Origins of metazoan body plans: the larval revolution

The origins of bilaterian animal body plans are generally thought about in terms of adult forms. However, most animals have larvae with body plans, ontogenies, and ecologies distinct from their adult forms. The first of two primary hypotheses for larval origins suggests that the earliest animals were small pelagic forms simi- lar to modern larvae, with adult bilaterian body plans evolved subsequently. The second suggests that adult bilaterian body plans evolved first and that larval body plans arose by interpolations of features into direct-developing ontogenies. The two hypotheses have different consequences for understanding parsimony in the evolution of larvae and of developmental genetic mechan- isms. If primitive metazoans were like modern larvae and distinct adult forms evolved inde- pendently, there should be little commonality of patterning genes among adult body plans. However, sharing of patterning genes in adults is observed. If larvae arose by co-option of adult bilaterian-expressed genes into independently evolved larval forms, larvae may show morpho- logical convergence but with distinct pattern- ing genes, as is observed. Thus, comparative studies of gene expression support independ- ent origins of larval features. Precambrian and Cambrian embryonic fossils are also consistent with direct development of the adult as primi- tive, with planktonic larval forms arising during the Cambrian. Larvae have continued to co-opt genes and evolve new features, allowing study of developmental evolution.
5.1 Evolutionary biology has primarily been about the study of adults

It is striking that studies of evolutionary histor- ies are nearly all about the evolution of adults. Palaeontologists, having only a few fossil larval forms, perforce have had to study adults, which make up most of the fossil record. Transitions that can be studied are almost inevitably those of adult character states. In popular representations this translates into computer animations where fins transform into legs, dinosaurs morph into birds, or apes into hominids—beguiling but misleading images. The bias extends to phylogeny, as most available characters are adult ones. Our defini- tions of the body plans of phyla are of adult body plans. This bias persists in evo-devo, which largely focuses on the evolution of novel adult features, for example the loss of legs in snakes and the origin of the turtle shell. These examples are approached by studies that combine morphological, palaeonto- logical, and gene regulatory data (Cohn and Tickle,
1999; Gilbert et al., 2001). Developmental biol- ogy also focuses primarily of the development of adults. This is largely dictated by interest in major body parts, for example insect wings or tetra- pod legs. Another source of the bias arises from our genetic and developmental model systems, limited to a few chosen for ease of laboratory use (Bolker, 1995; Jenner and Wills, 2007). Essentially all major genetic model systems are direct devel- opers, where the adult body plan of the phylum is generated progressively in development, even if



43

44 AN I M AL EV O L UTI O N



some form of metamorphosis occurs. This is true of Caenorhabditis elegans, a nematode, Drosophila melanogaster, an arthropod, or zebra fish, frogs, or mice—all vertebrates. The evolution of adult bias does not mean that early development is ignored, but that it is largely the study of early development leading to adult characters.


5.2 Most phyla have a second body plan

Not only has our focus been on the origins of adult body plans, but, of the phyla examined, vertebrates and arthropods have received the bulk of atten- tion in studies of evolution among Bilateria. Both phyla have been highly successful in terrestrial as well as marine environments and are primitively direct developers (Jenner, 2000; Sly et al., 2003). The result of the focus on these phyla is that the second largest episode of metazoan body plan evolution, that of larval body plans, has been less appreciated. The majority of the 33 or so bilaterian phyla are pri- marily or exclusively marine and exhibit indirect development in which a larval form with a body plan distinct from the adult is present (Figure 5.1). A radical metamorphic event finally releases the adult form at the end of larval development. These phyla thus have a distinct second life-history stage—that of their larval forms. These larvae differ greatly from the adults in ecology, and are generally plank- tonic filter feeders whereas their adults are benthic and often effectively sessile. Such larvae have his- torically been called ‘primary larvae’, on the basis of the historical idea that larval forms represent the primitive body plans of ancestral metazoans.
5.3 Did adult or larval body plans arise first?

How did two distinct kinds of body plans evolve? The classic view, which derives from Haeckel’s recapitulation theory, is that the first metazoans were similar to living larvae. Jågersten (1972) sum- marized it like this: ‘. . . the two phases of the life cycle arose when the adult of the primeval ances- tor of the metazoans, viz, the holopelagic, radially symmetrical Blastaea, descended to life on the bot- tom (and became bilateral), while its juvenile stage remained in the pelagic zone’. Nielsen and Nørrevang (1985) and Nielsen (1995) in the same vein sug- gested that a pelagic gastraea animal evolved into a pelagic trochaea animal (that is, resembling a particular type of living feeding larva), which was ancestral to protostome and deuterostome phyla. Nielsen (2008) has linked this scenario to a founda- tion in sponge larvae.
This hypothesis was incorporated, in the devel- opmental-genetic era, to mesh with inferences about gene regulatory systems (Davidson et al.,
1995). Gene regulatory systems of ancestral plank- tonic animals were hypothesized to resemble those found in living marine larvae (Figure 5.2). Bilaterian adults were suggested to have evolved through the innovation of imaginal ‘set aside’ cells distinct from the majority of differentiated larval cells. The imaginal cells gave rise to tissues of a new adult stage, and metamorphosis evolved to complete the transition. The new adults evolved a novel gene regulatory system similar to those of living adult bilaterians, including novel use of Hox genes to pattern the antero-posterior body axis.



(a) (b) (c)




Figure 5.1 Examples of indirect- developing planktotrophic larval forms: two lophotrochozoans and a deuterostome:
(a) Müller’s larva of a platyhelminth flatworm;
(b) trochophore of an annelid; (c) pluteus larva of a sea urchin. All are feeding larvae with guts and ciliary bands of various types. Parts (a) and (b) courtesy of G. Rouse.

E V OL UTION OF L A R V A L ST A G ES 45



This scheme explains the lack of an early meta- zoan body or trace fossil record as all evolution would have taken place in tiny planktonic adults. It ties larval forms into a phylogenetic scheme in which larval forms provide accessible proxies for the unfossilizable ancestors, and gives a develop- mental twist to the Cambrian radiation—the first fossil animals resulted from the appearance of new body plans.
There are difficulties for this interlinked suite of hypotheses (Sly et al., 2003; Peterson 2005; Peterson et al., 2005). Notably the larva-first hypothesis requires a vast number of convergent events, accounting for the massive molecular similarities in use of Hox and other regulatory genes in sup- posedly independently evolved descendant clades with benthic body plans. Further, somehow a selective role for set aside cells has to be accounted for before a new bilateral and benthic adult stage has evolved, which requires selection for novel developmental elements prior to need.
The planktonic metazoan ancestor has little evi- dence supporting it beyond analogies between the ontogeny of living larval forms and evolution of hypothetical ancestors. There is a second and more plausible evolutionary possibility, that the first bilaterians were just that, small benthic bilat- erally symmetric triploblastic animals similar in
complexity to living acoel flatworms (Figure 5.2). Molecular phylogenetic studies suggest that acoels may be the most basal living bilaterians (Ruiz- Trillo et al., 2004; Sempere et al., 2007), although this deep position is debated (Dunn et al., 2008). Developmental data also support the position of acoels as basal bilaterians (Hejnol and Martindale,
2008a). Acoels are direct developers, and possess anterior, middle, and posterior group Hox genes (Baguñà and Riutort, 2004; Ramachandra et al., 2002). The last common ancestor of protostomes plus deu- terostomes (PD ancestor) was probably somewhat more complex than acoels, and possessed the gen- etic machinery basic to eye development, nephridia, heart, and other mesodermal tissues (Erwin and Davidson, 2002; Erwin, 2006; Baguñà et al., 2008). This does not mean that these structures were pre- sent in derived states as seen in living protostomes or deuterostomes. It does mean that acquisition of bilaterian features was stepwise, with some fea- tures attained between the split from cnidarians to the acoelomorph grade, and further acquisitions from there to the PD ancestor. Further evolution of features characterizing the stem groups of phyla would have represented a third stage in evolution of features (Baguñà and Riutort, 2004).
The proposal of an ancestral benthic bilaterian
ancestor requires a hypothesis for the secondary





Novel adult body plan

Conservation of larval body plan

Novel larval body plan
Conservation of adult bilaterian body plan


Metamorphosis
Set aside cells
Novel regulatory genes

Planktonic adult, larva-like gene regulation


Planktonic larva-like ancestor
Metamorphosis
Larva-like regulation
Gene co-option


Benthic adult, bilaterian adult gene regulation


Benthic bilaterian ancestor

Figure 5.2 Conflicting larva-first and adult-first hypotheses of bilaterian origins. The hypotheses posit amounts of evolutionary change along branches leading to more derived developmental changes. In the larva-like ancestor hypothesis (left), most evolution of developmental characters lies on the branch leading to the benthic adult, with the larva retaining ancestral features. In the benthic bilaterian ancestor case (right), most evolution lies in the line to the planktonic larva, with the adult retaining ancestral features. Both hypotheses illustrate single lineages, but in the metazoan radiation, numerous lineages evolved in parallel. A large degree of homoplasy results in either case. The amount of convergence required to evolve planktonic larvae with their relatively simple organization is substantially less than evolving the entire basic suite of adult bilaterian features in 33 or so lineages.

46 AN I M AL EV O L UTI O N



evolution of the indirectly developing planktonic larvae, in place of the ancestral larval hypoth- esis. The inference of an ancestor lacking a larva has led to the intercalation model of larval origins (Valentine and Collins, 2000; Sly et al., 2003). In this hypothesis, ancestral bilaterians are hypothesized to be small worm-like creatures, perhaps part of an acoelomorph radiation. These ancestral bilateri- ans were direct developers, and had evolved the basic developmental gene regulatory systems of bilaterian development. With the opening of the Cambrian radiation, the evolution of more diver- gent bilaterians accelerated, and produced the basal clades that gave rise to modern phyla (Budd and Jensen, 2000), but planktonic larvae and their body plans evolved secondarily.
The requirements for a planktonic larva are sim- pler than for the larger benthic reproductive adult. Table 5.1 separates the characters of the benthic PD ancestor from those selected for in the evolution of a planktonic larva. Larvae require ciliary bands for swimming and capture of microscopic prey. A mouth and gut are needed to process prey. Simple neural systems allow some control of muscle-cell contraction, for example in the pharynx. Other sen- sory information allows avoidance responses and ultimately detection of signals from the substrate biofilm to induce metamorphosis. For the devel- opment of a coherent larval symmetry, systems



Table 5.1 Characters required to evolve a planktonic feeding larva from a benthic bilaterian.
for the determination of the larval axes (animal– vegetal, dorsoventral, and left–right) are needed. In order for the switch from larval to adult develop- ment, a developmental switch that controls cellular fates has to be assembled from existing signalling systems in more primitive metazoans (Matus et al.,
2006a). Finally, a system for metamorphosis evolves, which probably initially involves transformation of most larval cells and tissue into adult tissues. However, slow metamorphosis increases vulner- ability, and selection should favour evolution of a more rapid and efficient system using imaginal cells set aside as adult precursors within the larva to ensure rapid metamorphosis (Hadfield, 2000).
Sly et al., (2003) predicted that some portion of genes required for adult development and life history would have been co-opted to direct the acquisition of a set of features involved in the sim- pler larval ontogeny required to produce a new life-history stage of an indirect-developing feed- ing larva. The acquisition of features would have involved step-wise intercalation of genes already used in the adult to generate features of the larva. The most basic requirement for feeding structures was probably met by the use of some of the adult gut programme. We have found evidence to sup- port this idea in the common expression of genes in the gut of the sea urchin pluteus larva and in adult gut (Love et al., 2008). Other features, for example the apical plate with its ciliary tuft, have co-opted unrelated sets of regulatory genes in sea urchin versus mollusc larvae (Dunn et al., 2007). Larval evolution is suggested to have been a sequential assembly of features that would have diverted

Characters required in larvae
Adult characters not required in larvae
the ancestral course of development into two tem-
porally distinct streams, one that first produced a


Ciliary bands Locomotory appendages Gut Respiratory system Mouth Reproductive organs
feeding larva and a second stream that, from larval tissue, developed the juvenile adult. Imaginal cells and a discrete metamorphosis would have more

Simple neural/sensory system
Brain
sharply separated the two ontogenetic trajectories.
The second consequence of the intercalation

Axial determination Strongly expressed anteroposterior axis
hypothesis is that different metazoan lineages
would simultaneously have evolved planktonic lar-

Developmental switch to adult feature ontogeny
Nephridia
vae. Convergence would have been highly prevalent as the rise of feeding larvae followed in time the

Metamorphosis Eyes
Circulatory system
Skeleton
splitting of metazoan phyla or their precursor lin- eages. These evolving lineages would have evolved planktonic larvae with features noted in Table 5.1,

E V OL UTION OF L A R V A L ST A G ES 47



gained by co-option of different suits of regulatory genes to accomplish control of the development of broadly similar larval morphological structures. None the less, the convergence required would have been far less profound than that needed to independently evolve many lineages of bilaterians with the more complex features of the PD ancestor (Table 5.1).


5.4 Phylogeny and hypotheses of larval origins

The two hypotheses have distinct phylogenetic consequences with respect to mapping of devel- opmental features onto evolutionary history. The scheme with a larva-like plan first is difficult to reconcile with recent phylogenies of bilaterian metazoan clades. First, molecular phylogenetic analyses do not support a metazoan phylogeny in which basal clades are indirect developers (Dunn et al., 2008). Jenner (2000) noted that the strongest data allowing a decision on the primitive develop- mental mode would come from phylogenetic stud- ies in which a wide range of ‘minor’ non-coelomate phyla were included. He tested the occurrence of indirect versus direct modes of development using a phylogenetic tree on which minor as well as major phyla were mapped. Figure 5.3 shows an analo- gous tree. Direct development appears primitive in bilaterians and indirect-developing planktonic larvae have arisen independently in lophotrocho- zoans among the protostomes and in the echino- derm + hemichordate clade of deuterostomes. The other deuterostome clade, the chordates, is direct- developing. The echinoderms and hemichordates share a planktonic larval form, but the highly diverse lophotrochozoan clades (molluscs, anne- lids, brachiopods, bryozoans, nemertines, platy- helminths) have diverse larvae indicating a more complex history of multiple planktonic larval ori- gins (Rouse, 2000; Peterson, 2005). Other proto- stome clades, notably the ecdysozoans (which includes arthropods, nematodes, and others) are direct-developing. Finally, the basal acoels and other minor clades (not shown) are direct devel- opers. The mapping of the presence of planktonic larvae supports direct development as primitive in bilaterians, with separate origins of planktonic
larvae in the echinoderm + hemichordate clade and in the lophotrochozoans.


5.5 Evidence from gene expression patterns

One potentially strong discriminator for homolo- gous features is patterns of expression of develop- mental regulatory genes. This approach has had mixed success, because there has been extensive co-option of genes in evolution. There have been a small number of comparisons of gene expres- sion patterns of putatively homologous features of protostome trochophore larvae (annelids and molluscs) with deuterostome diplurula larvae (echinoderms + hemichordates) to test for pos- sible homologues at the level of gene deploy- ment (Arendt et al., 2001; Dunn et al., 2007). A few genes show similar expression patterns. Others do not. The collection of genes is small and the sampling incomplete. The case of nodal illustrates the uncertainties. Nodal is involved in left–right




Echinodermata

Hemichordata

Chordata

Annelida

Mollusca

Lophophorates

Platyhelminthes


Ecdysozoa Acoela Cnidaria

Figure 5.3 Developmental modes plotted on a metazoan phylogenetic tree. Open bars: direct development. Stippled box: ambiguous developmental mode. Filled boxes: planktotrophic indirect development. After Jenner (2000) and Peterson et al., (2005).

48 AN I M AL EV O L UTI O N



determination in echinoderms and vertebrates. However, it operates in a different domain (right side in echinoderms, left side in chordates), and interpretations of axial homologies are not yet pos- sible (Duboc and Lepage, 2006). Nodal appears to have no role in Drosophila, an ecdysozoan. It has been reported from lophotrochozoans (Grande and Patel, 2009).
The small sample of cross-phylum compari- sons of larval gene expression indicates homo- plasy in larval gene expression (Raff, 2008). That could arise from a case of homology between the trochophore and the dipleurula, but taken with the phylogenetic considerations it appears more likely to represent a convergence in evolution of larval features accompanied by convergence in gene regulation. Convergence is likely because the structure of larvae is simpler than the structure of adult bilaterians, and because co-option of genes may have been related to shared adult and lar- val functions. Thus, the patterns of expression of brachyury, Gsc, and Otx might represent co-option of gene expression in adult oral developmental into development of similar larval oral structures, a sort of serial homology. Fully defining phylogenies and comparative gene expression will be advanced by genomic data. Most genome sequencing has con- centrated on model or medically significant verte- brates, arthropods, and nematodes. A sea urchin genome has now been sequenced (Sodergren et al.,
2006), and the genomes of lophotrochozoans, espe- cially planktotrophic marine annelids and mol- luscs, are still needed.


5.6 Hunting for the larval revolution in the fossil record

We have good fossil time markers for the visible appearance of diverse complex bilaterians in the Cambrian fossil record, which starts 542 million years ago (Ma), and especially in the famous mid- Cambrian Chengjiang and Burgess Shale faunas (520–505 Ma). The origin of bilaterians lies in the late Precambrian: recent estimates suggest some- where between 580 and 600 Ma (Peterson et al.,
2005), although there is still a considerable range of uncertainty. An estimate of the timing for evolution of planktonic larvae of about 500 Ma is emerging,
which if correct puts the origin of these second body plans as much as 100 million years later than the divergence of the basal bilaterian benthic adult. Signor and Vermeij (1994) noted that the Cambrian fossil record showed relatively few benthic suspen- sion feeders or planktonic forms. They suggested that the evolution of planktonic feeding larvae took place in the late Cambrian to early Ordovician, driven by an expansion of plankton and sanctuary from predation—a point reinforced by Peterson (2005). The radiation of indirect-developing feeding larval in the late Cambrian was probably driven by a number of selective forces on larval traits as the Cambrian radiation produced a marine trophic organization similar to that of recent times (Dunne et al., 2008). Table 5.2 presents a number of evolu- tionary considerations affecting larvae, including ecological factors as well as effects of develop- mental and population features. These include egg size and provisioning (Allen and Pernet, 2007; McEdward, 2000; Moran, 2004), which dictate egg numbers and feeding or non-feeding larval forms. In addition, fully indirect development requires rapid metamorphosis and co-option of signal sys- tems (Hadfield, 2000). Finally, predation selects for a shorter planktonic larval life, but the length of planktonic life affects features from genetic dif- ferentiation within populations of a species to the distance that a species can disperse (Shulman and Bermingham, 1995).
The list in Table 5.2 is one of interacting char- acters. That is, if initial evolution of feeding lar- vae was driven by ecological conditions favouring



Table 5.2 Likely selective forces acting on evolution of planktonic larvae in Cambrian seas.

Trait Advantage

Larval feeding Lower investment in each egg
Lower investment in individual egg More eggs produced Higher egg numbers Increase number surviving Planktonic swimming Escape benthic predators Planktonic feeding Exploit new niche
Motility and time in water column Increase ‘dispersibility’ Character displacement vs adult Lower ecological competition Metamorphosis Rapid developmental shift in
body form

E V OL UTION OF L A R V A L ST A G ES 49



feeding on plankton, selection is likely to have initially favoured co-option of adult features and genes that introduced motility and feeding struc- tures into initial stages of larval development. Selection would then have favoured rapid develop- ment and metamorphosis to reduce vulnerability to predation. Other potentially advantageous traits such as dispersibility might conflict and in turn favour selection of the production of large numbers of small eggs to reduce the effects of predation. The rapid evolution of diverse modes of development among related living marine species shows that a variety of selective domains exist and continue to influence larval evolution (Raff and Byrne, 2006).
Direct fossil evidence for larval evolution comes from exquisite phosphoritic preservation of late Proterozoic cleavage stage embryos of unknown taxa, notably the embryos of the Doushantuo fauna (Xiao et al., 1998, Hagadorn et al., 2006). Early to mid Cambrian developmental series have been reported that include larval forms of cnidarians and small nemathelminth ecdysozoans (Bengtson and Zhao,
1997; Budd, 2004; Donoghue et al., 2006b; Maas et al.,
2007). An understanding of how embryos can be
preserved for mineralization is emerging (Briggs,
2003; Raff et al., 2006, 2008; Gosling et al., 2008).
The early fossil embryos so far described are large,
ranging from 350–1100 mm (Xiao and Knoll, 2000)
for late Precambrian embryos to 350–750 mm for
early to mid Cambrian embryos (Steiner et al., 2004;
Donoghue et al., 2006b). There are biases in the
record, notably low taxonomic diversity (Donoghue
et al., 2006b). The possibility that small embryos
typical of indirect-developing marine animals
(50–200 mm) exist has been checked by Donoghue
et al., (2006b), but does not appear to be the case.
Fossil embryo evidence for the time of appear-
ance of indirect developing forms is still scarce.
Nützel et al., (2006) have observed that Cambrian
larval mollusc shells are larger than those of the
Ordovician and Silurian, consistent with a shift
from direct to indirect development by the end of
the Cambrian.


5.7 Fossils, larvae, and Linnaeus

Linnaeus created a systematic approach that cre- ated a static hierarchical system of classification,
which has lent itself to evolutionary interpretation, and ultimately to modern phylogenetics. The fossil record has supplied crucial information for phy- logenetics and evo-devo (Raff, 2007). Larval and adult characters have produced homoplasies that yield some contradictory phylogenetic inferences among some of the deepest Linnean taxa. Thus, the trochophore larvae of annelids and molluscs carry a different phylogenetic signal from their adult body plan features. Rather than seeing these characters as conflicting, a better knowledge of the Cambrian fossil record of clades basal to living phyla allows us to dissect more finely the timing of evolution of both adult and larval body plans. Halwaxiids and their kin are sclerite-bearing mid- dle Cambrian animals that lie somewhere among basal forms in a clade that includes molluscs, anne- lids, and brachiopods (Conway Morris and Caron,
2007).
The characters of larval forms show some link-
ages between phyla obscured by changes in adult
morphology, and in fact agree with phylogenetic
inferences based on gene sequence data. Thus,
the trochophore shared by annelids and mol-
luscs belies segmentation and paired appendages
shared by annelids and arthropods, the so-called
Articulata. The existence of these forms suggests
that the primitive trochophoran larva may have its
origin in a Cambrian clade living before the split
of the lophotrochozoan phyla. This would move
the time of larval origin to earlier in the Cambrian.
This might suggest that the earliest planktotrophic
larvae have not yet been detected, or that the full
suite of planktonic feeding features were acquired
slowly, and included convergences among related
lineages (Rouse, 2000). Similarly, the dipleurula
larva links the pentameral echinoderms with
the bilaterian worm-like hemichordates, indicat-
ing that the origins of this larval form occurred
after the split of this clade from chordates. Basal
chordates and echinoderms are present in mid
Cambrian strata.


5.8 Gene co-option continues to occur in larval evolution

Larvae did not cease evolving in the Cambrian.
First, novel features evolved in planktonic larvae

50 AN I M AL EV O L UTI O N



after the initial evolution of larval body plans. This kind of evolution has been inferred by Rouse (2000) for downstream feeding in trochophore- like larvae by analysis of the distribution of fea- tures in a phylogeny of lophotrochozoan clades. Among deuterostomes, we have analysed the arms of the sea urchin pluteus larva (Figure 5.4a). This is an indirect-developing feeding planktonic larva
(a) (b)
ar


m
derived from the basal dipleurula-type larva of g r
echinoderms. The pluteus has, since the split of

sea urchins from other crown echinoderm classes about 450 Ma, evolved long arms that contain a novel rigid calcium carbonate skeleton and which bear the circumoral ciliary band (Bottjer et al.,
2006). These arms evolved somewhere between the late Ordovician and the Permian and thus followed the initial evolution of the dipleurula. The pluteus arm is a novel larval organ (Love et al., 2007). The arms consist of an ectoderm bearing a ciliary band and an underlying mesoderm consisting of skele- togenic mesenchyme cells. Expression of particular genes occurs in the tips of the growing arms (e.g. tetraspanin in ectoderm and advillin and carbonic anhydrase in mesenchyme). These genes also are expressed in various adult tissues. Their role in larval arms indicates that they have been recruited for expression in these structures following the ori- gin of the dipleurula. This recruitment serves as an accessible proxy for the more remote events of the Cambrian.
A second type of larval evolution is that of vari- ous non-planktotrophic derivatives of larvae in various clades, for example snails (Collin, 2004) and starfish and sea urchins (Raff and Byrne,
2006). In many taxa, planktonic feeding larvae have given rise to non-feeding, direct-developing planktonic or brooded larvae, and even vivipar- ous larvae. These modified larvae rapidly evolve distinct morphologies, as seen in the larvae of the congeneric sea urchins Heliocidaris tuberculata and Heliocidaris erythrogramma (Figure 5.4), which diverged about 4 Ma (Zigler et al., 2003). Heliocidaris tuberculata takes about 6 weeks of feeding in the water column to reach metamorphosis. Heliocidaris erythrogramma takes 3 days, and does not feed. The H. erythrogramma egg is 100 times the volume of that of indirect-developing sea urchins and
Figure 5.4 Rapid evolution of larvae shown by two congeneric sea urchins, diverged for 4 million years. (a) Planktotrophic pluteus larva of the indirect developer Heliocidaris tuberculata. The notable features are the arms (ar), each supported by a skeletal rod, and bearing a ciliary band; the large gut (g); the mouth (m); and the developing adult rudiment (r) that will grow to become the juvenile sea urchin released at metamorphosis (about 6 weeks’
post-fertilization). (b) Non-feeding direct-developing larva of Heliocidaris erythrogramma. All internal features are those of the developing adult. Metamorphosis is 3–4 days’ post-fertilization. Scale bar in both parts = 100 µm.



supports development through post-metamorphic development of the adult mouth.
At first glance it would appear that H. erythro- gramma is simplified by the loss of larval features but retains adult ontogeny. Some feeding struc- tures such as the larval arms and gut are lost, but developmental features retain a high degree of complexity, and dramatic novel features have appeared. These include changes in oogenesis and spermatogenesis, in maternal embryonic axis determination, in cleavage pattern, in embryonic cell lineages, and in heterochronies in larval gene expression and morphogenetic events (Raff and Byrne, 2006). Rapid and profound evolutionary changes in larval development occur frequently, with for example several clades of sea urchins hav- ing independently evolved larvae similar to that of H. erythrogramma (Sly et al., 2003). The evolutionary lability of larvae suggests that evolution of primary larval features would have been rapid in the face of selection under the new ecological regime of the late Cambrian and early Ordovician. It is also likely that the developmental regulatory features of living larval clades give us strong clues to those of early larval forms.

E V OL UTION OF L A R V A L ST A G ES 51



5.9 Developmental innovations and the metazoan radiation

The origin of the ancestral benthic bilaterian body plan was an immense evolutionary developmental innovation that produced a shift from the cnidar- ian frond-dominated world of the late Proterozoic to the diversified bilaterian-dominated world of the Cambrian. However, evolution of novel devel- opmental features depends both on the appear- ance of variation in development and on selection acting on developmental stages and processes. Developmental features of early metazoans may have been less constrained by a looseness of eco- logical fit, resulting in more experimentation with body plans, i.e. adaptive peaks were present, but in a fairly flat landscape where few deep valleys of low fitness were yet found. The rapid diversi- fication of basal taxa related to living phyla was probably the result of ecological pressures and opportunities that selected for the development of novel morphologies among bilaterians of relatively simple morphology. Acoelomorph bilaterian ances- tors would have possessed a large suite of genes regulating development that could be recruited for the evolution of new structures. The possibilities for body plan innovation in acoelomorph-grade
animals would, in many respects, have been easier than for proposed schemes that suggest diver- gence from more derived ancestors. Thus, the dorsal–ventral inversion of organs of protostomes and deuterostome would have been of little conse- quence at the acoelomorph grade of organization, but could have become a fixed element of body plan later. Segmentation, another feature of importance, may also be a product of convergence in emerging lineages (Seaver, 2003).
The evolution of planktonic larvae followed the origins of basal bilaterian phyla by about 100 million years. Again, it less likely that develop- mental novelties per se drove this evolutionary innovation. Instead, larvae bearing features aris- ing from the novel expression of genes used in adults were selected as agents of exploitation of greater ranges of ecological possibility, such as increasing planktonic food resources, escape from benthic filter-feeding predators, and a vastly improved dispersal than that offered by large direct-developing embryos. The evolutionary flexibility of larval development allowed diverse and rapid responses to selection. Selection on expression of existing genes in new contexts may underlie much of the evolution of novelties in development.