free software IMAGEJ v.1.28 (http://rsb.info.nih.gov/ij/).
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These measures are reliable and repeatable (Cornuau et al. 2012). We calculated body
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condition index of male and females using the residuals of the linear regression of the root
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cute of weight on SVL for each sex separately (Báncilá et al., 2010).
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Experimental design
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We aimed to investigate the consistency of males and females behaviour and the
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relative contribution of both males and females on several aspects of palmate newt courtship.
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Courtship display behaviours were assessed during dyadic encounters composed of one male
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and one female. Pairs of individuals were randomly made up, i.e. randomly with respected to
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morphological variables. Behaviours were observed three times: at day 1, the day after (day
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2), and finally six days after the first measure (day 6), for all individuals, resulting in a total of
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72 mate choice trials. However, all encounters were unique, i.e. each male could display to
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three different females, and each female encountered three different males. At the end of the
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experiment all 24 males and 24 females have performed three mate choice trials (one at day 1,
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one at day 2 and once at day 6).
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The mate choice trials were performed in an experimental tank (26×33.5×29.5 cm),
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from 08:00 to 12:00 am (Cornuau et al. 2012). Six mate choice trials were simultaneously
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performed, each in a separate tank, so that all individual 24 trials were conducted the same
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day. Each experimental tank contained 3 cm of sand and 8 cm of water. Before the trial,
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experiment tanks were divided in two parts, one for each sex, with a visual barrier. The male
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and the female were placed in each part of the experimental tanks during 5 min of
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acclimatization before the visual barrier was removed and individuals could interact freely
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during 40 min and this time was enough for the observations of sexual behaviours (Cornuau et
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al. 2012).
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Measurement of behaviour
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Each mate choice trial was recorded using a video camera placed above the
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experimental tank. The videos were analyzed with the software The Observer 7.0 (Noldus
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Information Technology). As explained in the introduction male palmate newts perform a
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complex display composed of several distinct behaviours, which are described in Table 1. We
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recorded the number of fan, whip and wave events performed by a given male over the 40
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minutes of the trial (static and retreat display, Table 1). Fan behaviour can last several
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minutes, so we also recorded the time spent in fan (Table 1). We counted the number of
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quivers and touch tail during the spermatophore transfer phase (Table 1). To avoid changes in
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female receptivity over the course of the experiment, we did not allow the females to take
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male spermatophores. Indeed female mate choice and female choosiness can change after a
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first mating (Gabor & Halliday 1997). To prevent spermatophore transfer, we stopped the
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female after touch tail using a glass rod. Both male and female still performed courtship
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behaviour immediately after this action (JHC personal observation). As we did not allowed
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spermatophore transfers to occur, we used the number of touch tail as a proxy of female mate
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preference. Touch tail is a good indicator of female receptiveness as it always precedes
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spermatophore transfer (Table 1). We identified this proxy using a personal data base
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containing 40 mate choice trials between one male and one female from the same population
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(JHC personal data). We found that touch tail was a great predictor of willingness to accepted
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a spermatophore (GLM, Z = 4.65, P < 0.001). Finally performing courtship in water may
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impose some costs to male newts so we counted the number of time the male surfaced to
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breath.
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Statistical analyses
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All statistical analyses were performed using R 2.13.1 software. First we tested
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whether the three static display behaviours (fan, whip and wave) performed by males during
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the experiment were correlated using Spearman rank correlations. Following this analysis we
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decided to use only the time spent in fan display as a proxy of the static display (Table 2). The
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time spent in fan corresponds to the most important courtship display behaviour in palmate
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newts (Cornuau et al. 2012).
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Secondly we investigated for each courtship display (time spent in fan display, number
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of quivers and number of touch tail) the relative influence of the day (day 1, 2 and 6), and
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both male and female identity. The time spent in fan display did not match with normality so
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we chose to work with non parametric statistics for this data set. Thus we used Kendall rank
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correlations to assess the effects of both male and female identities on the time spent in fan
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display. We used Kruskall Wallis tests to assess the effect of the day on the time spent in fan
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display. We used Poisson distribution of error terms both for the number of quivers and the
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number of touch tail behaviours. To estimate the variation in the number of quivers and the
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number of touch tail associated to male identity or female identity, we used general linear
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mixed effects models (package “lme4”). All models were fitted using the day (day 1, day 2 or
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day 6) as a fixed factor and both male identity and female identity as random factors. We
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assessed the statistical significance of fixed and random factors using log-likelihood tests by
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comparing a full model with reduced models without the fixed or random factor tested, and
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tested every possible model (Crawley 2007, Zuur et al. 2009). We used maximum likelihood
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(ML) to fit the models when models differed in their fixed factor.
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Thirdly we investigated the effect of morphology on the courtship display. We used
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Spearman rank correlations to test the link between time spent in fan display and male
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morphological characteristics (SVL, filament length, BCI, number of breathing events) and
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female characteristics (SVL and BCI). Then we assessed the influence of male morphological
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characteristics (SVL, filament length, BCI, number of breath event) and female characteristics
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(SVL and BCI) on the number of quivers and the number of touch tail using generalized
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linear mixed models with both male and female identity as random factors and morphological
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traits as fixed factors. Again we assessed the statistical significance of fixed and random
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factors using log-likelihood tests by comparing a full model with reduced models without the
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fixed or random factor tested (Crawley 2007, Zuur et al. 2009).
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Fourthly we investigated whether the variation in flexibility between individual was
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linked to morphological parameters. We used for each males and females the variance
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between the three tests as an estimate of the behavioral flexibility. Thus we tested whether the
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variance was explained by morphological parameters using an analysis of variance
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(ANOVA).
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RESULTS
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The correlation between filament length and male body size was not significant (r =
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0.24, df = 22, P = 0.28). The different behaviours performed by the males during the static
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displays were strongly correlated altogether (Table 2). Thus we subsequently used only the
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time spent in fan as a proxy of the static display.
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The number of males that did not perform at least one courtship display did not vary
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significantly between days (day 1: 1/24, day 2: 7/24, day 6: 3/24; χ2 = 1.14, df = 1, P = 0.28).
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We found that neither the variable day nor the female identity significantly explained the time
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spent in fan display (day: χ2 = 3.79, df = 2, P = 0.15; female identity: Wt = 0.34, χ2 = 23.7, df
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= 23, P = 0.42). However the male identity significantly explained the time spent in fan
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display (Wt = 0.56, χ2 = 38.9, df = 23, P = 0.02). We did not detect any effect of the male
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body size (rho = 0.11, P = 0.37), filament length (rho = -0.04, P = 0.76) or male BCI (rho =
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0.16, P = 0.17) on the time spent on fan display. Moreover we did not detect any effect of the
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female body size (rho = -0.03, P = 0.80) and the female BCI on the time spent in fan display
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(rho = 0.16, P = 0.19). However we found a positive link between the time spent in fan
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display and the number of breath events (rho = 0.27, P = 0.024). The variance in the time
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spent in fan display by males was not explained by the filament length (F1,20 = 0.79, P = 0.38),
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male body size (F1,20 = 0.01, P = 0.92) or male BCI (F1,20 = 0.59, P = 0.45). The variance in
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the time fan display was performed to a female was not explained by female body size (F1,21 =
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1.11, P = 0.31) or female BCI (F1,21 = 0.23, P = 0.63).
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We found a significant contribution of the day on the number of quivers (model 1 vs.
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model 4, χ2 = 19.95, df = 1, P < 0.001). Indeed the number of quivers decreased between day
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1 and day 2 (Paired Wilcoxon test: V = 246, df = 22, P = 0.001) and between day 1 and day 6
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(Paired Wilcoxon test: V = 148, df = 22, P = 0.007) but was constant between day 2 and day 6
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(Paired Wilcoxon test: V = 70.5, df = 22, P = 0.33). We found a significant contribution of
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both female and male identities on the number of quivers (female identity: model 1 vs. model
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4, χ2 = 5.02, df = 1, P = 0.025; male identity: model 1 vs. model 4, χ2 = 22.03, df = 1, P <
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0.001; Table 3). Male identity represented 28.3%, day 10.09% and female 7.77% of the total
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variance in the number of quivers. The residual variance, unexplained by the model,
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represented 53.84%. The number of quivers carried out by the males was not explained by
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male size (χ2 = 0.02, df = 1, P = 0.89), filament length (χ2 = 0.03, df = 1, P = 0.87) nor male
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BCI (χ2 = 2.36, df = 1, P = 0.12). The number of quivers performed to females was not
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explained by female body size (χ2 = 0.39, df = 1, P = 0.53) nor female BCI (χ2 = 0.53, df = 1,
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P = 0.47). The variance in the number of quivers by males was not explained by filament
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length (F1,20 = 0.82, P = 0.37), male body size (F1,20 = 0.02, P = 0.89) or male BCI (F1,20 =
278
0.07, P = 0.79). The variance in the number of quivers that were performed to a female was
279
not explained by female body size (F1,21 = 0.47, P = 0.50) or female BCI (F1,21 = 0.33, P =
280
0.57).
281
We found a significant contribution of the day on the number of touch tail (model 1
282
vs. model 4, χ2 = 27.26, df = 1, P < 0.001). Indeed the number of touch tail decreased between
283
day 1 and day 2 (Paired Wilcoxon test: V = 233.5, df = 22, P < 0.001) and between day 1 and
284
day 6 (Paired Wilcoxon test: V = 168.5, df = 22, P = 0.003) but was constant between day 2
285
and day 6 (Paired Wilcoxon test: V = 44.5, df = 22, P = 0.23). We did not found a significant
286
contribution of male identity on the number of touch tail (model 1 vs. model 4, χ2 = 1.03, df =
287
1, P = 0.31, Table 3). However we found a significant contribution of female identity on the
12
288
number of touch tail (χ2 = 20.33, df = 1, P < 0.001, Table 3). This means that whatever the
289
male identity, the number of touch tail was consistent within a female. The female identity
290
represented 34.12%, the day 24.21% and the male identity 3.51% of the total variance of the
291
number of touch tail. The residual variance, unexplained by the model, represented 38.16%.
292
The number of touch tail done by females was not explained by their body size (χ2 = 0.031, df
293
= 1, P = 0.86) nor their body condition (χ2 = 0.24, df = 1, P = 0.62). The number of touch tail
294
received by males was not explained by their body size (χ2 = 0.007, df = 1, P = 0.93), filament
295
length (χ2 = 0.96, df = 1, P = 0.33) or their BCI (χ2 = 1.97, df = 1, P = 0.16). The variance in
296
the number of touch tail done be the females was not explained by female body size (F1,21 =
297
0.02, P = 0.89) or female BCI (F1,21 = 0.14, P = 0.71). The variance in the number of touch
298
tail that males received was not explained by male body size (F1,20 = 0.13, P = 0.72), male
299
BCI (F1,20 = 0.39, P = 0.54) or male filament length (F1,20 = 0.26, P = 0.61).
300
301
DISCUSSION
302
The combined results of our study provide evidence of the influence of both male and
303
female identity on the expression of complex courtship display behaviours. We found that
304
both male and female identities influenced complex courtship behaviours but the relative
305
influence of both sex depends on the courtship phase. More precisely we found that the time
306
spent in fan display was explained by male and not by female identity. The number of quiver
307
displays was explained by both male and female identity, but the influence of female identity
308
was smaller than that of the male. Finally the number of touch tail behaviours was explained
309
by female and not male identity. We found also no significant influence of male or female
310
morphological traits (body size, body condition, and filament length) that could explain the
311
individual consistency. Altogether our results are one of the few that dissected the different
13
312
sources of variation that can affect behavioural repeatability of courtship display and provides
313
to our knowledge the first example in newts of significant within male variation in courtship
314
display.
315
In our study, although females varied greatly in their body size, body condition and
316
reproductive receptivity (measured by the number of touch tail), the time spent in fan display
317
was only explained by male identity. Thus the time spent in fan display seems to reflect male
318
ability to perform this behaviour and to not be influenced by any female characteristic we
319
measured. One possibility is that male palmate newts use a fixe strategy in term of the time
320
spent in fan display and not a strategy involving behavioral plasticity. Other sources of
321
variation not measured in this study could yet occur. Indeed courtship display could be
322
flexible according to environmental conditions, unmeasured in this study because laboratory
323
conditions remained constant over the course of the experiment. For example fan display of
324
the Alpine newts, Ichthyosaura alpestris, was affected by light condition and water
325
temperature (Denoël et al. 2005, 2010). Further investigations on the relative plasticity of
326
male fan display are necessary, especially in heterogeneous environment.
327
Contrary to the time spent in fan display; quiver display appears to be driven by both
328
male and female identify. Quiver behaviour seems more labile and male could adjust the
329
frequency of this behaviour according to female characteristics. A quiver represents a male
330
offer to deposit a spermatophore, and it has been suggested that this behaviour is influenced
331
by both male and female characteristics although the role of each sex remains unclear
332
(Halliday 1975). Our results show that both male and female identity influence the number of
333
quivers, and the influence of male identity still appeared to be more important that of female
334
identity. During the courtship display the male could respond to the female cue signaling her
335
receptivity, as the female moves towards the male, by the quiver behaviour that could lead to
336
spermatophore transfer (Halliday1975). Moreover we also observed in a previous study that
14
337
when males and females were separated for a long time more quivers probably due to an
338
increase in male motivation and/or a low selectivity of the females (JHC, personal
339
observation). It is probably adaptive to adjust the quiver behaviour to female receptivity to
340
access more rapidly to the spermatophore transfer phase. In this study we did not identify any
341
male or female features, such as body condition or size, that could explain the number of
342
quivers. However in a previous experiment in which we conducted an experimental diet
343
limitation we have found that males in lower condition tend to make more quivers (JHC, DS,
344
AL unpublished data). Additional work is clearly necessary to further determine which both
345
male and female features may explain the number of quivers.
346
We found, in agreement with our previous experiment (Cornuau et al. 2012), an
347
important variation in the proxy of male attractiveness (measured here by the number of touch
348
tail). Surprisingly, we did not detect any effect of male identity caused by important intra
349
individual variation in their attractiveness to females. Yet we found a significant effect of
350
female identity that explained the number of touch tail and which suggest an inter individual
351
variation in female receptivity or choosiness. Altogether these two results show that, firstly,
352
female mate preference seems not to be directed toward the same males. Indeed if all females
353
would have shown a preference for the same males or same male characteristics, we would
354
have detected a positive effect of male identity. Secondly female mate choice is better
355
explained by female identity than male identity, an argument in agreement with free female
356
mate choice in this species. In this study, the positive effect of female identity to explain the
357
number of touch tail event was not affected by female characteristics such as size or body
358
condition index. However we could not take into account the past history of female and the
359
number of mate encounters in the pond before the experiment that could create difference in
360
female selectivity and explain the observed influence of female identity (Gabor & Halliday
361
1997).
15
362
We found a relative consistency of male courtship display and female receptivity.
363
Within individual constancy in behaviour and particularly in courtship is well documented in
364
several taxa but rarely in salamander (Bell et al. 2009). Yet, within individual constancy in
365
behaviour is crucial in evolution because such inter individual variation give the opportunity
366
to selection especially via female mate choice (Jennions & Petrie 1997). Moreover within
367
individual constancy in behaviour is also crucial to such behaviour to be informative about
368
male quality (Jennions & Petrie 1997). In a recent meta-analysis of repeatability, Bell et al.
369
(2009) found that in average 35% of the variation among individuals is attributed to
370
individual differences, this result being consistent with what we found in this study. As fan
371
display was known to be a key factor that explain reproductive success in palmate newts
372
(Cornuau et al. 2012) our study highlights the opportunity to sexual selection via female mate
373
choice to shape courtship signal.
374
We found a significant effect of the day on the number of quivers, the number of touch
375
tail and not on the time spent in fan display. The influence of the day was however lower than
376
the influence of male identity and that of female identity to explain respectively the number of
377
quivers and the number of touch tail. The influence of the day might reflect an increase of
378
both male and female selectivity after the first trial. Indeed, in species with multiple mating
379
empirical evidence shows that individual selectivity increases after first a encounter especially
380
after a first mating with a high quality partner (Jennions & Petrie 2000). This strategy has
381
been found in newts (Gabbor & Halliday 1997). However in this experiment we did not
382
allowed spermatophore transfer to the female to avoid this problem. Yet our repeated design
383
might have created habituation or stress that affected every individual differently. However,
384
whatever the cause of variations observed for quiver and touch tail between days, these
385
variations were taken into account in our models and should not overestimate but may rather
386
underestimate our measure of behavioural constancy.
16
387
To conclude we found, for the first time in a newt species, a significant inter-
388
individual variation of courtship effort. Our study shows also that both male and female
389
identity influence in various ways the different phases of the complex displays of newts. As
390
the morphological traits we measured (body size, body condition and development of a sexual
391
trait) did not contribute to explain within male and within female variation in behaviour,
392
individuals characteristics explaining these variations remainted to be identified by future
393
investigations.
394
395
Ethical standards The experiments comply with the current laws of the country in which
396
they were performed.
397
398
Acknowledgements We are grateful to Laurence Walder for her help to collected data and
399
Adelaïde Sibeaux for her valuable and accurate comments on the manuscript. Financial
400
support was provided by the Ministère de la Recherche (PhD fellowship to JC and two CNRS
401
grants to AL and DS), the BioDiversa-project RACE, and the Observatoire Homme-Milieu
402
Pyrénées Haut-Vicdessos. This work was supported by the "Laboratoire d’Excellence
403
(LABEX)" entitled TULIP (ANR -10-LABX-41).
404
405
406
407
408
17
409
TABLES
410
Table 1 Courtship display behaviours of male palmate newts.
Display
Phase static and retreat
display
Fan
Description
The male folds his tail against his flank and the distal portion
of the tail vibrates.
The male rapidly brings back his tail against his flank.
The male holds his tail to be presented with a full view to the
female.
Whip
Wave
Phase spermatophore transfer
Quiver
411
After creep and follow, the male quivers his tail. This
behaviour could be assimilated to an offer to deposit a
spermatophore to the female.
Touch tail
Female move toward the male and touch the tail of the male.
Male put spermatophore on the floor (deposition).
Spermatophore transfer*
Female following male’s tail and take spermatophore.
*this behaviour was not assessed in this study (reason explained in the method section)
412
413
Table 2 Results from Spearman correlations between behavioural measures in male palmate
414
newts. *** : p<0.001, nb : number.
Fan (tps)
Fan (nb)
Whip (nb)
Wave (nb)
0.78***
0.51***
0.51***
Whip (nb)
0.74***
0.99***
Fan (nb)
0.73***
415
416
417
418
18
419
Table 3 The results of linear mixed effects models of number of quivers in male palmate
420
newts and number of touch tail in female palmate newts. The ΔAIC was the difference
421
between the best model and the model of interest.
422
Response
Model
Fixed factors
Random factors
AIC
ΔAIC
Quiver
1
Day
Male ID, Female ID
170.9
0
4
Day
Male ID
173.9
3
Male ID, Female ID
188.8
17.9
2
Touch tail
3
Day
Female ID
190.9
20
3
Day
Female ID
155.3
0
1
Day
Male ID, Female ID
156.3
1
4
Day
Male ID
174.6
19.3
Male ID, Female ID
181.6
26.3
2
423
424
425
426
427
428
429
430
431
432
19
433
FIGURE
Time spent in fan display
a)
2000
1600
1200
800
400
0
35
36
37
38
39
40
Male body size (SVL, mm)
41
42
434
Time spent by in fan display
b)
2000
1600
1200
800
400
0
38
40
42
44
Female body size (SVL, mm)
46
435
436
Figure 1. Time spent in fan display by males plotted against a) male body size and b) female
437
body size. Successive measures of a given male are connected by a solid line. Gray and dark
438
dots represent respectively two and three superposed dots.
439
440
441
20
442
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24
ARTICLE 4
Condition-dependance of multiple sexual traits in the
palmate newt (Lissotriton helveticus).
Cornuau JH, Pigeault R, Schmeller DS, Loyau A.
En préparation
1
Condition-dependence of multiple sexual traits in the palmate newt (Lissotriton
2
helveticus)
3
4
Jérémie H. Cornuaua • Romain Pigeaulta • Dirk S. Schmellera,b • Adeline Loyaua,b
5
a
6
09200 Saint Girons, France
7
b
8
Permoser Strasse 15, 04318 Leipzig, Germany
Station d’Ecologie Expérimentale du CNRS à Moulis, 2-4 Route du CNRS, Moulis Village,
Department of Conservation Biology, Helmholtz Centre for Environmental Research – UFZ,
9
10
Correspondence to J. Cornuau.
11
Email: [email protected]
12
Phone: + 33 5 61 04 03 60
13
Fax : + 33 5 61 96 08 51
14
15
16
17
18
1
19
Abstract Why females evaluate more than one sexual trait to choose their mates has received
20
increasing attention in recent years. The redundant messages, the multiple messages and the
21
unreliable signals hypotheses are the three main theories put forward to explain the evolution
22
of preference for multiple signals. To test these hypotheses, we examined the co-variation of
23
multiple traits with two aspects of male condition in the palmate newt Lissotriton helveticus.
24
We measured body condition and experimentally injected males with an antigen (LPS) to
25
manipulate health status. The development of three morphological sexual traits (filament
26
length, hind-feet-web size, and crest size) was positively correlated (suggesting a relationship
27
and no trade-off between these traits), and were related to the body condition. These results
28
support the redundant messages hypothesis. In contrast, the development of the sexual traits
29
was not affected by the experimental treatment (LPS vs. saline solution). Courtship frequency
30
was not influenced by any aspect of male condition we measured, rather providing some
31
support for the unreliable signal hypothesis. Our results suggest that females likely obtain
32
redundant information on male condition when evaluating filament length, hind-feet-web size,
33
and crest size during mate choice, and may obtain unreliable information when assessing
34
courtship activity alone. Our results further suggest that complex, multiple traits may evolve
35
because redundant messages, multiple messages and unreliable signals can coexist.
36
37
38
39
Keywords Sexual selection • Multiple signal theory • Redundancy • Back-up signal • LPS •
40
Lissotriton helveticus
41
42
43
2
44
Introduction
45
In many species, females assess several sexual traits during mate choice such as
46
coloration, morphological structures, calls and behavioral displays (Candolin 2003, Grether et
47
al. 2004, Hebets and Papaj 2005). Usually, females prefer mating with the males that are able
48
to express the most extravagant, conspicuous, sexual traits. This preference has been
49
explained by the cost of expression and maintenance of the traits, so that only males in good
50
condition can afford these costs. The development of a trait then reliably signals male quality
51
to the choosing females by co-varying with condition (Zahavi 1975, Johnstone et al. 2009).
52
For example, females could base their choice on male coloration because coloration is a good
53
indicator of male body condition (McGlothlin et al. 2007, Griggio et al. 2011, Taylor et al.
54
2011) or male immune abilities to cope with parasites and pathogens (Faivre et al. 2003;
55
Alonso-Alvarez et al. 2004; Baeta et al. 2008). In contrast, it has been argued that an
56
exaggerate male trait can evolve even if it is unreliable, as long as the trait is heritable and
57
female preference for this trait is heritable too (Fisher 1930).
58
If females can assess male attractiveness or quality using only one single trait, why do
59
females commonly use several, multiple, traits during mate choice? This question has
60
received growing consideration over the two past decades and continues to be an active
61
research area (Candolin 2003, Hebets and Papaj 2005, Bro-Jørgensen 2010). To date, several
62
theories have been developed to explain the evolution and maintenance of multiple sexual
63
traits and have been explored with mathematical models (reviewed by Candolin 2003). First,
64
the unreliable signal hypothesis proposed that the costs of secondary sexual traits and the
65
costs of assessing multiple traits should favor a single most-revealing trait, and thus other
66
additional traits should be unreliable (Møller and Pomiankowski 1993, Iwasa and
67
Pomiankowski 1994). Therefore, the expression of only one trait should co-vary with an
68
aspect of male condition. Secondly, unreliable traits may have evolved or be maintained
3
69
because they enhance the probability that the reliable signal is perceived, making it easier to
70
assess male attractiveness (amplifiers, Hebets and Papaj 2005). Thirdly, it has been shown
71
that the evolution of multiple traits can also be based on multiple condition-dependent sexual
72
traits (van Doorn and Weissing 2004, 2006), with each trait being related to a different aspect
73
of male condition (the multiple message hypothesis). Alternatively each condition-dependent
74
trait can be linked to the same aspect of male condition with a certain error (the redundant
75
signal hypothesis; Møller and Pomiankowski 1993). In this case, the redundant traits should
76
be correlated to each other, should co-vary with a given measure of individual condition, and
77
mate choice should be more accurate when several traits are used compared to only one trait
78
(Møller and Pomiankowski 1993, Partan and Marler 1999, 2005). Finally, an empirical work
79
suggested that the unreliable signal, multiple message and redundant signal hypotheses are
80
not necessarily mutually exclusive (Doucet and Montgomerie 2003). Indeed, these authors
81
showed that, in the Satin bowerbird Ptilonorhynchus violaceus, both the multiple message and
82
the redundant signal hypotheses contribute to explain the evolution of multiple sexual traits.
83
Despite the fact that Doucet and Montgomerie (2003) predicted that future studies will reveal
84
additional examples of such a “mosaic” of multiple signals, to our knowledge, no further
85
example has been identified so far.
86
Several approaches have been proposed to experimentally challenge the unreliable
87
signal, the multiple message and the redundant signal hypotheses (Partan and Marler 1999,
88
2005; Candolin 2003; Hebets and Papaj 2005). One approach consists in examining the
89
intensity of the receiver’s response to each trait separately versus altogether (Partan and
90
Marler 1999, 2005). Similar responses are interpreted as redundant traits whereas different
91
responses are interpreted as non-redundant traits. However, it is not always possible to
92
manipulate each trait separately with non-invasive methods. Another approach focuses on the
93
relationships between the traits and the information content of the traits, with similar
4
94
information content interpreted as redundant traits (Candolin 2003; Hebets and Papaj 2005).
95
Interestingly, these two approaches could lead to opposite conclusions about trait redundancy.
96
Indeed, two traits could provide similar responses (i.e. redundant) while reflecting different
97
pieces of information (i.e. non-redundant). We investigated the evolution of multiple traits in
98
the palmate newt using the information-content approach. This second approach entails 1)
99
examining whether the expression of each trait co-varies with male condition to explore the
100
information content of the trait (reliable or unreliable trait), 2) testing whether multiple traits
101
co-vary and if so positively or negatively (redundant or multiple traits), and 3) investigating
102
correlations and trade-offs with several aspects of male condition (redundant or multiple
103
traits).
104
We applied this framework in an amphibian, the palmate newt Lissotriton helveticus.
105
Male palmate newts display multiple conspicuous sexual traits that females assess during
106
mate choice (Haerty et al. 2007, Cornuau et al. 2012). These traits include both morphological
107
traits (a caudal filament at the end of the tail, a small crest on the upper part of the tail and
108
hind-foot-webs) and courtship display behaviors (Cornuau et al. 2012). Additional sexual
109
traits may also play an important role in determining female mate choice, such as pheromones
110
or genetic relatedness, as they do in closely related newt species (Garner & Schmidt 2003,
111
Jehle et al 2007, Houck 2009). Males of the palmate newt with more conspicuous
112
morphological and behavioral sexual traits transfer more sperm masses to the females
113
(Cornuau et al.2012). However, the information content of these multiple traits is still
114
unraveled. To address this issue we have tested whether the expression of sexual traits
115
assessed by females co-vary altogether and with male condition. To test the condition-
116
dependence of the multiple sexual traits we used two classical methods: a measure of body
117
condition and the response to an experimental injection of an antigen (gram-negative bacterial
118
lipopolysaccharides, LPS; Cotton et al. 2004).
5
119
120
Material and methods
121
Reproductive behavior in the Palmate newt
122
In the palmate newt after the terrestrial phase, males and females gather in aquatic ponds for
123
the breeding season (Griffiths and Mylotte 1988). In this species, courtship display is
124
composed of several phases (Halliday 1975, Cornuau et al. 2012). In the first phase named
125
orientation, the male searches and follows the female, using his hind-foot-webs and tail
126
(Halliday 1975). Then, the male places himself in front of the female and presents his tail
127
(with crest and filament) in full view to the female and produces three different behaviors
128
named whip, fan and wave with his tail, crest and filament (Halliday 1975). A whip represents
129
a rapid movement in which the male snaps his tail against his flank before making the fan.
130
The fan is a rapid vibration of the distal part of the tail including the filament that creates a
131
water flow towards the female’s head. During fan, the two hind-foot-webs could be crucial for
132
the male to maintain the upper part of his body immobile. Wave is a movement of the tail of
133
the male where he presents his tail including crest and filament in full view to the female. At
134
any time the female can stay or move away according to her interest for the male (Cornuau et
135
al. 2012). Courtship display in front of a female can last from a few seconds to more than 10
136
minutes (JHC personal observation). A female can watch several males over a short period of
137
time and can easily compare males according to their morphological and behavioral features.
138
The spermatophore transfer phase begins with the male’s offer to deposit a spermatophore to
139
the female with a small movement with his tail named quiver. Again the female has a full
140
view on the male tail. The female can accept or refuse spermatophore deposition by the male,
141
depending on whether she touches the extremity of the male tail or not. After spermatophore
142
deposition, the male places his body perpendicular to the female body and the female is
6
143
guided by the male so that her cloaca is on the spermatophore. Finally the female can transfer
144
the sperm mass in her cloaca.
145
146
Laboratory experiment
147
Palmate newts were captured in April 2011 during aquatic phase in their natural breeding site
148
(Etang Bouteve, Mourtis, France, altitude: 1682 m). Before the experiments, the individuals
149
were individually marked with subcutaneous implants of colored visible elastomers (VIE,
150
Northwest Marine Technology, Washington, Shaw Island, WA, USA) at the basis of one of
151
the four legs. During their entire captivity newts were fed ad libitum with larvae of
152
chironomids, daphnia and tubifex. A total of 123 males were included in our experiment.
153
To explore the trade-offs between sexual traits and male condition we used two
154
common methods (Cotton et al. 2004); 1) we measured natural variation in body condition
155
(Baker 1992, Băncilă et al. 2010), and 2) we injected newts with bacterial-wall
156
lipopolysaccharide (LPS). The use of the body condition index was probably the most
157
widespread and validated measure of male quality (Cotton et al. 2004). In amphibians the use
158
of the body condition index as an index of male quality is widespread particularly to study the
159
condition dependence of sexual traits (Green 1991, Baker 1992, Judge & Brook 2001). This
160
measure reflects the lipid content in newts (Denoël et al. 2002) and body condition in other
161
species (Cotton et al. 2004; Schulte-Hostedde et al. 2005) and was recently recommended for
162
the monitoring of amphibian populations (Băncilă et al. 2010).
163
The LPS is an antigen that mimics a bacterial attack and is readily recognized by a
164
host’s immune system (Llewellyn et al. 2011). Its constituents are among the most potent
165
activators of both innate and humoral immune processes of a vertebrate host, including
166
amphibian hosts (Table S1). We conducted a literature search to gather information regarding
167
the use of LPS in different types of experiments and on the largest number of species
7
168
possible. The results of this research revealed that only three amphibian species, all anurans,
169
were already injected with LPS (Bufo marinus, B. paracnemis and Xenopus laevis) and that
170
the response time to the immune challenge was found to be 1 to 30 days (Table S1). It also
171
allowed us to determine the concentration, volume and location of the LPS-injection for our
172
experiment (see Table S1). Newts were injected intraperitoneally with 0.02 mL of a solution
173
composed either of LPS (Escherichia coli serotype 055: B5, Sigma, Lyon) in saline solution
174
(0.9%), or of saline solution only. Thirty three newts were challenged with 0.14 mg of
175
LPS/ml (low dose, which approximately corresponds to a 2 mg of LPS/kg for an average
176
sized-individual of 1.4g as by Llewellyn et al. 2011 in B. marinus and Bicego et al. 2002 in B.
177
paracnemis, Table S1), 30 newts with 0.7 mg of LPS/ml (high dose, which approximately
178
corresponds to a 10 mg of LPS/kg for an average sized-individual, Table S1), and 60 newts
179
with a saline solution (control). Due to the small body mass of newts and the low resolution of
180
the standard tuberculin syringe used, we could not adjust the injected volume to SVL or body
181
mass. However, we took this individual difference into account by including SVL as a
182
covariate in the models. After injection, each individual was placed in an opaque tank
183
together with 11 other individuals. Tank groups were composed of 6 males injected with LPS
184
(both males injected with low and high doses) plus 6 males injected with the saline solution
185
(except for three tanks in which 7 males were injected with a low dose of LPS). Tanks
186
contained 10 liters of water, plants collected in the native environment of the newts, one
187
shelter perforated with 17 holes, and an air-pump to oxygenate the water. The temperature
188
was kept constant at 18°C (±1) and we used daylight lamps (Reptisun 2.0, ZooMed) to
189
simulate the natural light spectrum with a natural light/dark cycle (12h:12h).
190
Morphological sexual traits were measured at the start of the experiment, and 32 days
191
later at the end of the experiment. The length of the experiment was determined by a
192
preliminary experiment (JHC, data on demand). We recorded body mass with a digital scale
8
193
(accuracy: 0.01 g) and measured Snout-Vent-Length (SVL) using a photo taken on a
194
millimeter paper background (grid 1 mm²). In the same way, we measured filament length,
195
hind-foot-web size and crest size (Green 1991). The photos were analyzed using the ImageJ
196
software (http://rsbweb.nih.gov/ij/), a reliable and repeatable method for morphological
197
measures as shown earlier (Cornuau et al.2012). The body condition index (BCI) was
198
calculated for each individual using the residual of the linear regression of the cube root of
199
body mass on SVL, as recommended for amphibians (see Baker 1992 and Băncilă et al.
200
2010). The development of morphological traits was calculated as the value of the trait
201
measured at the start of the experiment minus the value of the trait measured at the end of the
202
experiment (Δ trait= traitend - traitstart). The development of morphological sexual traits (Δ
203
trait) did not differ between tanks (Kruskal-Wallis rank sum test, Δ filament length: χ² = 8.66,
204
df = 9, P = 0.47; Δ crest size: χ² = 8.12, df = 9, P = 0.52; Δ hind-foot-web size: χ² = 1.35, df =
205
9, P = 0.99). After the experiment, the individuals were released in their original breeding
206
site.
207
208
Outdoor experiment
209
Newts (60 males and 45 females) were collected during their reproductive period (10 May
210
2011) in a natural pond (Caumont, France, altitude: 438 m). They were individually marked
211
with VIE (Visible Implant fluorescent Elastomer) and measured for morphological sexual
212
traits (SVL, weight and filament length) as described above for our laboratory experiment.
213
The individuals were then placed in three outdoor tanks of a volume of 1000 liters by groups
214
of 20 males and 15 females per tank. Each tank was covered by a net to avoid flight and
215
predation, was filled with water, and contained aquatic plants from the pond of origin and
216
shelters. In this experiment, courtship frequency of each male was measured by counting the
217
number of times a given male was observed in courtship. Three sessions of observations (S0,
9
218
S1 and S2) were performed during this experiment. One session corresponded to three days of
219
observation and each session was separated by three days. In the first session of three days
220
(S0), behavioral observations were conducted continuously from 6:00 am to 7:00 pm. It
221
allowed to determine the time of day where most males interacted with females, which was
222
between 6:00 am and midday and between 5:00 pm and 7:00 pm. In the following sessions S1
223
and S2, the observer did perform subsequent observations during the activity peaks.
224
During each session (S0, S1 and S2) the observations were performed by one observer (RP)
225
walking around the three tanks until seeing a courting male. Daily observations corresponded
226
to a succession of 15 min of focal observations during which one tank was observed at a time
227
and all individuals in the tank observed altogether. Every 15 min, a different tank was
228
observed, and the tank order was changed everyday. Globally all tanks were similarly
229
observed, so the likelihood to observe male courtship was constant between tanks and there
230
was no effect of tank identity on the total courtship frequency observed in the tank (F1,54 =
231
1.24, P = 0.27). VIE marking did not allow remote identification of individuals. The courting
232
male was therefore caught using a net, identified and immediately released in the tank. We
233
counted the number of times each newt was seen in courtship activity during each session
234
over three days. If a male was seen two times in courtship it scored 2, whereas if a male was
235
seen twenty times in courtship it scored 20. Thus we obtained an index value of courtship
236
frequency of each male and were unable to assess courtship duration or any other measure of
237
intensity of display effort.
238
Male newts were assigned to the experimental treatment the night before S1 and the
239
night before S2. In each tank, at around 11:00 pm, 10 males were injected with a saline
240
solution and 10 males with LPS (10mg/kg) and immediately released back in their initial
241
outdoor tank. Courtship frequency was recorded the day following injection, and for a total of
242
three days (observation session S1). Then, females were removed from the tank for a three-
10
243
day period without observation, and placed back before the second injection of the males.
244
Males were injected a second time and a second observation period (S2) was performed under
245
similar conditions as described above. Post-injection courtship frequency was defined as the
246
total number of courtship observed during the two observational periods S1 and S2. At the
247
end of the experiment, morphological traits were measured again, and all newts were released
248
in their original breeding site.
249
250
Statistical analysis
251
Statistical analyses were performed using R (R development core team 2009, version 2.9.2).
252
First, we checked if male morphological traits (filament length, hind-foot-web size, crest size,
253
SVL and weight for the laboratory experiment; filament length, SVL, weight and courtship
254
frequency for the outdoor experiment) were homogenously distributed among experimental
255
treatments (saline, low and high doses of LPS) using a MANOVA test (laboratory
256
experiment: F2,10 = 0.88, P = 0.56; outdoor experiment: F1,4 = 0.10, P = 0.81).
257
Then, we used linear mixed models (LMMs) because assumptions for parametric
258
analyses were met (all LMMs had a Gaussian distribution of error terms), the link function
259
was identity. We built LMMs to explore relations between pairs of Δ traits (Δ filament length,
260
Δ crest size and Δ hind-foot-web size). In these models, we included the experimental
261
treatment (0, 2 and 10 mg/kg of LPS), Δ SVL and two-factor interactions as fixed variables,
262
and tank identity as a random variable. Including Δ SVL as a covariate controlled for
263
potential effects of Δ body size (Cotton et al. 2004). We evaluated the effect of the random
264
factor (tank identity) by testing whether its removal from the model caused a significant
265
decrease in the model fit and found that this random effect was never significant (all P >
266
0.05).We used linear mixed models (LMMs) to investigate the impact of the experimental
267
treatment (high dose vs. saline, low dose vs. saline, and low vs. high dose) on Δ traits (Δ
11
268
filament length, Δ hind-foot-web size and Δ crest size). We investigated whether Δ traits co-
269
vary with Δ BCI using LMMs with BCI, experimental treatment and two-factor interactions
270
as fixed variables, and tank identity as a random variable. Again, this random effect was never
271
significant. For the outdoor experiment, examined the relationship between S1 and S2 using a
272
LMM, with S2 as a fixed variable and tank identity as a random variable. We used LMMs to
273
test the effect of the LPS treatment and the body condition on courtship frequency, with tank
274
identity as a random variable. We investigated also, with LMMs the link between courtship
275
frequency, filament length and SVL.
276
277
Results
278
Laboratory experiment
279
Over the experiment, the size of the morphological traits did not remain constant. There was a
280
significant increase in SVL (paired t-test, t122 = 9.95, P < 0.001), body weight (paired t-test,
281
t122 = 15.95, P < 0.001), filament length (paired t-test, t122 = 3.63, P < 0.001) and hind-foot-
282
web size (paired t-test, t122 = 2.40, P = 0.018). In contrast, crest size showed a significant
283
decrease (paired t-test, t122 = -3.82, P < 0.001). Delta filament length, Δ hind-foot-web area
284
and Δ crest area were positively related (Table 1 and Table S2), and these relations were not
285
affected by Δ SVL and LPS treatment (0, 2 and 10 mg/kg; Table 1).
286
Contrary to our prediction Δ filament length, Δ hind-foot-web size and Δ crest size
287
were not affected by the injection of neither a low dose (Δ filament length: F 1,61 = 0.55, P =
288
0.46, Δ hind-foot-web size: F 1,61 = 0.01, P = 0.91 and Δ crest size: F 1,61 = 0.007, P = 0.94),
289
nor a high dose of LPS (Δ filament length: F 1,58 = 0.28, P = 0.60, Δ hind-foot-web size: F 1,58
290
= 0.001, P = 0.97 and Δ crest size: F 1,58 = 0.30, P = 0.59). Generally, there was no difference
291
between low and high dose treatments (Δ filament length: F 1,61 = 3.43, P = 0.07, Δ hind-foot-
292
web size: F 1,61 = 0.53, P = 0.47 and Δ crest size: F 1,61 = 0.84, P = 0.36). However, each
12
293
morphological sexual trait was significantly and positively influenced by the variation in BCI
294
(Table 2, Fig. 1). An increase in male Δ BCI marked an increase in Δ filament length, Δ crest
295
area and Δ hind-foot-web area, and was not affected the experimental treatment (Table 2, Fig.
296
1).
297
298
Outdoor experiment
299
Males that performed more courtships in the first observation session (S1) performed
300
also more courtships in the second session (S2) (F 1,54 = 232.33, P < 0.001). Post-injection
301
courtship frequency (S1+S2) was not explained by the experimental treatment (F1,52 = 0.98, P
302
= 0.33), BCI (F1,52 = 0.09, P = 0.76) or their interaction (F1,52 = 0.01, P = 0.91). However,
303
courtship frequency was significantly related to the SVL at the end of the experiment (F1,52 =
304
6.62, P = 0.013) and marginally to filament length (F1,52 = 3.39, P = 0.071) but not to their
305
interaction (F1,52 = 0.08, P = 0.78). Our analysis indicates that the longer the filament length
306
and the lower the SVL, the higher the courtship frequency (Fig. 2).
307
308
Discussion
309
In the palmate newt, both morphological (filament length, crest size, hind-foot-web size) and
310
behavioral (courtship activity) traits influence female mate choice (Cornuau et al. 2012, see
311
also Haerty et al. 2007). In this study, we aimed at understanding the information content of
312
these traits by investigating their condition-dependence to 1) natural variation in body
313
condition and 2) response to an experimental injection of LPS. Here, our results obtained on
314
morphological sexual traits provide support for the redundant signal hypothesis (Møller &
315
Pomiankowski 1993, Candolin 2003). Indeed, the development of filament length, crest area
316
and hind-foot-web area co-vary positively and all these traits co-vary with male condition as
317
measured by the body condition index BCI (even though these traits were not affected by the
13
318
experimental injection of LPS). Conversely, courtship frequency was not influenced by male
319
morphological sexual traits or male condition and was not affected by the LPS-injection. Our
320
study supports the idea that courtship frequency may not be a reliable signal of male condition
321
(unreliable signal hypothesis, Møller & Pomiankowski 1993).
322
The development of filament length, crest area and hind-foot-web area was positively
323
correlated under the conditions of our experiment, and this relation was stronger than a simple
324
allometric relationship with body size. This is a first evidence to validate the redundant
325
message hypothesis (Hebet and Papaj 2005). It further shows that there is no energy or
326
physiological constraint for the production and maintenance of the filament length, the hind-
327
foot-web size and the crest size, contrasting to the multitasking hypothesis stating that the
328
signaler’s ability to produce one sexual trait is constrained by the ability to produce other
329
sexual traits (Hebet and Papaj 2005). However, in our experiment, newts were fed ad libitum
330
that could reduce the likelihood to find trade-offs among traits. Moreover, we cannot exclude
331
the existence of individual strategies in the development of these sexual traits. For example,
332
some males could invest more in filament length whereas others invest more in crest size
333
maybe linked to internal factors or environmental conditions. Additional experiments are
334
therefore needed to determine the relationship between morphological sexual traits at the
335
individual level more precisely.
336
A second assumption of the redundant message hypothesis is that all traits should co-
337
vary with one aspect of the sender’s condition (Hebet and Papaj 2005). In agreement with this
338
assumption, filament length, crest size and hind-foot-web size were all good predictors of
339
male condition, measured as body condition index. Our experimental study therefore provides
340
one additional example to the few examples of redundant signals found so far (birds:
341
Birkhead et al. 1998, Jawor et al. 2004, Roulin et al. 2011, frogs: Vásquez and Pfennig 2007,
342
lizard: Martἰn and Lόpez 2010, and spiders: Gibson and Uetz 2008). Our correlative data
14
343
showed that the better the body condition (result of food intake) the better developed the
344
sexual traits were. This is in line with previous correlative studies showing that crest height
345
was linked to body condition in the crested newt Triturus cristatus, and the smooth newt
346
Triturus vulgaris (Green 1991, Baker 1992), suggesting that condition-dependence of
347
morphological sexual traits is ubiquitous in newts. These traits grow at the start of the
348
breeding season in newts, when males go into the water (Griffiths and Mylotte 1988). They
349
could therefore provide information about the food intake during this critical period, and
350
females probably obtain a more reliable picture of the overall male quality when they assess
351
several ornaments related to male condition, which increases the likelihood to select a good
352
quality male (Møller and Pomiankowski 1993).
353
A third rarely tested assumption of the redundant message hypothesis is that “the
354
probability of selecting a truly high condition mate will be improved when females choose by
355
examining two or more male traits, if the errors in different traits are uncorrelated” (Møller
356
and Pomiankowski 1993, see also Partan and Marler 1999, 2005). For example in the barking
357
tree frog Hyla gratiosa, female preference for larger males was stronger when females had
358
access to all call characteristics than when only one was available (Poole and Murphy 2007).
359
In this study we did not challenge this third assumption that need to examine how female
360
react to each trait separately (here filament, hind-foot-web and crest) that is impossible for the
361
moment without important damage for newts. Yet interestingly, we have recently explored
362
female mate choice in palmate newts by manipulating filament length. When the relative
363
filament length between two males was experimentally reversed (higher became smaller), the
364
choice of females was not totally reversed. This result suggests that, in addition to filament,
365
hind-foot web and crest development may be necessary to females to choose a mate (Cornuau
366
et al. 2012). However, further experiments with independent manipulation of the three sexual
367
traits are needed to confirm this hypothesis.
15
368
Male condition is a broad and complex concept that may relate to capacities of energy
369
storage and fat reserves, parasitic load or health status. In our experiment, we used body
370
condition as one indicator of male condition, and we also injected newts with an elevated dose
371
of an antigen (LPS) to experimentally mount an immune response that mimic an alteration of
372
health status. LPS has been shown to efficiently activate the immune system in a large range
373
of taxa including insects, birds, mammals, reptiles and anuran amphibians (Table S1). To our
374
knowledge, no LPS challenge has been reported so far in urodele species, such as newts.
375
More specifically, LPS has an impact on the metabolism and activity of frogs (Table S1) and
376
the newt immune system is not dramatically different from frogs (Todd 2007; Raffel et al.
377
2009). We could therefore expect that the LPS injection may yield the same immune
378
activation in newts as in frogs, despite being unable to verify it at the physiological level. In
379
our study, we did not find any effect of LPS on morphological and behavioral sexual traits. In
380
the absence of physiological, morphological and behavioral evidence that the injected
381
individuals actually mounted an immune response, we cannot exclude a non-activation of the
382
immune system by LPS in the palmate newt. Such non-activation is surprising given the
383
similarities between anuran and urodele immune systems, but not impossible. Given that an
384
activation of the immune system of anurans by LPS could sometime take up to 30 days
385
(Llewellyn et al. 2011, Table S1), the immune reaction of newts in our study may have been
386
slow and still below the threshold of detectability after 3 days. Another possibility is that LPS
387
did activate the new immune system but this activation did not have a negative impact on the
388
expression of morphological and behavioral sexual traits. Similar results were found in the
389
zebra finch Taeniopygia guttata in which sexual traits appear condition-dependent but not
390
linked to immune capacity (Birkhead et al. 1998). There could be an absence of a relationship
391
between sexual traits and health status in male palmate newts, whatever the environmental
392
conditions experienced, or environmental conditions may hide trade-offs between condition
16
393
and sexual traits due to ceiling or floor effects. Indeed, good environmental conditions may
394
hide trade-offs between condition and sexual traits that are sometimes revealed in harsh
395
environmental conditions (e.g. Jacot et al. 2005, Leman et al. 2009). Stress of captivity or
396
high initial parasitic load in the newt population, on the other side, may prevent mobilization
397
of energy to mount an immune response. In the absence of evidence of LPS-driven immune
398
activation, only one aspect of male condition was measured with certainty in this study, and
399
thus we cannot draw conclusions on the multiple message hypothesis.
400
In palmate newts, males with higher courtship activity have higher reproductive
401
success (Cornuau et al. 2012); however, courtship activity was not influenced by either body
402
condition or the experimental treatment that supports a low cost of this behavioral sexual trait.
403
Courtship display could obviously contain information on aspects of male quality that were
404
not assessed in this study, such as sperm quality (Chargé et al. 2010, Weir & Grant 2010),
405
locomotor ability (Byers et al. 2010) or heterozygosity (Drayton et al. 2010). However, the
406
cost of courting has been evaluated in a related species, the Plethodontid salamander
407
Desmognathus ochrophaeus, and the results were consistent with our findings: courtship
408
activity was not subject to any energetic limitations (Bennett and Houck 1983). This low cost
409
of courting supports the unreliable signals hypothesis.
410
In conclusion, while we were not able to specifically test for the multiple message
411
hypothesis, our results provide support for the redundant messages hypothesis for
412
morphological sexual traits (filament length, hind-food-web size and crest development), and
413
the unreliable signal hypothesis for the behavioral sexual trait (courtship frequency). Our
414
results are in line with previous work suggesting that the unreliable, multiple message and
415
redundant messages hypotheses are not necessarily mutually exclusive (Doucet and
416
Montgomerie 2003). Future experiments should manipulate the three morphological sexual
417
traits to further investigate their relative effect on female mating decisions.
17
418
419
Acknowledgments
420
Adelaïde Sibeaux is thanked for technical assistance. We also thank four anonymous
421
reviewers for insightful comments that greatly improved the manuscript. Catching permits
422
n°2009-13 (Ariège) and n°2009-12 (Haute Garonne). This work was supported by the
423
Ministère de la Recherche (PhD fellowship to JHC), two CNRS grants to AL and DS, the
424
BioDiversa-project RACE and the Observatoire Homme-Milieu Pyrénées Haut-Vicdessos.
425
426
Ethical standards
427
The experiments comply with the current laws of the country in which they were performed.
428
429
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Table 1 Relationships between the development of morphological sexual traits for the
laboratory experiment. (Δ trait = traitend – traitstart, df = degree of freedom, Sum Sq = sum
of the squares, SVL = Snout-Vent-Length, Experimental treatment = injection of LPS or
PBS).
Response
Δ Filament
Δ Crest
Δ Hind-foot-web
Predictor
Δ Hind-foot-web
Δ SVL
Experimental treatment
Δ Hind-foot-web : Δ SVL
Δ Hind-foot-web : Experimental treatment
Residuals
Sum Sq
31.64
15.06
0.98
5.77
2.02
133.53
Df
1
1
2
1
2
115
F
27.51
12.9
0.38
4.98
0.87
P
<0.001
<0.001
0.69
0.03
0.42
Δ Crest
Δ SVL
Experimental treatment
Δ Crest : Δ SVL
Δ Crest : Experimental treatment
Residuals
70.84
2.78
0.94
2.75
1.14
110.55
1
1
2
1
2
115
73.7
2.89
0.5
2.86
0.59
<0.001
0.09
0.61
0.09
0.56
Δ Filament
Δ SVL
Experimental treatment
Δ Filament : Δ SVL
Δ Filament : Experimental treatment
Residuals
17634.23
1680.99
74.89
315.27
1618.44
25724.19
1
1
2
1
2
115
79.56
7.94
0.15
1.85
3.61
<0.001
0.0057
0.86
0.18
0.03
Δ Hind-foot-web
Δ SVL
Experimental treatment
Δ Hind-foot-web : Δ SVL
Δ Hind-foot-web : Experimental treatment
Residuals
7101.06
5041.50
8.14
444.64
1304.68
33147.96
1
1
2
1
2
115
24.51
18.29
0.05
1.85
2.4
<0.001
<0.001
0.95
0.18
0.096
Δ Filament
Δ SVL
Experimental treatment
Δ Filament : Δ SVL
Δ Filament : Experimental treatment
Residuals
181.02
1.70
1.73
1.81
29.42
865.78
1
1
2
1
2
115
21.71
0.31
0.09
0.31
1.78
<0.001
0.58
0.91
0.58
0.17
Δ Filament
Δ SVL
Experimental treatment
Δ Filament : Δ SVL
Δ Filament : Experimental treatment
Residuals
163.23
1.05
0.72
0.01
28.22
888.2326
1
1
2
1
2
115
19.76
0.15
0.07
0.13
1.37
<0.001
0.70
0.93
0.72
0.26
Table 2 Relationships between the development of morphological sexual traits and the
variation in Body Condition Index (BCI). (Δ trait = traitend – traitstart, df = degree of freedom,
Sum Sq = sum of the squares, Experimental treatment = injection of LPS or PBS).
Response
Δ Filament
Predictor
Δ BCI
Experimental treatment
Δ BCI : Experimental treatment
Residuals
Sum Sq
9.44
4.71
2.26
172.59
Df
1
2
2
117
F
6.46
2.13
0.81
P
0.012
0.12
0.45
Δ Crest
Δ BCI
Experimental treatment
Δ BCI : Experimental treatment
Residuals
10438.80
592.90
699.04
35317.25
1
2
2
117
17.40
34.73
0.93
1.17
<0.001
0.40
0.31
Δ Hind-foot-web
Δ BCI
Experimental treatment
Δ BCI : Experimental treatment
Residuals
185.09
3.66
2.98
889.73
1
2
2
117
14.86
21.48
0.49
0.09
<0.001
0.61
0.91
Figures
Fig. 1 Positive relationships between the development of morphological sexual trait (Δ trait =
traitend – traitstart) and Δ Body Condition Index (Δ BCI). Positive relations with BCI were
found for Δ filament, Δ crest and Δ hind-foot-web after controlling for experimental treatment
and tank identity (Δ filament: F1,117 = 6.46, P = 0.012; Δ crest: F1,117 = 17.4, P < 0.001; Δ
hind-foot-web: F1,117 = 14.86, P < 0.001).
Fig. 2 Relationships between courtship activity and two morphological traits. SVL measured
at the end of the experiment was negatively correlated to courtship activity (F1,52 = 6.62, P =
0.013) and marginally positively correlated to filament length after controlling for SVL (F1,52
= 3.39, P = 0.071).
1
0
-1
-3
-2
Δ Filament length
2
3
Figure 1
-0.05
0.00
0.05
0.10
-20
-60
-40
Δ Crest
0
20
Δ Body Condition Index
-0.05
0.00
0.05
0.10
5
0
-5
Δ hind-foot-web
10
Δ Body Condition Index
-0.05
0.00
0.05
Δ Body Condition Index
0.10
25
20
15
0
5
10
15
10
5
0
Behavioral activity
20
25
Figure 2
33
34
35
36
SVL (mm)
37
38
39
3
4
5
6
7
Filament length (mm)
8
Fish
Amphibian
Amphibian
Perca
flavescens
Bufo marinus
Bufo marinus
15
15
1
0.126
12.6
0.01
1
Fish
5
Insect
Salmo salar
100
1.2
Insect
20
20
3
10
20
1
65
-
Insect
1
20.8
5
Insect
Allonemobius
socius
0.5
Insect
Insect
Tenebrio
molitor
Cyphoderris
strepitans
Euoniticellus
intermedius
Gyrllus
campestris
Gryllodes
sigillatus
Clade
Species
-
-
0.3
0.1
0.005
0.01
0.001
0.01
0.001
0.005
132-237
100-300
50-200
7.92
0.25
1.2
0.05
0.77
-
0.12
Concentration
Quantity
Dose
per mg/kg
injected Weight (g)
(mg/ml) animal
(ml)
weight
Table S1 Use of LPS in the literature in a range of different species groups.
Supplementary material
C
C
B
B
A
A
A
A
A
A
hormonal
behavioral fever
metabolic rate
E
0127:B8
E
0127:B8
mx response
sexual signal,
paternal
resources
sexual signal,
mating success
reproductive
investment
sexual signal,
longevity
spermatophore
production
prophylaxis
Effect
E 055:B5
E
0128:88
-
S L6136
S L6136
S L6136
S L6136
E L8274
Injection
Serotype
method
Sherman and
Stephens 1998
Salinas et al.
2004
Haukenes et al.
2011
Sherman et al.
1991
Kerr et al. 2010
Jacot et al. 2004
Leman et al.
2009
Reaney and
Knell 2010
Fedorka and
Mousseau 2007
Moret and SivaJothy 2003
Reference
Streptopelia
decaocto
Zonotrichia
leucophrys
Pavo cristatus
Passer
domesticus
Taeniopygia
guttata
Taeniopygia
guttata
Gallus Gallus
Bufo
paracnemis
Bufo
paracnemis
Xenopus
laevis
Lissotriton
helveticus
Ctenophorus
fordi
Iguana
iguana
Anolis
carolinensis
Podarcis
hispanica
Bufo marinus
-
211.6
2116
0.08
-
Reptile
Reptile
Reptile
Reptile
0.1
Bird
1
0.26
Brid
Bird
1
0.1
Bird
Bird
0.1
Bird
-
2.5
25
0.14
0.7
Amphibian
Bird
2.5
-
Amphibian
1
-
1
0.88
0.58
0.3
0.5 to 5
2.5
5
0.2
2
0.02
0.2
2
10
-
Amphibian
0.2
2
-
1
Amphibian
Amphibian
0.1
0.2
4
0.15
0.1
0.1
0.1
0.05
0.25
1
-
0.02
-
-
-
-
26
-
4000
17
17
30
-
-
3.8-4.6
85
3–5
1.4
200-300
150-250
150-250
45-400
-
B
D
B
B
B
B
B
B
-
B
B
B
C
C
C
E 055:B5
E 055:B5
E 055:B5
E 055:B5
E 055:B5
E 0111B4
E
0111:B4
E 055 :
B5
E 055:B5
E 0111B4
E L3129
E 055:B5
-
E
0111:B4
E
0111:B4
0111:B4
immune
responses
Sell et al. 2003
Deen and
Hutchison 2001
Merchant et al.
2008
López et al.
2009
Uller et al. 2006
Bonneaud et al.
2003
Alonso-Alvarez
sexual signal
et al. 2004
body weight,
Bertrand et al.
oxidative damage 2006
Loyau et al.
sexual signal
2005
Eraud et al.
survival
2009
hormone,
Owen-Ashley et
activity, song,
al. 2006
activity and
fitness
brain activity
sexual signal
hypothermia
reproductive
investment
fever or
hypothermia
sexual signal
This study
Zou et al. 2000
behavioral fever
behavioral fever
Llewellyn et al.
2011
Bicego and
Branco 2002
Bicego et al.
2002
feeding rate,
activity
Mammal
Mammal
Mus musculus
Mus musculus
0,1
-
0,5
0.18
0.4
0.5
0.67
0.8
4.65
4
0.05
0.2
0.02
1
0.2
0.05
0.1
25-30
-
20
1500
28.6
16-27
25
Leg
B
wing
B
F
D
E
Velando et al.
2006
Losdat et al.
2011
Aubert et al.
1997
Raghavendra et
al. 2000
Durazzo et al.
2008
reproductive
success
nest building,
fever
hyperalgesia
E
0111:B4
sperm
Munoz et al.
2010
Owen-Ashley
and Wingfield
2006
Toomey et al.
2010
song, territorial
defense
retinal carotenoid
E 08:B28
E 055:B5
E 055:B5
E 055:B5
S L7261
E 055:B5
song, body
weight, hormone
fever
Phodopus
Mammal
0.5
0.1
NA
S L-6511 food intake
sungorus
Rattus
E 0127:
exploratory
Mammal
0.05
0.1
B
Rico et al. 2010
norvegicus
B8
behavior
A = In pleural membrane between two abdominal segments, B = Intraperitoneal, C = Dorsal lymphatic sac, D = Intramuscular, E = Intravenous,
F = Subcutaneous.
Bird
Parus major
0.0286
Bird
0.1
2
Bird
Bird
1
Bird
Sula nebouxii
gambelii
Melospiza
melodia
morphna
Carpodacus
mexicanus
Zonotrichia
leucophrys
oriantha
r
0.40
0.61
0.39
95% CI
0.25, 0.54
0.49, 0.71
0.23, 0.53
P
<0.001
<0.001
<0.001
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ARTICLE 5
Impacts of varying environmental conditions on
sexual traits and consequences for mate choice in the
palmate newt.
Cornuau JH, Sibeaux A, Tourat A, Schmeller DS, Loyau A.
En préparation
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Impacts of varying environmental conditions on sexual traits and
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consequences for mate choice in the palmate newt
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Jérémie H. Cornuaua, Adélaïde Sibeauxa, Audrey Tourata, Dirk S. Schmellera,b and Adeline
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Loyaua,b
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a
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09200 Saint Girons, France
Station d’Ecologie Expérimentale du CNRS à Moulis, 2-4 Route du CNRS, Moulis Village,
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10
b
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Permoser Strasse 15, 04138 Leipzig, Germany, both senior authors
Helmholtz Center of Environmental Research – UFZ, Department of Conservation Biology,
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Address correspondence to J. Cornuau. Email: [email protected].
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Keywords: multiple signals; sexual traits; condition dependence; trade-off; GEI
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Primary Research Article
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Changing environments may substantially alter population dynamics when they impact on
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sexual traits, their expression and information content. During mate choice, females
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commonly assess multiple, sexual traits. Theory predicts that females’ preferences for
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multiple sexual traits have evolved because the reliability of these sexual traits varies
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differently according to the environment. Morphological sexual traits, more static and less
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labile may provide information about past condition but may not be reliable when the
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environment changes. In contrast, behavioral sexual traits are more dynamic and more labile
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and may provide information about current condition. Here we tested these predictions using
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a full factorial design experiment of food limitation over long and short time periods in the
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palmate newt (Lissotriton helveticus). We created stable and unstable environments. We
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found that morphological sexual traits were little labile. Therefore, they may indicate the
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bearer's genetic condition or long-term viability, rather than current condition. In contrast,
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some behavioral traits (quivers and breathing) appeared dynamic, potentially signaling the
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current male condition. However, courtship display remained fixed over the time scale of the
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experiment and was the main determinant of female mate choice. Finally, we found some
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plasticity in female preference for morphological traits depending on environmental stability.
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Our study shows that environmental change can have profound impacts on the expression of
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morphological and behavioral sexual traits and on female preferences. It further underscores
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the importance to pay attention to behavioral cues to understand the impact of global change
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on population viability.
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INTRODUCTION
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It is often predicted that past and current anthropogenic influences on environment will
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render environmental conditions more variable and unpredictable (Meyers & Bull, 2002;
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Kussell & Leibler, 2005; Reed et al., 2010). Directional environmental changes, such as
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higher temperatures due to global warming may be predictable and individuals and
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populations may adapt to such changes (e.g. Winder & Schindler, 2004; Vatka et al., 2011).
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However, when environmental changes are irregular and unpredictable, it is much more
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difficult to predict how individuals will deal with such variations and whether their
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morphological and behavioral responses will be adaptive (Kussell & Leibler, 2005;
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Ghalambor et al., 2007; Reed et al., 2010; Hof et al., 2011). It is further suggested that
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environmental changes can affect evolutionary mechanisms such as natural or sexual selection
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(Candolin & Heuschele, 2008; Candolin & Wong 2012). Therefore, some models predict that,
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under certain conditions, environmental changes affect the expression of both male sexual
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traits and female mating preference, which may lead to a fundamental breakdown in the
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mechanism of sexual selection and therefore modify population faith (Greenfield &
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Rodriguez, 2004; Higginson & Reader, 2009; Kokko & Heubel, 2008; Ingleby et al., 2010).
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It has been recently proposed that natural variations in environmental pressures can be
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finely reflected in male sexual traits and that female can adaptively modify their mate
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preference so that the best mates are chosen in every environment (Chaine & Lyon, 2008;
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Bro-Jørgensen, 2010, Cornwallis & Uller 2010). According to Bro-Jørgensen (2010), females
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can do so using multiple sexual traits (i.e., the “fluctuating environments hypothesis”). This
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hypothesis not only could resolve an issue puzzling biologists since decades (Møller &
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Pomiankowski, 1993; Candolin, 2003; Bro-Jørgensen, 2010), but also shed light on how
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adaptive female mating preferences can be maintained in changing environments (Chaine &
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Lyon, 2008). The fluctuating environments hypothesis assumes that environmental variation
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in time and/or space could have strong effects on signaler condition (i.e. male condition),
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signal transmission or signal reliability (Mills et al., 2007; Higginson & Reader, 2009;
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Rundus et al., 2010; Tolle & Wagner, 2011). For example, male body condition is a dynamic
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individual characteristic that can rapidly vary according to either time and/or environment
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(Lailvaux & Kasumovic, 2011). Bro-Jørgensen (2010) assumes that labile (or flexible) sexual
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traits are evolutionary shaped to reliably signal male condition for the choosy female even
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when facing environmental variability. In contrast, the less labile sexual traits could be
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particularly misleading when individual condition changed due to environmental change, but
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may be more informative in a stable environment than labile traits (Bro-Jørgensen, 2010).
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Using both labile and fixed traits may therefore provide to females reliable information about
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male quality in any environment encountered and/or at any time scale, thus enabling adaptive
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female mate choice in heterogeneous and fluctuating environmental conditions (Bro-
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Jørgensen, 2010).
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Behavioral and morphological sexual traits are probably the best examples of a
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difference in trait lability. This difference is linked to the physiological delay that exists
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between the production or maintenance of the trait and the moment of the female’s evaluation
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(Butler & McGraw 2011). For example in Himalayan warbler Phylloscopus humei feather
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development seems reflected the period of feather growth and not current male quality
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(Scordato et al., 2012, see also Naguib & Nemitz, 2007). Contrary to morphological sexual
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traits, behavioral ones may respond rapidly to changes in male condition and thus are
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generally expected to provide more accurate information about male condition at the time of
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assessment (Loyau et al., 2005; Leman et al., 2009; Chargé et al., 2010). In the Houbara
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bustard Chlamydotis undulata undalata, a change in male health status has a rapid effect on
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sperm quality and may therefore be rapidly assessed by females via a change in the expression
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of behavioral sexual traits (Chargé et al., 2010; Loyau & Lacroix, 2010).
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Amphibians are strongly impacted by global change and are considered the most
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threatened vertebrate taxa worldwide (Stuart et al., 2004; Alford, 2011). As global change is
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expected to affect freshwater ecosystems at several trophic levels (Woodward et al., 2010),
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we chose to manipulate environmental quality through food availability in male diet. Here, we
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tested the predictions of the fluctuating environment hypothesis on the palmate newt
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(Lissotriton helveticus), an amphibian species with strong sexual dimorphism involving both
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morphological and behavioral sexual traits that are driven by female preference (Haerty et al.,
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2007; Cornuau et al., 2012). We hypothesized that (1) morphological sexual traits are more
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static (less labile), provide information about past environmental conditions and unreliable
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signal male condition in unstable/varying environments (2) behavioral sexual traits are more
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dynamic (more labile) and provide reliable information about current condition even in
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unstable/varying environments, (3) females use both static and labile sexual traits to obtain
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reliable information about male condition and to adaptively choose their mate, thus female
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mate choice strategy is not the same under stable and variable environmental conditions
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because unpredictable environmental variation alters trait reliability. Generally, our results
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contribute to the understanding of how global change can affect reproduction and population
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dynamics of an amphibian species by impacting on morphological and behavioral sexual
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traits.
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MATERIAL AND METHODS
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126 male palmate newts and 40 females were collected by dip netting from one pond
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near Caumont (N43.02630 E1.07247, Ariège, France) at a very early point of the breeding
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season (February 07th and March 01st 2011). Individuals were in their early aquatic stage with
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male sexual traits only at the very start of their development. Newts were brought and
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maintained in captivity at the Station d’Ecologie Expérimentale du CNRS à Moulis, France.
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Unisex groups of 10 individuals were placed in opaque tanks (52×33.5×29.5 cm) with 10
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liters of water, plants collected in their native environment, and a clay brick perforated with
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holes to ensure shelter. Newts were individually marked by subcutaneous injection of Visible
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Implant Elastomers (VIE, Northwest Marine Technology, Washington, Shaw Island, WA,
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USA) by injecting one of 4 colors at the base of the four legs. They were kept at 18°C (±1)
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under fluorescent tubes (ReptiSun 2.0, ZooMed) to simulate natural light with a 12 hours
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light/ 12 hours dark cycle.
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Diet treatment
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To test the condition dependence of sexual traits and their reliability under stable versus
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unstable environmental conditions, we used a diet treatment for males (Cotton et al., 2004).
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We chose to perform “food” and “no food” treatments after a preliminary experiment that
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showed no mortality in male newts due to a lack of food during a 4-week-period (Green,
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1991, data not shown). After one week of acclimatization the 126 males were randomly
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assigned to one of four dietary treatments (Fig. 1). Each treatment consisted of a long
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treatment (four weeks) of either high- (H) or low-diet (L), followed by a short treatment (one
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week) of H- or L-diet. Our experimental setup resulted in a full factorial design of long and
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short treatments for male diet: HH, HL, LH, and LL. Therefore, HH and LL males
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experienced a stable, yet different environment, whereas HL and LH males experienced a
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varying environment. Males under H-diet were fed with 100 mg of chironom larvae per
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individual every two days complemented with tubifex and daphnia every week, which
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corresponds to an ad libitum diet. Males under L-diet were not fed. During the long and short
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male diet treatments, females were fed ad libitum with living chironom larvae, tubifex worms
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and daphnia, therefore experiencing a stable environment.
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In order to understand the impact of laboratory treatment on male sexual traits on
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longer time scales we conducted an additional experiment where male newts were place in
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semi-natural tank (Fig. 1). After these 5 weeks of long and short treatments and of low or high
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diet simulating stable and variable environmental conditions, we divided males into two
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groups of 63 males each and placed each group of males with 20 females in an outdoor semi-
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natural tank (1000 L) filled up with water and covered with a net to prevent predation. Newts
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fed ad libitum on prey that was naturally growing in these tanks. Prey availability was likely
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intermediate between the H and L diets. After 5 weeks in outdoor tanks, males were caught
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and the morphological traits were measured (see below). Seventeen males were not re-caught
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due to an unknown cause (predation by dragonfly larvae or snake, natural death). Missing
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males were homogenously distributed among treatments (4/32 for HH, 4/31 for HL, 6/32 for
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LH and 3/31 for LL), and these males did not differ from re-caught males in any
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morphological trait measured before the release in outdoor tanks (all P > 0.20). We released
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all individuals in the population of origin at the end of the experiment.
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Morphological data
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Morphological sexual traits of males were measured four times (n=126 for the
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laboratory experiment and 109 at the end of the outdoor experiment), (i) at the start of the diet
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treatment (t0), (ii) after the long diet treatment (t4 = 4 weeks later), (iii) immediately after
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behavioral measurements at the end of the laboratory treatment (t5 = 5 weeks after t0), and (iv)
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after 5 weeks in outdoor tanks (t10 = 10 weeks after t0). We recorded body mass (accuracy:
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0.01 g) and SVL (Snout-Vent-Length, from the snout tip to the posterior end of the cloaca)
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with a caliper (accuracy: 0.01mm). We further calculated a body condition index (BCI) as the
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residual of the linear regression of the cube root of body mass on SVL (Baker, 1992). The
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BCI reflects the lipid content in newts and has high accuracy in amphibians (Denoël et al.,
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2002; Báncilá et al., 2010). The three morphological traits of the palmate newts measured
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included crest, hind foot web and the tail filament (Cornuau et al. 2012, Fig. S1). The crest is
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usually small in palmate newts and we chose to use tail area as an index of crest development
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(Green, 1991). All measures were realized by taking a photo on a millimeter paper
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background with a digital camera, with subsequent processing in IMAGEJ v.1.28
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(http://rsb.info.nih.gov/ij/). We averaged the size of left and right hind foot web. The crest,
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hind foot web and filament length were highly positively correlated at t4, t5 and t10 and these
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correlations were true for each of the four diet groups (all P < 0.001). Therefore, we
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synthesized these traits in a single variable by performing a Principal Component Analysis
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(PCA). The first principal component (hereafter called PC1) explained 66.65% of the variance
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and was positively correlated to crest area (r = 0.85), hind foot web area (r = 0.85) and
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filament length (r = 0.74). All the morphological variables measured in our study were
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randomly distributed amongst the different treatment groups (MANOVA, Wilkinson test, start
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of the long treatment: F6,119 = 1.68, P = 0.13, start of the short treatment: F6,119 = 0.67, P =
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0.67).
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Behavioral and mate choice data
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We used 40 females and 120 males for behavioral tests. Each female was used three
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times to reduce the number of females necessary for the experiment, always separated by a
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delay of two days (we took a female effect into account in our model, see below). After diet
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treatment (long treatment plus short treatment, Fig. 1), one female and one male were
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randomly chosen and placed in an experimental tank (26×33.5×29.5 cm). The female was
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placed in an opaque PVC-cylinder previously disposed in the center of the experimental tank.
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The male was placed close to, but outside of, the PVC-cylinder. Experimental tanks contained
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2 cm of large grained sand and 8 cm of de-chlorinated water. After 5 min of acclimatization,
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the opaque cylinder was removed and individuals could interact freely during 40 min to allow
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for observations of sexual behaviors (see also Cornuau et al. 2012). We recorded the male
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behavior using a video camera placed above the experimental tank. The videos were analyzed
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with the software The Observer 7.0 (Noldus Information Technology). Newts generally
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performed several distinct sexual behaviors (for details see Table S1; see also Halliday, 1974;
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Wells, 2007), of which we focused on display, quiver and breathing. Display activity
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corresponds to the time spent (in seconds) in courtship (fan, whip and wave), quiver
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corresponds to the male offering to deposit a spermatophore to the female by slowly quivering
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his tail, while a breathing event corresponds to surfacing of newts to breathe (Table S1). We
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also recorded the number of sperm mass transfers to females. For each of the 120 males, we
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evaluated the access to reproduction as 0 if the male did not transfer any spermatophore to the
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female or 1 if he transferred at least one spermatophore. Finally, we calculated the number of
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male offers declined by females (i.e. male failures), by subtracting the number of quivers by
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the number of spermatophores taken by the female.
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Statistical Analyses
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Data were analyzed using R version 2.13.1 (http://cran.r-project.org/). The effect of
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diet treatments (long treatment, short treatment and their interaction) and environmental
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stability (HH and LL against HL and LH) on the BCI trajectory and morphological sexual
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traits (PC1) was assessed by repeated measure analysis of variance (ANOVA). The test was
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done on data collected at the end of the laboratory treatment (t5) and at the end of the outdoor
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experiment (t10). Males were maintained in groups so we nested the tank identity within the
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diet treatment. Sexual traits showed some degree of allometric scaling with SVL, which was
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corrected of by including SVL as a covariate in the models (Cotton et al., 2004).
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We tested the effect of the diet treatment (long, short and the interaction between long
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and short diet) on display, quiver, breath, access to reproduction and number of failures using
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general linear mixed models (GLMMs). We conducted additional models to test the effect of
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environment stability (HH and LL against HL and LH) on behavioral measure. In order to
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assess the effect of morphological and behavioral sexual trait on female mate choice, we
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conducted a model with PC1, display and quiver as independent variable and access to
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reproduction as dependant variable. In order to assess if the used of morphological sexual trait
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and behavioral sexual trait depend of the environment stability, we tested the interaction
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between factor of interest and environment stability on the access to reproduction. In our
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experiment females were used three times. To control for any effect of the female identity we
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included female as a random effects. We detected any effect of female order (1st, 2nd, or 3rd
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male) or female reproductive status (reproduction with no, 1 or 2 males) on display, quiver,
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breath, access to reproduction or number of failure (all P > 0.05). However to avoid any
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potential effect of this variable on our result we included female order and female
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reproductive status as random effects in all the models.
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On the whole, we assessed the effect of independent variable on dependant variable
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by testing whether the removal of an independent variables or their interaction caused a
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significant decrease in the model fit (Crawley 2007, Zuur et al. 2009). The statistical
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significance was assessed by comparing a full model with reduce models not containing factor
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of interest. The p-values corresponded to the decrease in deviance when the respective
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variable or their interaction was removed. The statistical significance of the factor of interest
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was based on log likelihood tests. Log likelihood tests follow a χ2 distribution and the degrees
253
of freedom always differ by one. We used maximum-likelihood to fit the models.
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RESULTS
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Impacts of diet treatments on body condition index
258
The long and short treatments affected BCI variation over the time course of the
259
experiment (Table 1). The BCI of the males assigned to the HH-diet remained constant during
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the laboratory experiment t0-t5 (long plus short treatments) but decreased after the outdoor
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experiment t5-t10 (Fig. 2a). The BCI of the males assigned to the HL-diet remained constant
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during long treatment but decreased during the short treatment (Fig. 2a). In contrast, males
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assigned to the LH-diet showed a strong decrease of their BCI already during the long
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treatment but an increase during the short treatment (Fig. 2a). Finally the BCI of the males
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assigned to the LL-diet decreased both during the long and the short treatments and increased
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during the outdoor experiment (Fig. 2a). We measured a significant effect of both long and
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short treatments on BCI at t5 (long treatment: F1,122 = 67.393, P < 0.001, short treatment: F1,122
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= 56.687, P < 0.001, long×short treatments: F1,122 = 13.895, P = 0.001). In contrast both long
269
and short treatments did not influence BCI measured at t10 (long treatment: F1,105 = 1.621, P =
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0.206, short treatment: F1,105 = 0.720, P = 0.398, long×short treatment: F1,105 = 1.184, P =
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0.279).
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Lability of morphological sexual traits
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The variation of the PC1 synthesizing the morphological traits was significantly
275
affected by the diet during the long treatment but not the short one (Table 1). Generally, PC1
276
was linked to the amount of food provided to the individuals. The PC1 of HH and HL males
277
strongly increased during the long treatment, remained constant during the short treatment and
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decreased during the outdoor experiment (Fig. 2b). PC1 of LH and LL males remained
279
constant during both long and short treatments but increased during the outdoor experiment
280
(Fig. 2b).
281
PC1 at t5 (end of the laboratory experiment), was significantly affected by the long
282
treatment but not the short treatment (long treatment: F1,121 = 101.382, P < 0.001, short
283
treatment: F1,121 = 0.963, P = 0.328, long×short treatments: F1,122 = 0.364, P = 0.547, SVL:
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F1,121 = 68.891, P < 0.001). Globally we found a positive correlation between PC1 and BCI
285
measured at t5 (BCI: F1,124 = 27.615, P < 0.001). The relationship between PC1 and BCI
286
varied with environmental stability (F1,122 = 4.062, P = 0.046), being significant only in stable
287
environments (stable: F1,61 = 36.880, P < 0.001, varying: F1,61 = 0.612, P = 0.437). PC1 at t5
288
was positively correlated to BCI at t0, but this relationship depended on the diet group during
289
the long treatment (BCI: F1,122 = 10.252, P = 0.002, BCI×long diet: F1,122 = 6.111, P = 0.015,
290
Fig. 3). The significance was driven by the males assigned to the L-diet during the long
291
treatment (L-diet: F1,122 = 10.598, P = 0.002, H-diet: F1,122 = 0.052, P = 0.820, Fig. 3).
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At t10 (end of the outdoor experiment) we did not find a significant effect of neither
293
long or short treatment on PC1 (F1,104 = 2.029, P = 0.157, F1,121 = 0.002, P = 0.962,
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respectively; long×short treatments: F1,122 = 0.079, P = 0.780, SVL: F1,121 = 28.965, P <
295
0.001). However, we found a positive correlation between PC1 and BCI (F1,107 = 11.289, P =
296
0.001, Fig. 4). This relationship was not affected by the experimental outdoor tanks
297
(BCI×tanks: F1,105 = 0.034, P = 0.854), environmental stability (BCI×environment: F1,105 =
298
0.652, P = 0.421), nor treatments (BCI×long treatment: F1,105 = 0.174, P = 0.678; BCI×short
12
299
treatment: F1,105 = 0.698, P = 0.405). We also did not find a relationship between PC1 at t10
300
and BCI measured at t0, t4 or t5 (all P > 0.110).
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Lability of behavioral sexual traits
303
Both short and long diet treatments had no impact on male display activity (Table 2,
304
Fig. 5a). Display activity was not related to male BCI (χ21 = 0.946, P = 0.331) and there was
305
no difference between males experiencing stable and varying environments (χ21 = 0.771, P =
306
0.380). However, we found a significant effect of female body condition on the time spend in
307
display (χ21 = 4.936, P = 0.026). There was evidence that the number of quivers was
308
significantly affected by the short diet treatment (Table 2, Fig. 5b). Males assigned to the L-
309
diet during the short treatment made more quivers compared to males assigned to the H-diet
310
(Fig. 5b). The number of quivers was largely explained by male BCI (χ21 = 4.279, P = 0.038)
311
but not by environmental stability (χ21 = 0.428, P = 0.513). Breathing appeared to be
312
negatively affected by the short treatment, with males on the L-diet breathing less frequently
313
than males on the H-diet (Table 2). The numbers of breathing events was positively
314
influenced by male BCI (χ21 = 6.234, P = 0.0125) but was not explained by environmental
315
stability (χ21 = 0.461, P = 0.497).
316
317
Impacts of diet treatments on male mating success
318
Neither the long or short diet treatment had an impact on male access to reproduction,
319
while the short treatment had an impact on the number of failures (Table 3). Males assigned to
320
the L-diet during the short treatment were less successful in the transition between quiver and
321
sperm mass transfer to females than H-diet males, experiencing more failures (Table 3). We
322
found that access to reproduction was not influenced by PC1 at t5 (χ21 = 1.258, P = 0.262). In
323
contrast display activity and the number of quivers had a strong impact on access to
13
324
reproduction (χ21 = 11.160, P = 0.001; χ21 = 14.236, P < 0.001, Fig. 6), and this result was not
325
influencing by environments stability (χ21 = 0.054, P = 0.816; χ21 = 1.526, P = 0.217). The
326
probability to access to reproduction was positively explained by the courtship activity and
327
the number of quivers (Fig. 6). Neither male BCI (χ21 = 0.021, P = 0.89) nor environmental
328
stability (χ21 = 0.723, P = 0.395) significantly affected the access to reproduction. However,
329
access to reproduction was affected by the interaction between environmental stability and
330
PC1 (χ21 = 6.72, P = 0.010, Fig. 7). Indeed morphological sexual traits did not contribute to
331
mating success in stable environments (χ21 = 1.234, P = 0.267, Fig. 7), while females
332
preferred males with less developed morphological sexual traits in varying environments (χ21
333
= 4.170, P = 0.030, Fig. 7).
334
335
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336
337
338
DISCUSSION
339
and behavioral sexual traits in the palmate newt under stable and varying environmental
340
conditions. We tested the predictions of the fluctuating environment hypothesis and found that
341
both morphological and behavioral sexual traits expressed by males varied in their lability.
342
Our study suggests that female mate choice may be driven by several sexual traits that varied
343
in their lability and their information-content: a fixed trait (display activity) unrelated to
344
environmental conditions, a very labile trait (quiver frequency) that signals male current
345
condition, and traits of a higher variation in the degree of lability (morphological sexual traits)
346
that would reliably signal male current condition in stable environments and past condition in
347
an unstable environment. Display activity may inform females about male intrinsic quality
348
(genetic or long-term quality) whatever the environment experienced by both sexes, quiver
349
frequency may signal male reproductive motivation and current male condition,
350
morphological traits may inform about male mid-term condition and are only reliable in rather
351
stable environments. Our results therefore support the fluctuating environment hypothesis
352
(Bro-Jørgensen 2010) as during mate choice females of the palmate newt have access to
353
multiple signals that varied in their lability. Our study showed that the signal reliability of
354
morphological sexual traits could be compromised when environmental fluctuations are rapid.
Here, we investigated the information content and variation of multiple morphological
355
356
As expected, we found that the morphological sexual traits (filament length, hind foot
357
web area and crest size) showed a low degree of lability, because they were affected by the
358
food restrictions only during the long treatment (4 weeks). Further, males in better condition
359
at the beginning of the experiment (t0, before the long treatment) were able to develop
360
morphological traits of higher quality (e.g. longer filaments), suggesting that fat reserves
361
maintained over the terrestrial winter season could be crucial during the breeding season.
15
362
These findings confirm that the production of morphological sexual traits, on a yearly basis, is
363
an expensive physiological process linked to male body condition. However, we found that
364
the relationship between the expression of male morphological sexual traits and body
365
condition varied with environmental stability. It means that changing environmental
366
conditions may weaken the reliability of morphological sexual traits (Robinson et al., 2007;
367
2012). Indeed, in a rapidly changing environment, morphological sexual traits may accurately
368
reflect past male condition but are poor predictors of current condition. In that case, females
369
who base their choice only on morphological sexual traits would not obtain reliable
370
information on male condition at the exact time of assessment and may perform maladapted
371
mate choice (Bro-Jørgensen, 2010).
372
373
We expected behavioral sexual traits to be more labile than morphological sexual
374
traits. However, not all behavioral sexual traits were impacted the same way by varying
375
environmental conditions. Firstly, contrary to our expectations, courtship display activity
376
(including fan, wave and whip) remained fixed over the time scale of the experiment, despite
377
varying environmental conditions. This suggests that display activity is not condition-
378
dependent, which is supported by a previous study in the Plethodontid salamander
379
Desmognathus ochrophaeus showing that metabolic costs of display were low (Bennett &
380
Houck, 1983). While display activity is fixed, its assessment during mate choice cannot
381
provide reliable information on current male condition. However, if display activity is
382
genetically determined (Drayton et al., 2010) and female preference for such a trait is
383
heritable, mating with high displaying males will pay-off in any environment the offspring
384
will experience (Fisher 1930). Therefore, the use of a fixed, unreliable trait might be a good
385
mate choice strategy in a varying environment.
386
16
387
Secondly, we found that some male behavioral traits (the number of quivers, the
388
number of breath events and the number of male failures in the transition between quiver and
389
spermatophore transfer) were more labile than display activity. These behaviors were labile
390
over a short term. Surprisingly, the males who experienced the low diet during the short
391
treatment made more quivers than the males who experienced the high diet, but were less
392
successful in the transition between quiver and sperm mass transfer (=access to reproduction)
393
to females. As a quiver represents a male’s offer to deposit a spermatophore to the female, a
394
food shortage may increase male motivation to reproduce, maybe as a terminal effort (Sadd et
395
al., 2006; Saaristo et al., 2010). However, in our experiment, females appear to be able to
396
detect such a motivation at least to some extent, as the higher motivation of L-diet males did
397
not result in a higher mating success compared to H-diet males.
398
399
Plasticity in female preferences during mate choice can involve the direction of the
400
preference for a given trait. In this case, females always evaluate the same trait(s) but prefer
401
males with the more developed traits in some environments and males with the less developed
402
traits in others (Chaine & Lyon, 2008; Bro-Jørgensen, 2010). Plasticity in female preference
403
can also affect the strength of the preference, so that females assess different traits in different
404
environments, or prioritize some traits over others depending on the circumstances (Cotton et
405
al., 2006; Chaine & Lyon, 2008). Here, we found some plasticity in female preference for
406
male morphological sexual traits, depending on the circumstances. Female mate choice was
407
not driven by male morphological sexual traits in stable environments, while there was a
408
negative association between female choice and morphological sexual traits in varying
409
environments. In addition, in a previous study in the palmate newt, we found that females
410
prefer males with more developed morphological sexual traits (Cornuau et al., 2012; see also
411
Haerty et al., 2007). Hence, when the environmental variations cannot be reliably tracked by
17
412
labile sexual traits, females may prefer using a fixed trait and may only use labile traits as
413
additional source of information. Our results further suggest that the degree of lability might
414
contain important information for female mate choice. In our experiment, medium labile traits
415
(morphological traits) and very labile traits (behavioral trait quivers) were used differently in
416
different environments and determined reproductive success of males.
417
418
In conclusion, we were able to show that the access to reproduction of males vary with
419
fluctuating environmental conditions. That was especially the case when environment
420
changed in quick alterations. Our study is one of few showing the impact of varying
421
environments on reproduction experimentally. The interactions environment x reproductive
422
strategy appear to be complex, but need to be better understood for a wide range of species to
423
allow predicting population size and dynamics for conservation-relevant species. Such
424
knowledge is key in situations where population-level estimates of reproductive outcome and
425
survival are not enough to correctly predict the population dynamics of the focal species.
426
Pinpointing those situations where information on individual behaviors is needed will help to
427
direct efforts towards gathering relevant information for the management of focal species. Our
428
study has shown that when stress was unpredictable, it was much more difficult to predict
429
how individuals will deal with such variations and whether their morphological and
430
behavioral responses will be adaptive (Kussell & Leibler, 2005; Ghalambor et al., 2007; Reed
431
et al., 2010; Hof et al., 2011). We have also shown that a varying environment changed the
432
link between different traits, thus changing the information reliability, which could lead to
433
maladaptive behavior and increased stress. Therefore, it is important to further analyze the
434
variability of the investment in the expression of costly sexual signals that convey honest
435
information about their quality and that will be of interest to individuals of the other sex
436
seeking prospective mates in stable and variable environments.
18
437
Ethical standards The experiments comply with the current laws of the country in which
438
they were performed.
439
440
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441
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563
564
24
565
TABLES
566
Table 1. Results of the repeated measures analysis of variance on variation of BCI and
567
morphological sexual traits PC1 (filament length, hind foot web and crest). Significant
568
interactions are highlighted in bold.
569
BCI
F
P
PC1
F
P
Between subjects
Long treatment
Short treatment
Long×Short treatments
SVL
48.732
2.644
3.339
<0.001 37.526 <0.001
0.107 0.015 0.903
0.071 0.705 0.44
71.236 <0.001
Within subjects
Time
Time×Long treatment
Time×Short treatment
Time×Short×Long treatments
SVL
103.632
50.596
24.775
4.446
<0.001
<0.001
<0.001
0.004
570
571
572
25
43.371
21.470
0.314
0.159
81.098
<0.001
<0.001
0.815
0.924
<0.001
573
Table 2. Summary results of the effect of diet treatment on on behavioral measurements
574
(Display: time spent in courtship, Quiver: number of quivers, Breath: number of breathing
575
events). Bold values represent significant parameters.
576
Dependant variable
Display
Independent variable
Long treatment
Short treatment
Long×Short treatments
χ2
0.178
0.348
0.816
Df
1
1
1
P
0.673
0.555
0.366
Quiver
Long treatment
Short treatment
Long×Short treatments
0.043
8.518
0.257
1
1
1
0.836
0.003
0.612
Breath
Long treatment
Short treatment
Long×Short treatments
2.926
10.194
0.673
1
1
1
0.087
0.001
0.412
577
578
579
26
580
Table 3. Summary results of the effect of diet treatment on reproductive success
581
(Morphological sexual traits = index of morphological sexual traits, Failures = number of
582
quivers minus number of successful spermatophore transfers). Bold values represent
583
significant parameters.
584
Dependant variable
Access to Reproduction
Independent variable
Long treatment
Short treatment
Long×Short treatments
χ2
0.008
0.211
0.725
Df
1
1
1
P
0.926
0.650
0.395
Failures
Long treatment
Short treatment
Long×Short treatments
0.016
7.681
0.787
1
1
1
0.898
0.005
0.375
27
585
FIG. LEGENDS
586
Fig. 1. Experimental design composes by one laboratory experiment and one outdoor
587
experiment. During laboratory experiment males newt was assigned one of four dietary
588
treatments. Each treatment consisted of a long treatment (four weeks) of either high- (H) or
589
low-diet (L), followed by a short treatment (one week) of H- or L-diet. Our experimental
590
setup resulted in a full factorial design of long and short treatments for male diet: HH, HL,
591
LH, and LL. Morphological measure was carry out at t0, t4, t5 and t10 (M = morphological
592
measure). Behavioral measure was carry out at t5 (B = behavioural measure). During outdoor
593
experiment all males was placed in semi natural outdoor tanks during five weeks before
594
release in their initial pond.
595
596
Fig. 2 Variation in (a) BCI (Body Condition Index) and (b) PC1 (index of morphological
597
sexual traits including crest, hind foot web and filament length) over the experiment
598
according to the diet treatment (mean ± SE). H-diet during long and short treatments (HH),
599
black bars; H-diet during long treatment and L-diet during short treatment (HL), dark-gray
600
bars; L-diet during long treatment and H-diet during short treatment (LH), light-gray bars; L-
601
diet during long and short treatments (LL), white bars. The laboratory experiment was
602
performed between t0 and t5. The outdoor experiment was performed between t5 and t10.
603
604
Fig. 3 Relationship between PC1 at t5 (index of morphological sexual traits) and BCI at t0
605
(Body Condition Index). Males assigned to high diet during long treatment: open circle and
606
dashed line. Males assigned to low diet during long treatment: closed circles and continuous
607
line).
608
28
609
Fig. 4 Relationship between PC1 (index of morphological sexual traits) and BCI (Body
610
Condition Index) at t10.
611
612
Fig. 5 Effect of the diet treatment on (a) the time spent displaying (mean ± SE) and (b) the
613
number of quiver H-diet, black bars; L-diet, white bars.
614
615
Fig. 6 Variation of (a) the time spent displaying (mean ± SE) and (b) the number of quiver
616
according to the access or not to reproduction.
617
618
Fig. 7 Variation of the PC1 (index of morphological sexual traits) according to the access or
619
not to reproduction and the environmental stability. Access to reproduction, black bars; no
620
access to reproduction, white bars.
621
622
623
624
625
626
627
628
29
Laboratory experiment
M
t0
Outdoor experiment
M
Long diet
four weeks
t4
B
Short diet
one week
M
t5
M
five weeks
t10
High diet
Sampling
Low diet
natural diet
High diet
Release
High diet
Low diet
Low diet
629
630
Fig. 1. Experimental design composes by one laboratory experiment and one outdoor
631
experiment. During laboratory experiment males newt was assigned one of four dietary
632
treatments. Each treatment consisted of a long treatment (four weeks) of either high- (H) or
633
low-diet (L), followed by a short treatment (one week) of H- or L-diet. Our experimental
634
setup resulted in a full factorial design of long and short treatments for male diet: HH, HL,
635
LH, and LL. Morphological measure was carry out at t0, t4, t5 and t10 (M = morphological
636
measure). Behavioral measure was carry out at t5 (B = behavioural measure). During outdoor
637
experiment all males was placed in semi natural outdoor tanks during five weeks before
638
release in their initial pond.
639
640
641
642
643
644
645
646
30
0.06
+
(a)
Body Condition Index
0.04
0.02
0
-0.02
-0.04
-
-0.06
-0.08
647
+
(b)
t0
t4
t5
t 10
t4
t5
t 10
1.6
1.2
PC1
0.8
0.4
0
-0.4
-
-0.8
-1.2
648
t0
649
Fig. 2 Variation in (a) BCI (Body Condition Index) and (b) PC1 (index of morphological
650
sexual traits including crest, hind foot web and filament length) over the experiment
651
according to the diet treatment (mean ± SE). H-diet during long and short treatments (HH),
652
black bars; H-diet during long treatment and L-diet during short treatment (HL), dark-gray
653
bars; L-diet during long treatment and H-diet during short treatment (LH), light-gray bars; L-
654
diet during long and short treatments (LL), white bars. The laboratory experiment was
655
performed between t0 and t5. The outdoor experiment was performed between t5 and t10.
656
31
+
5.5
4.5
3.5
PC1 at t5
2.5
1.5
0.5
-0.5
-1.5
-2.5
-
-3.5
-4.5
-0.04
-0.02
-
0
0.02
0.04
BCI at t0
0.06
0.08
+
657
658
Fig. 3 Relationship between PC1 at t5 (index of morphological sexual traits) and BCI at t0
659
(Body Condition Index). Males assigned to high diet during long treatment: open circle and
660
dashed line. Males assigned to low diet during long treatment: closed circles and continuous
661
line).
662
663
32
+
4
3
2
PC1 at t10
1
0
-1
-2
-
-3
-4
-5
-0.15
-0.1
-
-0.05
0
0.05
0.1
0.15
+
BCI at t10
664
665
Fig. 4 Relationship between PC1 (index of morphological sexual traits) and BCI (Body
666
Condition Index) at t10.
667
668
33
Time spent displaying (s)
(a) 800
NS
NS
N=60
N=60
750
N=60
N=60
700
650
669
(b)
short
diet
Short
treatment
NS
**
13
12
Number of quivers
long
diet
Long
treatment
10
N=60
N=60
N=60
N=60
8
6
4
2
0
670
Long treatment
Short treatment
671
Fig. 5 Effect of the diet treatment on (a) the time spent displaying (mean ± SE) and (b) the
672
number of quiver H-diet, black bars; L-diet, white bars.
673
674
675
34
Time spent displaying (s)
(a) 1000
900
***
N=67
800
700
600
N=53
500
Access
access
676
(b)
13
No
access
no access
***
Number of quivers
12
10
N=53
N=67
8
6
4
2
0
Access
No access
677
678
Fig. 6 Variation of (a) the time spent displaying (mean ± SE) and (b) the number of quiver
679
according to the access or not to reproduction (boxplot).
680
681
682
683
35
1.2
+
*
0.8
PC1 at t5
0.4
NS
0
-0.4
-
-0.8
-1.2
684
Stable environment
Varying environment
685
Fig. 7 Variation of the PC1 (index of morphological sexual traits) according to the access or
686
not to reproduction and the environmental stability. Access to reproduction, black bars; no
687
access to reproduction, white bars.
688
689
690
691
692
693
694
695
696
697
698
699
700
701
36
702
SUPPLEMENTARY MATERIAL
703
Table S1. Short description of palmate newt behavior during breeding season.
step of behavior
orientation
static and retreat display
(here name display)
behavior
sniff
follow
fan
wave
whip
spermatophore transfer
quiver
touch tail
deposition
taking spermatophore
breath
breath
description
male smells the female
cloaca
male follows the female
male folds its tail against its
flank and the distal portion of
the tail vibrates rapidly
male held its tail to be
presented with a full view for
female.
male brought back its tail
against its flank with a
extremely quickly movement
after passing the female,
male quivers its tail. This
behavior represent a
spermatophore transfer
request that the female can
accept or refuse according if
it touch or not its tail (name
touch tail)
female touch the tail of male
signaling that it accepts
spermatophore transfer
male deposits one
spermatophore on the floor
female following male's tail,
moves on spermatophore
which will stick on its cloaca
male goes up to the surface
to breathe. This behavior can
occurs during each steps
describe above
704
Bold characters represent behavior used in our study. Fan, wave and whip were synthesized
705
and name display in this paper. After Halliday 1974; Halliday 1975; Denoël 1999; Wells
706
2007.
707
708
37
1
2
3
4
709
710
Figure S1. Pictures of morphological sexual traits during breeding season with natural
711
variation. 1-Male newt; 2-Crest; 3-Hind fit web; 4-Filament. All pictures were taken by JHC.
38
712
REFERENCES
713
Denoël M. 1999. Le comportement social des urodèles. Cahiers d’Ethologie. 19, 221–258.
714
Halliday TR. 1974. Sexual behaviour of the smooth newt, Triturus vulgaris (Urodela,
715
716
717
718
719
Salamandridae). Journal of Herpetology. 8, 277–292.
Halliday TR. 1975. An observational and experimental study of sexual behaviour in the
smooth newt, Triturus vulgaris (Amphibia: Salamandridae). Anim Behav. 23, 291–322.
Wells KD. 2007. The ecology and behavior of amphibians. Chicago and London. The
University of Chicago Press.
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39
SUMMARY:
Multiple signals and mate choice in the palmate newts.
The aim of this PhD is the study of multiples signals in mate choice in the palmate
newts Lissotriton helveticus. In a first part, we have made a review about multiples signals
theory (article 1). In a second part we have study the effect of ornaments on female mate
choice (article 2 et 3). In a third part we have study the trade-off between ornament and
male’s quality (article 4 et 5). Finally we have investigated the effect of environment
heterogeneity on multiples signals and male success (article 5). Globally our result shows that
access to reproduction is explain by multiples signals that need to be study in a dynamic
framework. Our results have important implication about sexual selection, population
dynamic, global change and emergent diseases.
AUTEUR : Jérémie CORNUAU
TITRE : Signaux multiples et choix du partenaire chez le triton palmé Lissotriton helveticus
DIRECTEUR DE THÈSE : Adeline Loyau, Dirk Schmeller
LIEU ET DATE DE SOUNENANCE : Station d’Écologie Expérimentale du CNRS à Moulis,
04-12-12
RÉSUMÉ :
L’objectif général de cette thèse est l’étude des signaux multiples dans le cadre du
choix du partenaire sexuel chez le triton palmé Lissotriton helveticus. Premièrement nous
avons réalisé une synthèse sur les signaux multiples dans le cadre du choix du partenaire
(article 1). Deuxièmement nous avons étudié l’importance des ornements du mâle sur le choix
des femelles (article 2 et 3). Troisièmement nous avons étudié le rôle des signaux multiples
en tant que signaux de qualité individuelle (article 4 et 5). Quatrièmement nous avons étudié
l’effet de l’hétérogénéité de l’environnement sur l’honnêteté des signaux multiples et l’accès à
la reproduction des mâles (article 5). Ces résultats ont des applications aussi bien théoriques
que pratiques sur la compréhension de la sélection sexuelle, la dynamique des populations,
l’effet des changements globaux et l’impact des maladies émergentes.
MOTS-CLÉS : Signaux multiples, Sélection sexuelle, Choix du partenaire, Condition
dépendance, Changements globaux, Triton palmé, Lissotriton helveticus
DISCIPLINE ADMINISTRATIVE : Sciences et Vie de la Terre, Spécialité Écologie
Comportementale
Station d’Écologie Expérimentale du CNRS, 2,4 Route du CNRS, 09200, Moulis, France