The Development of Radial and Biradial Symmetry: The Evolution of

AMER. ZOOL., 38:672-684 (1998)
The Development of Radial and Biradial Symmetry:
The Evolution of Bilaterality1
MARK Q. MARTINDALE 2 AND JONATHAN Q. HENRY
Department of Organismal Biology and Anatomy, University of Chicago,
1027 E. 57th St. Chicago, Illinois 60637
Department of Cell and Structural Biology, 601 S. Goodwin Ave., University of Illinois,
Urbana, Illinois 61801
INTRODUCTION
Recent reports indicate that there is surprising conservation in the cellular and molecular basis of embryonic patterning
events in organisms as diverse as mice and
insects. One can only wonder how deeply
rooted these mechanisms are within the
Metazoa, and how such a diverse array of
creatures could have evolved from an ancestor that utilized these conserved patterning mechanisms. Bilaterally symmetrical
organisms, the Bilateria, are likely to have
evolved from some kind of ancestor with a
cnidarian- or ctenophore-like level of body
construction, as members of the so-called
"Radiata" (Morris, 1993; Wainright et al,
1993; Brusca and Brusca, 1990). When attempting to formulate theories about how
such a radical change in the body plan
could arise, one must have some understanding of the developmental basis for
their construction. In contrast to many bilaterians, we know little about the development and evolution of members of the
Radiata. The evolution of the Bilateria, by
definition, is ultimately concerned with the
origins of the dorsal-ventral and bilateral
axes, yet little information is currently
available to suggest how these major body
axes might have evolved. This paper reviews various aspects of axial specification
in the Radiata, including some of recent
work on ctenophore embryos, and addresses issues regarding the invention of stereotypical cleavage programs and the possible
transitions between radial, biradial and bilaterally symmetrical body plans.
THE RADIATA
The two eumetazoan phyla which comprise the Radiata are the cnidarians and the
ctenophores. The major adult body axis of
both ctenophores and cnidarians is the
"oral-aboral" axis. In both phyla, the outer
1
From the Symposium The Evolution of Develop- epidermal epithelium surrounds an inner
ment: Patterns and Process presented at the Annual gastrodermic pouch that opens at the mouth
Meeting of the Society for Integrative and Comparative Biology, 26—30 December 1996, at Albuquerque, (Fig. 1). Separating these two layers is the
mesoglea, a largely acellular extracellular
New Mexico.
2
matrix. Although individual cells reside
E-mail: [email protected]
672
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SYNOPSIS. Understanding the evolutionary origin of novel metazoan body plans
continues to be one of the most sought after answers in biology. Perhaps the most
profound change that may have occurred in the Metazoa is the appearance of
bilaterally symmetrical forms from a presumably radially symmetrical ancestor.
The symmetry properties of bilaterally symmetrical larval and adult metazoans
are generally set up during the cleavage period while most "radially" symmetrical
cnidarians do not display a stereotyped cleavage program. Ctenophores display
biradial symmetry and may represent one intermediate form in the transition to
bilateral symmetry. The early development of cnidarians and ctenophores is compared with respect to the timing and mechanisms of axial determination. The origin
of the dorsal-ventral axis, and indeed the relationships of the major longitudinal
axes, in cnidarians, ctenophores, and bilaterian animals are far from certain. The
realization that many of the molecular mechanisms of axial determination are
conserved throughout the Bilateria allows one to formulate a set of predictions as
to their possible role in the origins of bilaterian ancestors.
673
EARLY METAZOAN DEVELOPMENT
D
Apical Organ
Polar Field
Ciliated Furrows
Tenatacle
Ctene Row
Comb Plate
Esophagus
Endodermal Canal
Mouth
Comb Plate
FIG. 1. The normal body plan of the two phyla of the "Radiata," cnidarians (A, B) and ctenophores (C, D).
Both phyla are "diploblastic" and possess an outer epidermis and inner gastrodermis (darkly shaded) separated
by a largely acellular mesoglea. The cnidarians generally have multiple planes of mirror symmetry which pass
through the major longitudinal axis, the oral-aboral axis. A. Cross section of the benthic polyp form which
attaches to the substrate via the basal discs located at the aboral pole. Numerous tentacles surround the mouth.
B. Cross section of the pelagic medusa morph. These animals swim with their mouths trailing behind. C. Lateral
view of a tentaculate stage ctenophore (e.g., Mnemiopsis) with the aboral pole located towards the top of the
page. Note that the apical organ is located on the aboral surface and is connected to each ctene row via a ciliated
groove. These animals are approximately 0.5 mm in diameter after hatching from their vitelline membrane and
retain this morphology until they are approximately 4.0 mm when they transform into lobate stage adults (not
shown). D. Diagrammatic representation of the tentaculate stage ctenophore as seen from the aboral pole. There
are eight ctene rows located on the surface of the animal and two tentacles used for capturing prey. The
endodermal canals open centrally to the stomach and terminally they run subjacent to each of the ctene rows.
Ctenophores were previously considered as "biradially symmetrical" with planes of symmetry passing through
the tentacle sheathes, and esophageal plane. (The two polar fields associated with the apical organ run along the
esophageal plane.) We now recognize, however that there are no true planes of mirror symmetry; rather, there
are an infinite number of planes of rotational symmetry due to the oblique placement of the two anal canals.
Thus, any two "halves" of a ctenophore bisected along the oral-aboral axis are only superimposable when one
is rotated 180 degrees around the oral-aboral axis.
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Basal Disc
674
M. Q. MARTINDALE AND J. Q. HENRY
the moniker "radial symmetry". There is
morphological evidence in some cnidarians
that the number of planes of symmetry may
be reduced, and that biradial (with two major planes of symmetry) or even bilateral
body plans are present (with only one plane
of mirror symmetry). For example, some
hydrozoan medusae have scores of tentacles
surrounding the margins of the bell, while
other species have only two or four tentacles. Most adult anthozoans (e.g., corals
and sea anemones) possess indicators of bilateral symmetry in the folded pleats of
their gastrodermis. Recent evidence indicates that anthozoans are the basal members
of the Cnidaria (Bridge et al., 1995; Odorico and Miller, 1997) and so it is possible
that ancestral cnidarians were not radially
symmetrical.
The symmetry properties displayed by
ctenophores are significantly different from
those of cnidarians and may represent an
intermediate step in the evolution of bilaterality. Ctenophores have been described
as being biradially symmetrical, with two
perpendicular planes of symmetry (Fig. ID)
that run through the two tentacles (the tentacular plane) and the plane of the flattened
esophagus (the "sagittal" plane) that define
four body quadrants. The endodermally derived anal canals connect the gut to the external environment via the anal pores which
are located at the aboral surface in two diametrically opposed quadrants (Fig. ID).
Thus, the tentacular and sagittal planes of
symmetry are not simple planes of mirror
symmetry. Instead, these represent planes
of two-fold mirror (rotational) symmetry.
Thus, any plane that includes the oral-aboral axis represents a plane of rotational
symmetry, including both the plane that
passes through the anal pores and the plane
orthogonal to it. In fact, ctenophores do not
possess a single true plane of mirror symmetry. The diverse nature of symmetry
properties amongst members of the Radiata
raises several questions. Do their symmetry
properties bear some relationship to those
of bilaterians? Does the establishment of
rotational symmetry have a different developmental/molecular basis than the establishment of mirror symmetry? For instance,
the presence of diametrically distinct quad-
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within or wander through the mesoglea, no
true mesodermal tissue layer is present, and
hence these organisms are often referred to
as "diploblastic." While the gastric cavity
is blind in cnidarians, ctenophores possess
two small openings on either side of the
apical organ, the anal pores, which connect
the gut cavity to the outside environment.
Effectively, the mouth also acts as an anus,
since the anal pores are too small to pass
the majority of undigested matter.
Due to the complex and diverse life history strategies present in the Cnidaria, distinctly different benthic and pelagic forms
are often generated. Most cnidarians display variations of one or both of the following morphs: a sessile polyp with a mouth
surrounded by tentacles located at the oral
end of the longitudinal axis and a basal disc
or holdfast located at the aboral end (Fig.
1A). Alternatively, a free-living pelagic medusa may be formed that possesses its
mouth at the tip of the manubrium, which
is suspended beneath a swimming bell (Fig.
IB). In most cnidarians, embryogenesis results in a solid ciliated planula larva (with
no mouth or functional gut) that has only a
single recognizable, anterior-posterior, axis.
The planula eventually metamorphoses into
a sessile polyp in which the anterior pole
of the planula (denned by swimming direction) becomes the basal disc (holdfast) and
the posterior pole becomes the mouth. In
hydrozoans, the polyp later buds a pelagic
medusa which will go on to form functional
gametes. In anthozoans, the polyp morph
produces gametes directly. On the other
hand, virtually all ctenophores are pelagic
animals with direct development. There is
no true larval phase and embryogenesis results in the production of a cydippid stage
adult. In some orders, the cydippid undergoes additional growth that transforms it
into a secondarily-derived adult, but this
does not entail a radical metamorphosis or
change in the basic body plan.
Of special interest is the diverse variation
in symmetry seen in members of the Radiata. Both cnidarians and ctenophores now
show various forms of symmetry in planes
passing along the oral-aboral axis (Fig. 1).
In some cnidarians, this takes the form of
multiple planes of mirror symmetry, hence
675
EARLY METAZOAN DEVELOPMENT
view (Fig. 2) that ctenophores are the sister
group to the Bilateria (Harbison, 1985; Ax,
1989; Schram, 1991; Eernisse et al., 1992).
However, the next few years should bring
us to a better understanding of early metazoan phylogeny.
EARLY DEVELOPMENT AND AXIAL
SPECIFICATION IN THE RADIATA
What little is known about the relationship of early development to the formation
of the body axis in cnidarians is derived
from a handful of different hydrozoan species (Tessier, 1931; Freeman, 1980, 1981,
1983, 1990). These studies have pointed out
significant parallels with some aspects of
development in ctenophores (Freeman,
1983). The eggs of both cnidarians and
ctenophores are centrolecithal and possess
a thin peripheral layer of cytoplasm surrounding a central yolk mass. Experiments
have shown that fertilized eggs of both hydrozoans and ctenophores lack any meaningful axial information that is used to construct the embryo, including the animalvegetal axis. Rather, the major longitudinal
body axis is normally set up by the initiation site of the unipolar first cleavage division. This site defines the oral pole in
both phyla (Tessier, 1931; Freeman, 1977,
1980, 1981). These features tend to unite
Deuterostomes
Protostomes
spiral/idiosyncratic cleavage1
schizocoelyl
ectomesoderm
Ctenophores
radial cleavage ' dorsoventral polarity
enlcrocoely1
mesodermal layer
Cnidarians
"Bilateria"
"Radiata"
stereotyped cleavage
program continuous digestive tract 4
signallingcenters3
endomesodermal muscle cells
Porifera
indetermiriant cleavage
epithelium] scle cells
mesoglea
oral/aboral axis
global polarity?
Blind gut
Eumetozoa
FIG. 2. Diagram indicating one likely relationship between "radially" and bilaterally symmetrical metazoans.
Recent work suggests that the ancestral bilaterians displayed radial, indeterminate cleavage and enterocoely.
Several key features of early development are mapped onto this presumed phylogeny. ('Valentine, 1997, Goldstein and Freeman, 3Martindale and Henry, 1997b, "Martindale and Henry, 1995; in preparation.).
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rants in ctenophores, which eliminates true
radial symmetry, may represent precursors
of secondary polarized axes, such as the
dorsal-ventral axis of bilaterians. On the
other hand, radial symmetry may represent
a derived condition, and all eumetazoans
may actually be constructed upon an underlying bilaterally symmetrical platform.
An understanding of the developmental
basis of the symmetry properties in the Radiata is needed before any relationship to
the evolution of bilaterian body plans can
be obtained. This information will be difficult to interpret, however, since the phylogenetic relationships of these phyla to bilaterians, and to each other, have not yet
been clarified. While cnidarians and ctenophores appear to occupy pivotal positions
in metazoan phylogeny, there is no consensus as to their exact relationships to other
extant phyla. Historically, ctenophores have
been grouped with cnidarians as the Coelenterata (Christen et al., 1991; Morris,
1993) and compelling arguments have also
been proposed which would either make the
cnidarians the sister group to the bilaterians
(Wainright et al., 1993) or position ctenophores as degenerate deuterostomes (Nielson, 1995). On the basis of developmental
and morphological evidence, and for the
sake of argument, we currently favor the
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M. Q. MARTINDALE AND J. Q. HENRY
zygote
2-cells
4-cells
• = anal canals
• = circumesophageal muscle
FIG. 3. Segregation of developmental potential for
anal canals (dark shading) and circumesophageal and
longitudinal muscle (light shading) into diagonally opposed macromeres (\EM and /EM) prior to the fourcelled stage. These differences in developmental potential are ultimately segregated into the V2M and /2M
macromeres at the 60-cell stage.
the development of cnidarians and ctenophores is the fact that there is a precocious
segregation of developmental potential into
identified blastomeres in ctenophore embryos. For example, each of the first four
cell divisions in ctenophores is associated
with important developmental decisions.
First cleavage establishes the oral pole and
sagittal axis (Freeman, 1977). Second
cleavage establishes the tentacular and anal
axes (delimits the "/" vs., "\" quadrants,
Fig. 3; see Martindale and Henry, 1995; in
preparation). Third cleavage delineates the
E and M lineages and involves the differential segregation of light producing potential to the M cells, and comb plate potential
to the aboral pole (Freeman and Reynolds,
1973). Fourth cleavage segregates the comb
plate-forming potential to the e, (Reverberi
and Ortolani, 1963; Farfaglio, 1963) and m,
micromeres and comb plate-inducing potential to the e, micromeres (Martindale and
Henry, 1997£>). These determinative events
in the early cleavage program are accompanied by the condition in which ctenophore embryos have virtually no capacity
to regulate following the removal of various
embryonic regions (Chun, 1880; Martindale
and Henry, 1991b). In most cnidarians,
however, there is no evidence of regional
specialization other than the initial formation of the oral pole at first cleavage. Subsequent cleavages are not utilized to establish pattern along or around the major longitudinal body axis, and no differences can
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the ctenophores and cnidarians because no
other metazoans appear to display these developmental features (Goldstein and Freeman, 1997). It is interesting to note, however, that the oral pole of adult cnidarians
(hydrozoans) is generated from the posterior pole of the planula larva. This seems
to indicate that there is an "inversion" of
axial properties in cnidarians between different life history phases and that the relationship of the earliest determinative events
are conserved relative to the adult body
plans in these two taxa.
In most metazoans, a stereotypical species- and often phylum-specific cleavage
program ensues after fertilization. Virtually
all cnidarians lack such a regular cleavage
program. In fact, cnidarian development often involves "chaotic" cleavage in which
no two embryos in the same spawning will
exhibit an identical cleavage pattern. In
some species, cleavage furrows regress,
forming temporary syncytia that cellularize
at later stages of development. The absence
of a cleavage program suggests that cells
do not become reproducibly positioned
with respect to other cells and that it is impossible to identify homologous cells from
embryo to embryo. In contrast to cnidarian
development, ctenophores develop according to a highly stereotypic and phylogenetically unique cleavage program not shared
by any other extant phylum. For example,
the first and second cleavages always correspond to the sagittal and tentacular planes
of symmetry, respectively. The cells in the
ctenophore embryo can all be identified,
their developmental history deduced by
their position within the embryo, and their
normal fates followed both within and between different species (see Reverberi,
1971; Ortolani, 1989, and Martindale and
Henry, 1997a for reviews). Ctenophores
may represent the most basal extant metazoan phylum to have evolved a stereotyped
cleavage program that delineates distinct
lineages of cells during early embryogenesis.
Information is known about how the
cleavage program segregates developmental
potential to specific regions of the developing embryo in many types of metazoan
embryos. One fundamental difference in
EARLY METAZOAN DEVELOPMENT
that display rudimentarily discrete cleavage
programs. Experiments by Freeman (1983)
have also shown that some trachyline hydrozoans and the bilaterally symmetrical siphonophores also segregate developmental
potential via the early cleavage divisions. In
one, but not all species of siphonophore,
first cleavage corresponds to the sagittal
body axis. In other species, the fates are
associated with the appearance of distinct
germ layers at the eight-cell stage, separating prospective endoderm from ectoderm.
While these determinative decisions are not
obviously homologous to the cell lineage
decisions taking place in ctenophores they
indicate that regular cleavage programs in
basal metazoans can be recruited to accomplish different developmental decisions.
Does the co-option of stereotypical cleavage patterns, which segregate developmental potential within an isotropic egg, represent an important step in the generation of
novel body plans (e.g., conversion between
radial, biradial or bilateral symmetry)? If
cnidarians and/or ctenophores are derived
from bilaterally symmetrical forms then the
variations in cleavage programs and timing
of cell commitment events might have more
to do with changes in life history strategy
than with changes in body plan. For example, ctenophores, siphonophores and trachyline hydrozoans are all direct developers
and the precocious segregation of developmental potential may be related to the advantages in the rapid formation of the adult
body plan (Freeman, 1981, 1983).
The precocious segregation of developmental potential present in ctenophore embryos is not shared by all metazoans. One
of the primary roles of the cleavage program in metazoan evolution might have
been to establish "signaling centers" which
helped direct the fates of neighboring cells.
In that they lack a stereotyped cleavage program, cnidarians do not appear to possess
this capacity, and every cell is functionally
interchangeable with any other cell during
the early phases of development. Virtually
all other metazoans demonstrate localized
sites or "poles" of inductive activity. For
example, several metazoan phyla display a
pattern of cleavage known as spiral cleavage. In these forms, the dorsal-ventral axis
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be identified amongst the embryonic cells
(Freeman, 1983). Instead, cells appear to
become determined at later developmental
stages by virtue of cell-cell interactions that
operate within developmental fields (Freeman, 1981). Thus, the timing of cell commitments and the ability to regulate are dramatically different between members of the
Radiata.
This is not to say that in ctenophores
each and every cell is determined at the
time of its birth. Recent work has shown
that cell-cell interactions are required for
the normal appearance of comb plates by
m, micromere descendants and the endodermal canals in ctenophore embryos (Martindale, 1986; Martindale and Henry,
1997&). The cleavage process is involved in
segregating the developmental potential for
this inducing activity to the e[ micromere
lineages. The lineage-specific signaling activity observed in ctenophores and in virtually all bilaterians illustrates another, often overlooked, aspect of stereotypical
cleavage programs, namely that cells are
generated and reside in predictable locations within the embryo. Stereotyped cleavage programs can not only segregate inducing potential to discreet regions of the embryo, but also place other cells in defined
and reproducible locations with respect to
these signaling centers. The fact that individual cells assume reproducible fates within the ctenophore embryo has led to the
false assumption that all identified cell lineages are denned precociously (Reverberi,
1971; Ortolani, 1989). Only experimental
intervention is able to discriminate between
cells that are specified early, and those
whose determination requires interactions
with adjacent cells. The most dramatic example of this phenomenon is seen in the
development of the soil nematode C. elegans in which numerous cell interactions
play an important role during early embryogenesis despite the occurrence of stereotyped cleavage patterns (see Schnabel,
1997 for a recent review).
The notion that stereotypical cleavage
programs were co-opted early in metazoan
evolution to localize developmental potential is reinforced by the finding that there
are some highly derived cnidarian embryos
677
678
M. Q. MARTINDALE AND J. Q. HENRY
rows and that there has been a reduction to
the stable 8 rows present in all extant combbearing species. Does this reduction in morphological complexity represent a move to
bilaterality within the Radiata? In other
words, do such axes as the dorsal-ventral
axis arise de novo in a polarized fashion via
the establishment of a localized signalling
center, or do such axial properties arise
from unpolarized axes that subequestly become polarized (like the anal axis of ctenophores)?
Ctenophores are composed of four nearly
identical quadrants separated by the tentacular and esophageal (sagittal) planes (Fig.
2D). Each of these planes would define
planes of mirror symmetry were it not for
the presence of the anal canals. Cell lineage
studies have shown that each of the four
quadrants normally contributes to structures
along both the tentacular and esophageal
axes. For example, each of the first four
cells gives rise to portions of one of the
tentacular apparati. This situation is not true
for the formation of the anal canals. Cell
lineage analysis in the lobate ctenophore
Mnemiopsis leidyi has revealed a phenomenon that we refer to as "diagonal determination" (Martindale and Henry, 1995).
The two endodermally-derived anal canals
are generated from descendants of diagonally opposed 2M macromeres at the 60
RELATIONSHIP OF AXIAL PROPERTIES IN
cell-stage (the backslash or "\" pair). The
THE RADIATA AND BLLATERIA
other two 2M macromeres (the slash or "/"
A variety of possible scenarios for early pair) do not contribute to the formation of
evolution in the Metazoa have been consid- anal canals, but they do make circumesoered in detail (Hyman, 1940; Hadzi, 1963; phageal and longitudinal muscle cells,
Salvini-Plawen, 1978; Neilsen, 1995). If bi- which are not produced by the "\" lineages.
laterians are derived from a radially or bi- Thus, these four seemingly identical 2M
radially symmetrical stock, how did these macromeres, which are all in contact with
new symmetry properties arise? Did the one another at the animal (oral) pole, are
evolution of a new axis, the dorsal-ventral differentially organized as two pairs of diaxis, arise from an already existing axis, agonally opposed cells (Fig. 3). In fact,
like the tentacular or anal axes? Or, did it these quadrant specific differences are esarise de novol Bilaterality might have ap- tablished at the four-cell stage.
peared by a suppression or modification of
Depending on whether radial or bilateral
aspects of a radially symmetrical patterning symmetry is ancestral, the anal axis of ctenmechanism in which only a single axis was ophores could represent an incipient preco-opted for future elaboration. Recently cursor, or a remnant, of the dorsal-ventral
discovered fossils from the Mid- and pos- axis found in bilaterians. Does the formasibly even Lower-Cambrian (Morris and tion of the anal axis in ctenophores tell us
Collins, 1996) suggest that ctenophores anything about how bilateral symmetry
may have once had as many as 80 comb arose in metazoan evolution? Our ability to
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is "organized" by the so-called D quadrant.
The early spiralian cleavage program is extremely important in both the establishment
of the D quadrant, as well as the organizing
influence the D quadrant macromere has on
adjacent cells (See Verdonk and Cather,
1983; van den Biggelaar and Guerrier,
1983; see also the paper by Boyer and Henry, 1998). In some situations such signaling
centers have profound global effects on axial organization (e.g., vertebrate, echinoderm, nematode, and spiralian phyla) while
in others they may serve to provide localized inductive cues (ctenophores). This
strategy is in marked contrast to the evolution of a complex cleavage program in
which fates of each and every cell are predetermined during the embryonic period as
a "mosaic" of individual parts of the larval
or adult body plan. It should be noted that
no organism exhibiting such a "mosaic"
pattern of development has ever been
found. Recent arguments have been made
that bilaterian ancestors displayed radial
and indeterminate cleavage (Valentine,
1997). Figure 2 indicates some of the key
features of early embryogenesis at the base
of the Metazoa. The role of the cleavage
process and regional determination in metazoan evolution has been thoroughly covered elsewhere (Davidson, 1991).
679
EARLY METAZOAN DEVELOPMENT
B.
C.
j ~ | =Ct-labial
| | = Ct-Antp
obtain answers to these questions is hampered by the fact that we do yet not understand the relationships of the major body
axes of the radiata to those of the bilaterians. It is often assumed that the major longitudinal axis of the Radiata (oral-aboral
axis) is homologous to the anterior-posterior axis of bilaterians. However, there is no
compelling evidence to support this claim,
and even if it holds, it remains unclear
which end of the oral-aboral axis corresponds to the anterior pole in bilaterians.
This question has become all the more interesting and tractable due to recent work
showing a conserved molecular basis for
the formation of both the anterior-posterior
and dorsal-ventral axes in bilaterians.
Several interesting implications arise
when one considers the possible evolutionary transitions between radial and bilateral
symmetry. Highly conserved and robust
molecular markers currently exist for both
the anterior-posterior (Slack et al, 1993;
Akam, 1995) and dorsal-ventral axes (Ferguson, 1996; DeRobertis and Sasai, 1996)
in all bilaterians thus examined, and it is
likely that these genes are also expressed in
radially and biradially symmetrical metazoans. The markers for the anterior-posterior axis are the Hox genes. Hox genes have
been reported in both cnidarians (Schierwater et al, 1991; Schummer et al, 1992;
Naito et al, 1993; Shenk et al, 1993a, b.
Finnerty and Martindale, 1997) and ctenophores (Finnerty et al, 1996); however
their patterns of expression have yet to be
thoroughly explored in either group. A
comparison of Hox gene expression in the
Radiata might reveal the actual relationship
of the longitudinal axes in these two
groups. For example, if "anterior" Hox
genes (such as a labial ortholog) are expressed closer to the mouth than "midbody" or "posterior" Hox genes, it would
provide evidence that not only are the oralaboral axis and the anterior-posterior axis
homologous, but that the polarity along
these axes has been conserved (Fig. 4A).
The fact that adult ctenophores swim with
their mouth forward, they possess anal canals on the side opposite the mouth, and the
oral pole is derived from the "animal" pole
of the embryo (as defined by the first cleavage division) suggests that the oral pole in
ctenophores corresponds to the anterior
pole of bilaterian descendants.
If, on the other hand, the polarity of Hox
gene expression is reversed, and "anterior"
genes are expressed closer to the aboral
sense organ (Fig. 4B), it would suggest that
the mouth of radially/bilaterally symmetrical metazoans is homologous to the anus of
bilaterians and that the mouth may have
evolved in different locations in protostome
and deuterostome lineages (see below). Of
course, it is also possible that the anterior-
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FIG. 4. Diagram indicating some possible expression patterns of Hox genes in the Ctenophora. Predicted
relationship of two Hox genes, including: an "anterior" Hox gene Cteno labial like and a "midbody" CtenoAntp-like ortholog. (A) If "anterior" Hox genes are expressed around the oral pole one can argue that the
common ancestor of protostomes and deuterostomes did not form mouths independently from a blind digestive
tract, and this suggests that there was a shift of the mouth to the dorsal side in deuterostomes from an ancestral
ventral location in protostomes (Lacalli, 1996). (B) If "anterior" Hox genes are expressed at the aboral end of
ctenophores, one can argue that the oral pole of radially/biradially symmetrical organisms has become the anus
of bilaterians, and that new mouths appeared independently in protostomes and deuterostomes. (C) Hox gene
expression patterns may exhibit other relationships to the oral-aboral axis.
680
A
M. Q. MARTINDALE AND J. Q. HENRY
Bilaterian Metazoans
Protostome-like Ancestor
Deuterostome
dpp/Bmp-4
sog/chordin
sog/chordin
M
dpp/Bmp-4
Deuterostome
aboral
Radial Cnidarian-like Ancestor
oral
Biradial Ctenophore-Iike Ancestor
Deuterostome
sog/chordin
anal canals
aboral
oral
r—1 _ Neurogenic region and
"—'
area of sog/chordin expression
FIG. 5. Possible scenarios for the formation of the metazoan dorsal-ventral axis and its implications for the
relationship of the oral-aboral axis of radial/bilaterally symmetrical animals to the anterior-posterior axis of
bilaterians. dpplBMP-4 and sog/chordin orthologs are likely to be involved in establishing the dorsal-ventral
axis in both extant protostomes and deuterostomes (see Ferguson, 1996 for review). The position of the neurogenic region of both protostomes ("ventral") and deuterostomes ("dorsal") is marked by the expression of
sog/chordin orthologs (shading). A. Formation of a deuterostome body plan from a protostome-like ancestor
that already possessed well-defined anterior-posterior and dorsal-ventral polarity. The position of the mouth
changed in deuterostomes such that the mouth forms on the side opposite the central nervous system. B. The
mouth of protostomes and deuterostomes could have formed independently from an ancestor that possessed a
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B
EARLY METAZOAN DEVELOPMENT
possessed a blind gut and a dorsal-ventral
axis. In this case, mouths would have
evolved independently on different sides of
the embryo with respect to the dorsal-ventral axis in protostome and deuterostome
lines (Lacalli, 1996). If this scenario is true,
it implies that there might have been an
"inversion" of the anterior-posterior axis,
where the mouth (the common mouth and
anus) of the ancestor became the anus of
bilaterians (Fig. 5B). The possible "inversion" of the oral-aboral axis points to the
uncertainty in the evolutionary relationship
of the body plans of radially and biradially
symmetrical organisms to those of bilaterians. No good transitional organism extant,
or fossilized, has yet been identified and the
number of potential candidates, including
the fiatworms, appears to dwindle as the
phylogenetic relationships of the Metazoa
are unraveled (Aguinaldo et al., 1997; Balavoine, 1997; Valentine, 1997).
A third scenario can also be considered
(Fig. 5C). If a ctenophore-like organism
represents the ancestor of both protostomes
and deuterostomes, their descendants might
have co-opted an existing axis (such as the
anal axis) for constructing the dorsal-ventral axis. In this situation, asymmetric polarity along that axis would develop, possibly as the ancestors assumed a benthic existence, and descendent lines would have
had to utilize one of the anal canals as their
new mouth. Whether the anal pores of ctenophores represent the sites of either the protostome or deuterostome mouth remains to
be seen.
There should be a way to determine
whether the ctenophore anal axis (or other
axes such as the tentacular or esophageal
axes) represents an incipient dorsal-ventral
axis. Recently, two sets of genes have been
identified in fly and amphibian embryos
which are causally involved in the estab-
blind gut and dorsal-ventral polarity. This ancester was presumeably derived from a radially symmetrical stock
possessing no dorsal-ventral axis and a peripheral nerve net along the oral-aboral axis. C. Deuterostomes and
protostomes could have been derived through the selective loss of one of the anal canals from a ctenophorelike ancester. This suggests that the anal axis of ctenophores corresponds to the future bilaterian dorsal-ventral
axis and that polarity along that axis evolved secondarily. A = anus, M = mouth. The ? indicates a possible
pattern of expression for dorsal-ventral patterning genes. It is not yet known whether members of the Radiata
possess dpplBMP-4 or soglchordin orthologs. See text for additional details. (A, and B, after Lacalli, 1996).
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posterior axis is not homologous with the
oral-aboral axis. It could be, for example,
that the oral-aboral axis corresponds more
closely with the dorsal-ventral axis (Fig.
4C). For example, there are some derived
ctenophores which have abandoned their
pelagic existence and live on the sea floor.
These "creeping" ctenophores lose their
comb rows late in embryogenesis and move
about with their mouth towards the substrate (i.e., "ventral") but with no preferred
direction of movement, that is, no anteriorposterior polarity (G. Freeman, personal
communication). In addition, it could be
that the relationship of the oral-aboral axis
is different between ctenophores and cnidarians, requiring that we completely reevaluate the phylogenetic relationship of
these organisms to other extant metazoans
(see Nielsen, 1995, for example). Finally,
Hox genes may not be deployed in axis
specification, but may be involved in cell
type determination or other developmental
functions (Davidson, 1991).
Lacalli (1996) has pointed out two possible scenarios for the evolution of the dorsal-ventral axis in bilaterians that also have
implications for the formation of the anterior-posterior axis. In one scenario, an ancestor possessed a continuous digestive
tract and dorsal-ventral polarity (as evidenced by the placement of the central nervous system and mouth on the ventral side).
Deuterostomes, which utilize orthologous
genes to establish the dorsal-ventral axis
(see below), would have evolved by the formation of a new mouth, or through migration of the existing mouth to the ancestral
"dorsal" side of the embryo (Fig. 5A). This
scenario is complicated by the difficulty of
envisioning transitional forms where the
mouth attains the new position. Another
scenario predicts that the common ancestor
of both protostomes and deuterostomes
681
682
M. Q. MARTINDALE AND J. Q. HENRY
SUMMARY
While some aspects of early development
are shared in the embryos of cnidarians and
ctenophores, similarities are lost quickly after the first cleavage division. Ctenophores
display a stereotyped cleavage program that
generates cells in distinct positions with respect to other cells within the embryo and
segregates developmental potential into defined lineages. Inductive ability is also redistributed into distinct cell lineages in
ctenophore embryos and it is likely that the
coordinated deployment of inducing activity, resulting in the formation of "organizing centers," may be one of the fundamental inventions of metazoan developmental
programs that allowed for the establishment
and exploitation of bilaterally symmetrical
body plans (Fig. 2). The extent to which
such changes in the early cleavage program
have led to the radiation of diverse metazoan phyla exhibiting bilaterally symmetrical body plans, or whether these events
are related to changes in life history stratagies, remains unclear. One way of understanding these changes is to learn more
about the molecular basis of axis specification in the "Radiata," as virtually nothing is known about the evolution of the dorsal-ventral axis or the relationships between
the oral-aboral or anterior-posterior axes in
these animals. While we can speculate on
these evolutionary events, the mechanistic
basis for body plan evolution underlying
the transition from radial to bilateral symmetry will be difficult to interpret until
metazoan realationships are known.
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Corresponding Editor: Gregory A. Wray
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