Valentijnsdag in het dierenrijk

Transcription

Joris M. Koene
Dierecologie, Vrije Universiteit, Amsterdam
&
Terrestrische Zoologie, Naturalis, Leiden
www.joriskoene.com
Joris M. Koene
Yumi Nakadera, Elferra Swart, Jeroen Hoffer, Fernando Monroy, Monica Lodi
A. ter Maat, N.K. Michiels, B. Reyes-Tur, S. Chiba, M. Schilthuizen, N. Anthes,
L. Schärer, P. David, S. Cummins, D. Roelofs, J. Ellers, N.M. van Straalen
Dierecologie, Vrije Universiteit, Amsterdam
&
Terrestrische Zoologie, Naturalis, Leiden
www.joriskoene.com
over de voor- en nadelen van voortplanting
Geven en nemen
Seksuele selectie en conflict
Gescheiden seksen
Simultaan hermafrodieten
Verschillen tussen Gs en Sh
Rol van accessoire geslachtsklieren
Implicaties
Kingfisher Alcedo azurea © National Geographic
Nursery-web spider Pisaura mirablis © Premaphotos
Dance Fly Empis snoddyi © M.A. Brittain
Tropical house cricket Gryllodes sigillatus © D. Funk
Direct benefit
Natural selection will favour a
mean female mating preference
f the
for
th male
l nuptial
ti l gift
ift size
i th
thatt
maximizes female fitness
Scorpionfly Harpobittacus similis © D. Gwynne
Direct benefit
Prey size increases copulation
duration
Copulation duration increases
sperm transfer
Scorpionfly Harpobittacus similis © D. Gwynne
"eggs
eggs are expensive,
expensive sperm are cheap"
cheap
Males
Females
Many cheap gametes (sperm)
Few expensive gametes (eggs)
RS depends on number of mates
RS depends on resources
Reproduc
R
ctive
succes
ss
max
Number of matings
Number of matings
Bateman 1948
"eggs
eggs are expensive,
expensive sperm are cheap"
cheap
Bateman's principle
Males
Females
more eager to mate
less eager to mate
do not expect resources from mate
expect resources from mate
invest in mate attraction
invest in offspring
less choosy (quantity matters)
more choosy (quality matters)
reproductive success more variable
reproductive success less variable
sexual selection stronger
sexual selection weaker
Reproduc
R
ctive
succes
ss
max
Number of matings
Number of matings
Bateman 1948
Sexual selection
Selection on traits that affect mating success
(e.g., secondary sexual characters: genitalia, signals, weapons, ...)
Charles Darwin 1809 - 1882
Trade-off between:
mating success (sexual selection) and survival (natural selection)
Sexual selection
Pre-copulatory
Post-copulatory
p
Intrasexual selection Male-male competition
Sperm
p
competition
p
Intersexual selection Mate choice
Cryptic female choice
Darwin 1871, Parker 1970
Competition for fertilisation
Male
C tl ejaculates,
Costly
j
l t
sperm digestion,
sperm storage
Adaptations to increase
fertilisation chances
Inhibit remating
Influence egg laying
Increase sperm storage
Reviewed in Koene 2012; Photos:
Rönn, Siva-Jothy, Jaenike, Arnqvist, Han
Damage caused by male
Crudgington & Siva-Jothy 2000
Damage caused by male reduces female fitness
Den Hollander & Gwynne 2010
Hotzy et al. 2012
Competition for fertilisation
Male
C tl ejaculates,
Costly
j
l t
sperm digestion,
sperm storage
Counteradaptations
Sexual conflict with
Female
Reviewed in Koene 2012; Photos:
Rönn, Siva-Jothy, Jaenike, Arnqvist, Han
Sperm and eggs
hermaphrodites have both
Stelt u zich voor…
Hermaphrodites
are…
Marlin (Finding Nemo)
Jabba the Hutt (Star Wars)
Gynandromorph, G1 (Zhao et al. 2010)
Hermaphroditus (Greek god)
Hermaphrodites
are everywhere!
+ most plants
Anthes 2010
Sperm and eggs
hermaphrodites have both
Does this cause fundamental differences in sexual selection?
Sexual selection "Not
Not in simultaneous hermaphrodites"
hermaphrodites
"With animals belonging to the lower
classes, the two sexes are not rarely
united in the same individual, and therefore
secondary sexual characters cannot be
developed.
…
Moreover, it is almost certain that these
animals have too imperfect senses and
much too low mental powers,
powers to appreciate
each other's beauty or other attractions, or
to feel rivalry".
Darwin 1871
Competition for fertilisation in simultaneous hermaphrodites
Sperm donor
C tl ejaculates,
Costly
j
l t
sperm digestion,
sperm storage
Baur 1998
Koene & Chasse 1998a,b
Koene et al. 20
013
Koene & Ter M
Maat 2005
Koene et al. 20
002, 2005
Inhibit remating
Influence egg laying
Increase sperm storage
Decrease sperm digestion
Bedhomme et al. 2009
Koene 2012
Tropical hermaphroditic flatworm (Pseudoceros bifurcus)
Penis fencing
Injection wounds
Sperm injection is typically unilateral
Michiels & Newman 1998
Tropical hermaphroditic flatworm (Pseudobiceros bedfordi)
Double penis fencing
Injection wounds
Sperm injection
Michiels et al. unpubl., Whitfield 2004
Competition for fertilisation in simultaneous hermaphrodites
Sperm donor
C tl ejaculates,
Costly
j
l t
sperm digestion,
sperm storage
Counter adaptations
Counter-adaptations
Sperm recipient
Koene 2012
“Shooting”
Shooting of love darts in land snails
Gilbert White "The Natural History of Selborne" 1981
Hermaphrodites
Snail mating
Dragon fly
Isabella Rossellini
Dart shooting in Cornu aspersum (Helix aspersa)
2
1
1 mm
50 µm
Both individuals shoot a dart into their partner
Koene & Chase 1998
General snail reproductive morphology
AG
Sperm storage
S
t
Sperm digestion
FPSC
HD
Diverticulum
SO
BC
FL
VD
Spermatophore
receiving
i i organ
BT
DG
DG
Mucus glands
PRM
S
V
Introduces mucus into blood
P
G
Spermatophore from partner
Koene & Chase 1998
Effect of dart shooting in Cornu aspersum
No mucus
Mucus
BC
BTD
BC
BTD
GA
GA
Inhibits sperm digestion
Koene & Chase,1998
Effect of dart shooting in Euhadra peliomphala
No mucus
Mucus
Inhibits sperm digestion
Kimura Chiba & Koene 2014
Dart:
hit
missed
Increases sperm storage
Rogers & Chase 2001
Increases paternity
Landolfa, Green & Chase 2001
Rogers & Chase 2002
Chase & Blanchard 2006
Summary of dart shooting in Cornu aspersum
Introduces mucus into blood (Adamo & Chase 1990)
Closes off sperm digesting organ (Koene & Chase 1998)
Increases sperm storage (Rogers & Chase 2001)
Sexual conflict
Increases paternity (Chase & Blanchard 2006)
Unreliable as quality signal (Koene & Schulenburg 2005)
Photos: R. Chase, C. Levesque
Can sexual conflict lead to an arms race in hermaphrodites?
Sperm donor
C tl ejaculates,
Costly
j
l t
sperm digestion,
sperm storage
Counter adaptations
Counter-adaptations
Sperm recipient
Koene 2012
Koene & Schulenburg 2005
Chilostoma glaciale
Helicigona lapicida
Chilostoma cingulatum
Arianta arbustorum
0.75
Chilostoma planospira
Marmorana scabriuscula
1.0
Marmorana serpentina
Cantareus aspersus
1.0/95
0.8/62
Cantareus aperta
0.96/72
Eobania vermiculata
0.7
0.94/77 Otala lactea
Helicidae
Theba pisana
1.0/66
Helix pomatia
1.0/99
H li llucorum
Helix
Cepaea hortensis
Cepaea nemoralis
0.64
Helminthoglypta nickliniana
0.98/89
Helminthoglyptidae
0.73
Helminthoglypta tudiculata
0.84
kelletti
Xerarionta kellettii
0.82
Humboldtiana nuevoleonis
Monadenia fidelis
0.5
0.67
Bradibaena similaris
0.97/55
Aegista vulgivaga
Bradybaenidae
Fruticicolafruticum
fruticum
Fruticola
0.65
1.0/88
Euhadra sandai
0.78
Euhadra amaliae
Euhadra q
quaesita
0.78
Vespericola colombiana
Satsuma japonica
Cernuella cisalpina
Cernuella hydruntina
0.85/61
Cernuella virgata
55
Xerosecta cespitum
Xerotricha
e ot c a co
conspurcata
spu cata
1.0/66
1.0/93
Helicella itala
Xeromunda durieui
Cochlicella acuta
0.86
Hygromiidae
Monachoides vicinus
0.86/69
1.0/99
Perforatella incarnata
1.0/98
Perforatella bidentata
Hygromia cinctella
0 85
0.85
Trichia striolata
0.99/70
1.0/98
Trichia hispida
0.98/81
Pseudotrichia rubiginosa
Monacha cartusiana
0.58
Monacha parumcincta
Leptaxis erubescens
Polymita picta
Deroceras reticulatum
1.0/99
Arion ater
Discus rotundatus
28S rRNA
0.92
0.54
0.72
0.82
no dart
no dart
no dart
no dart
no dart
no dart
no dart
no dart
0.1
Co-evolution
Co
evolution of dart with glands
4
R 0 675 p<0.0001
R=0.675,
0 0001
2
1
Bivariate Norma
al Ellipse, P=0.95
Glan
nd comple
exity
(G
Gland PC1
1)
3
0
-1
-2
-3
-4
-5
-5
-4
-3
-2
-1
0
1
2
3
4
5
Dart shape (Dart PC1)
Co-evolution
Co
evolution of dart,
dart dart sac and glands
Elaborate darts,
darts fewer dart sacs,
sacs
and larger glands
Increases effectiveness of allohormone
transfer by dart
Counter-adaptations in the spermatophore
receiving organ?
4
R=0.498, p=0.0002
3
2
1
Bivariate Normal Elllipse, P=0.95
Spe
ermatopho
ore-receivving organ
(Divvert. PC1))
Counter-adaptive
Counter
adaptive co-evolution
co evolution between love darts and
spermatophore-receiving organs
0
-1
-2
2
-3
-4
-5
5
-6
-5
-4
-3
-2
-1
0
1
2
3
4
5
Dart shape (Dart PC1)
With darts becoming more specialized for mucus transfer,
female system counteracts by making it more difficult for sperm to reach storage site
C
Co-evolu
ution
Counter-ada
aptation
Evolution of reproductive organs
28S rRNA
Chilostoma glaciale
Helicigona lapicida
Arianta arbustorum
0.75
1.0
Cantareus aspersus
1.0/95
0.8/62
Cantareus aperta
0.96/72
Eobania vermiculata
0.7
Theba pisana
1.0/66
Helix pomatia
1.0/99
H li llucorum
Helix
Cepaea hortensis
Cepaea nemoralis
0.64
0.98/89
0.73
0.84
kelletti
0.82
Monadenia fidelis
0.5
0.67
0.97/55
Aegista vulgivaga
Fruticicolafruticum
fruticum
Fruticola
0.65
1.0/88
Euhadra sandai
0.78
Euhadra amaliae
Euhadra q
quaesita
0.78
Satsuma japonica
Cernuella cisalpina
0.85/61
Cernuella virgata
55
Xerosecta cespitum
Xerotricha
e ot c a co
conspurcata
spu cata
1.0/66
1.0/93
Helicella itala
Xeromunda durieui
Cochlicella acuta
0.86
Monachoides vicinus
0.86/69
1.0/99
Hygromia cinctella
0 85
0.85
Trichia striolata
0.99/70
1.0/98
Trichia hispida
0.98/81
Monacha cartusiana
0.58
Monacha parumcincta
Leptaxis erubescens
Polymita picta
1.0/99
Arion ater
Discus rotundatus
0.92
0.54
0.72
0.82
1.0/98
Dart shooting behaviour?
0.1
Koene & Schulenburg 2005, Koene & Chiba 2006, Reyes Tur & Koene 2007, Lodi & Koene, unpubl.
Chilostoma glaciale
Helicigona lapicida
Arianta arbustorum
0.75
1.0
Cantareus aspersus
1.0/95
0.8/62
Cantareus aperta
0.96/72
Eobania vermiculata
0.7
Theba pisana
1.0/66
Helix pomatia
1.0/99
H li llucorum
Helix
Cepaea hortensis
Cepaea nemoralis
0.64
0.98/89
0.73
0.84
kelletti
0.82
Monadenia fidelis
0.5
0.67
0.97/55
Aegista vulgivaga
Bradybaenidae
Fruticicolafruticum
fruticum
Fruticola
0.65
1.0/88
Euhadra sandai
0.78
Euhadra amaliae
Euhadra q
quaesita
0.78
Satsuma japonica
Cernuella cisalpina
0.85/61
Cernuella virgata
55
Xerosecta cespitum
Xerotricha
e ot c a co
conspurcata
spu cata
1.0/66
1.0/93
Helicella itala
Xeromunda durieui
Cochlicella acuta
0.86
Hygromiidae
Monachoides vicinus
0.86/69
1.0/99
1.0/98
Hygromia cinctella
0 85
0.85
Trichia striolata
0.99/70
1.0/98
Trichia hispida
0.98/81
Monacha cartusiana
0.58
Monacha parumcincta
Leptaxis erubescens
Polymita picta
1.0/99
Arion ater
Discus rotundatus
28S rRNA
0.92
0.54
0.72
0.82
0.1
Dart shooting behaviour in Euhadra subnimbosa,
subnimbosa the samurai snail
Repeated stabbing: approx. 3311 times (21.9 min±16.0, N=11)
100 µm
1 mm
Total dart shooting phase: 56.6 min (±10.7, N=11)
B f
Before
transfer
t
f off spermatophore
t h
Koene & Chiba,2006
Similar behaviour within the family Bradybaenidae
Euhadra
subnimbosa
Bradybaena Euhadra
similaris
sandai
Euhadra
peliomphala
Euhadra
brandtii
Euhadra
quaesita
Euhadra
latispira
100 µm
3311x
< 100x
Koene & Chiba 2006
Chilostoma glaciale
Helicigona lapicida
Arianta arbustorum
0.75
1.0
Cantareus aspersus
1.0/95
0.8/62
Cantareus aperta
0.96/72
Eobania vermiculata
0.7
Helicidae
Theba pisana
1.0/66
Helix pomatia
1.0/99
H li llucorum
Helix
Cepaea hortensis
Cepaea nemoralis
0.64
0.98/89
Helminthoglyptidae
0.73
0.84
kelletti
0.82
Monadenia fidelis
0.5
0.67
0.97/55
Aegista vulgivaga
Bradybaenidae
Fruticicolafruticum
fruticum
Fruticola
0.65
1.0/88
Euhadra sandai
0.78
Euhadra amaliae
Euhadra q
quaesita
0.78
Satsuma japonica
Cernuella cisalpina
0.85/61
Cernuella virgata
55
Xerosecta cespitum
Xerotricha
e ot c a co
conspurcata
spu cata
1.0/66
1.0/93
Helicella itala
Xeromunda durieui
Cochlicella acuta
0.86
Hygromiidae
Monachoides vicinus
0.86/69
1.0/99
1.0/98
Hygromia cinctella
0 85
0.85
Trichia striolata
0.99/70
1.0/98
Trichia hispida
0.98/81
Monacha cartusiana
0.58
Monacha parumcincta
Leptaxis erubescens
Polymita picta
1.0/99
Arion ater
Discus rotundatus
28S rRNA
0.92
0.54
0.72
0.82
0.1
Dart shooting in Cornu aspersum (Helix aspersa)
2
1
1 mm
50 µm
Shoot once and lose dart
Similar behaviour: e.g. Arianta arbustorum, Cepaea nemoralis, Helix pomatia, etc.
"Dispossable"
0.92
0.54
0.72
0.82
"Reusab
ble"
Chilostoma glaciale
Helicigona lapicida
Arianta arbustorum
0.75
1.0
Cantareus aspersus
1.0/95
0.8/62
Cantareus aperta
0.96/72
Eobania vermiculata
0.7
Helicidae
Theba pisana
1.0/66
Helix pomatia
1.0/99
H li llucorum
Helix
Cepaea hortensis
Cepaea nemoralis
0.64
0.98/89
Helminthoglyptidae
0.73
0.84
kelletti
0.82
Monadenia fidelis
0.5
0.67
0.97/55
Aegista vulgivaga
Bradybaenidae
Fruticicolafruticum
fruticum
Fruticola
0.65
1.0/88
Euhadra sandai
0.78
Euhadra amaliae
Euhadra q
quaesita
0.78
Satsuma japonica
Cernuella cisalpina
0.85/61
Cernuella virgata
55
Xerosecta cespitum
Xerotricha
e ot c a co
conspurcata
spu cata
1.0/66
1.0/93
Helicella itala
Xeromunda durieui
Cochlicella acuta
0.86
Hygromiidae
Monachoides vicinus
0.86/69
1.0/99
1.0/98
Hygromia cinctella
0 85
0.85
Trichia striolata
0.99/70
1.0/98
Trichia hispida
0.98/81
Monacha cartusiana
0.58
Monacha parumcincta
Leptaxis erubescens
Polymita picta
1.0/99
Arion ater
Discus rotundatus
28S rRNA
0.1
Love darts increase male reproductive success, causing
sexually antagonistic co-evolution
Mucus loaded on the dart
Love dart of Everettia corrugata (Mollusca: Gastropoda: Dyakiidae)
100 µm
Everettia corrugata (Mollusca: Gastropoda: Dyakiidae); Koene, Thor-Seng Liew, Montagne-Wajer & Schilthuizen, 2013
Love dart of Everettia corrugata (Mollusca: Gastropoda: Dyakiidae)
True injection! Behaviour? Physiology? Paternity?
100 µm
Gland Sac
Dart
100 µm
Conclusions so far
Conclusions,
Delivery of accessory gland proteins (i.e.,
(i e
allohormones) can increase reproductive success
Current evidence is consistent with counter-adaptive
counter adaptive
co-evolution between male and female organs and
behaviour in hermaphrodites
Sexual conflict is important evolutionary force for
hermaphrodites
But are there fundamental differences in sexual
selection?
Can hermaphrodites influence both sex functions of
their mating partners?
Fundamental difference
Unidirectional
Bidirectional
Male donates, female receives,
female physiology affected
Sperm donor is also recipient,
both sexes are potentially affected
Implications for transfer of accessory gland products?
Mating behaviour of the great pond snail Lymnaea stagnalis
1. Mounting
4. Partial eversion
Photos: C. Levesque
2. Circling
3. Positioning
5. Total eversion and probing
6. Intromission
reviewed in Jarne, David, Pointier & Koene 2010
Mating system of Lymnaea stagnalis
Mixed mating in the field, with preference for outcrossing
80-100% outcrossing when sperm received
Sperm storage up to 62 days
Strategic sperm allocation
Sperm utilisation
tilisation random
High male investment
Multiple mating
Koene & Ter Maat 2007, Loose & Koene 2008, Koene et al. 2008, Hoffer et al. 2010, Nakadera et al. 2014, Nakadera et al. in prep.
Reproductive system of the great pond snail Lymnaea stagnalis
Egg mass
o
fert. pf
mi
me
ti
tc
AG
BC
PCO
M
O
C
BT
U
OT
OTD
SV
HD
V
Allosperm
AD
SD
PG
VD
PS
PP
Autosperm
PE
Prostate gland produces accessory gland proteins
reviewed in Jarne, David, Pointier & Koene 2010
Testing the effects of accessory gland proteins in Lymnaea
Koene et al. 2009, 2010
The effect of accessory gland extract on egg laying
100
Replicate 1 (N=20)
Replicate 2 (N=30)
%L
Laying eg
ggs
80
60
40
20
χ2=6.02, df=2, P=0.036
0
Control
Seminal fluid
Seminal fluid (prostate gland extract) suppresses egg laying
Koene et al. 2009
Identification of accessory gland proteins in the semen of Lymnaea
Relattive abso
orbance
1.0
0.9
0.8
0.7
0.6
0.5
0.4
0.3
0.2
0.1
a,b a,b
12
0.0
0
20
3
40
60
567 8
4
80
100
120
140
9 10
160
Time (min)
Prostate gland transfers several novel
novel, identified proteins
Koene et al. 2010
Identification of accessory gland protein suppressing egg laying
120
b
a
a
Totall eggs ± S
SE
100
80
60
40
20
ANOVA:
F2,42=3.77, P=0.03
(P
(Post-hoc:
h
P 0 05)
P<0.05)
0
Control
Ovipostatin Ovipostatin
+sperm
Koene et al. 2010
Can accessory gland proteins affect the male function?
Sexual selection in hermaphrodites
Sperm donors can use accessory gland proteins to influence
female and male sex functions of mating partner
Fundamental differences between separate sexes and hermaphroditism

Valentijnsdag in het dierenrijk

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