Biol. Bull. 216: 216-225. (June 2009)
© 2009 Marine Biological Laboratory
Molluscan Larvae: Pelagic Juveniles or Slowly Metamorphosing Larvae?
Louise R. Page
Department of Biology, University of Victoria, P.O. Box 3020 STN CSC, Victoria, British Columbia V8W 3N5, Canada
E-mail: lpage{at}uvic.ca
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Abstract
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Asking the right questions about evolution of development, larval morphology, and life history requires knowledge of ancestral state. Two hypotheses dominate current opinion about the ancestral life cycle of bilaterians: the "larva-first" and the "intercalation" hypotheses. Until recently, the larva-first hypothesis was preeminent. This proposes that the original indirect life cycle of bilaterians included a planktotrophic larva followed by a benthic adult. Phylogenetic evidence suggests that a planktotrophic larva is plesiomorphic for echinoderms. A preponderance of developmental studies on echinoderms may have fostered a tendency to extrapolate conclusions about echinoderm development to other clades, particularly the concept that larval and juvenile/adult bodies are mostly separate entities. However, some of the recent reconstructions of bilaterian phylogeny suggest that nonfeeding larvae may have been ancestral for bilaterians, and these may have been intercalated into a life cycle that was originally direct. I review comparative data on molluscan development that suggests the trochophore-like stage is little more than a gastrula with transient structures (prototroch and apical sensory organ) to allow a temporary planktonic phase during development. Most lineage founder cells of molluscan embryos generate progeny that develop through the veliger stage into structures of the juvenile, which becomes benthic when the prototroch and apical sensory organ are lost. In light of this, the model of separate larval and juvenile bodies with the latter developing from nests of multipotent cells within the larva is inappropriate for molluscs. The intercalation hypothesis may be a better model for interpreting development of molluscs and other lophotrochozoans.
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Introduction
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Metazoans originated within the ocean during the distant past, and the ocean remains the cauldron of greatest diversity for most metazoan phyla. Many marine animals within at least 15 phyla begin free-living life as delicate planktonic larvae that eventually settle onto the benthos, transform into juveniles, and become sexual adults (Thorson, 1950; Strathmann, 1993; Young, 2002). Amazingly, larvae from phyla that diverged during or even before the Cambrian may have similar morphological features, presumably resulting from either convergence or common ancestry (Strathmann, 1978, 1993; Nielsen, 1985; Strathmann and Eernisse, 1994; Wray, 1995, 2000; Henry and Martindale, 1999; Peterson, 2005). If the latter is true, then planktonic larvae existed before extremely ancient events of cladogenesis, and a great deal of metazoan evolution has occurred within the context of an indirect, pelago-benthic life cycle.
Thorson's (1950) pioneering speculation about the ecological causes and consequences of different life-history patterns among marine invertebrates led him to delineate three main types: (1) those with planktonic larvae that feed, (2) those with planktonic larvae that do not feed, and (3) those without a planktonic larval stage (direct development). Excellent reviews have discussed these three developmental types in terms of environmental selection, ecological factors, and life-history trade-offs (Strathmann, 1978, 1985, 2007; Moran, 1994; Havenhand, 1995; Levin and Bridges, 1995; Pechenik, 1999; Levitan, 2000). Nevertheless, writing from the standpoint of a morphologist reviewing developmental diversity among opisthobranch gastropods, Bonar (1978) saw a problem with the category of "direct development" because it lumped together patterns of morphogenesis that were markedly different. Subsequently, McEdward and Janies (1993, 1997) extended Bonar's effort to incorporate morphogenesis into Thorson's tripartite classification and its emphasis on ecologically relevant criteria. Their scheme, initially inspired by echinoderms but later extended to all marine invertebrates (McEdward, 2000), sought to better reflect the multidimensional aspect of evolutionary transitions in life histories.
Widespread renewal of interest in the relationship between development and evolution in recent years has fostered a dramatic increase in studies on evolutionary transitions in morphogenesis among marine invertebrates. Topics have included diversification of larval morphology, transitions between feeding and nonfeeding larvae, larval versus juvenile/adult morphogenetic programs, and gene expression profiles associated with all of these. A great deal of this research has involved echinoderms, a group for which robust phylogenetic evidence indicates that an indirect life cycle with a feeding larva is plesiomorphic (Smith, 1997). The paradigm that organizes much theory, research, and interpretation of data regarding developmental evolution among echinoderms is one that distinguishes separate larval and adult body plans, separate genetic control programs for each, and relatively little integration between larval and adult developmental programs (e.g., Raff, 1987; Wray, 1995, 2000; Davidson et al., 1995, 1998; Lowe and Wray, 1997; Raff and Sly, 2000; Arenas-Mena et al., 2000; Raff and Byrne, 2006; Smith et al., 2007).
In this essay I address two questions that are particularly relevant to lophotrochozoans, but I focus most of my discussion on molluscs. First, do molluscs have a larval body that is qualitatively distinct from the juvenile body? Second, what was the original molluscan life history? Did an initial planktonic organism precede the addition of a morphologically different juvenile/adult stage during evolution or was a larva intercalated into the development of the juvenile/adult body? Answers to these questions are critically important for interpretations of developmental regulatory systems and for understanding mechanisms that have generated diversity in larval and adult morphology. We need to know if extant molluscan larvae have resulted from shunting of juvenile traits onto an ancestral larval form that had a body plan unique to the larval stage, or if molluscan larvae are better interpreted as differentiating juveniles that secondarily acquired traits facilitating a planktonic or even a planktotrophic lifestyle.
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Bilaterian Larvae—Hypotheses About Evolutionary Origin
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The subject of possible links between the origin of the pelago-benthic life cycle and the origin of major metazoan lineages has a long history of debate (see Willmer, 1990). However, the discovery of highly conserved developmental control genes among metazoans, new fossil finds, and revolutionary new hypotheses about metazoan relationships have breathed new life into speculation about the original body plan of bilaterians and the pelago-benthic life cycle (Knoll and Carroll, 1999; Irwin and Davidson, 2002). Recent essays have analyzed strengths and weaknesses of what currently stand as the two major hypotheses about the evolutionary emergence of this biphasic life cycle (Haszprunar et al., 1995; Wray, 1995, 2000; Wolpert, 1999; Nielsen, 2000; Valentine and Collins, 2000; Sly et al., 2003; Peterson et al., 2005; Degnan and Degnan, 2006). These two proposals, which are outlined in Figure 1, can be called the "larva-first hypothesis" and the "intercalation hypothesis."
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Figure 1. Illustration of three evolutionary stages (A–C) for the larva-first and intercalation hypotheses for the origin of indirect life cycles among bilaterians. Under the larval-first hypothesis, stage A consists of holoplanktonic feeding adults (the trochaea hypothesis posits that the protostome and deuterostome lineages diverged at this stage); stage B has added a terminal, benthic adult stage, and the original planktonic stage persists as a sexually immature larva that feeds; stage C is a transition of the planktonic larvae from feeding to nonfeeding. Under the intercalation hypothesis, stage A consists of holobenthic adults; stage B has added a planktonic larval stage to early development; stage C is a transition of the planktonic larva from nonfeeding to feeding.
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The larva-first hypothesis has been extensively developed by Nielsen as the "trochaea theory" (Nielsen and Nørrvang, 1985; Nielsen, 1985, 1995). Building on earlier proposals by Haeckel (1874), Hatschek (1878), and Jägersten (1972), the trochaea theory proposes that pre-bilaterian metazoans were small holoplanktonic creatures that swam and captured suspended food particles by using a single ciliary band. This stem form gave rise to trochophore and dipleurula (= tornaria) lineages, which each subsequently added a benthic stage to the life cycle. Sexual maturation was shunted to the terminal benthic stage, but the swimming, feeding trochophore and dipleurula were retained as the larval form of protostomes and deuterostomes, respectively. According to the trochaea theory, the split between protostomes and deuterostomes occurred before their respective benthic stages were added, so adults of protostomes and deuterostomes do not have a common ancestor that was a sexually mature, benthic animal.
Davidson and coworkers (Davidson et al., 1995, 1998; Peterson et al., 1997; Cameron et al., 1998) endorsed a larva-first scenario because of how they interpreted differences in cell-fate specification for larval and juvenile/adult bodies of sea urchins. The larval body is built by embryonic cells having limited division capacity, and differentiation is specified by signals between individual cells. Davidson and co-workers suggested that the first metazoans built their bodies using this mechanism ("type I embryogenesis") and that they were small, planktonic organisms like modern invertebrate larvae. By contrast, the juvenile/adult body of sea urchins arises from nests of multipotent "set-aside cells" within the larval body. These set-aside cells have much greater mitotic potential, and morphogenesis is patterned by transcription factors such as the Hox gene complex acting on spatial domains of cells (Arenas-Mena et al., 2000). This "type II embryogenesis" was interpreted as an innovation that facilitated evolution of larger bodies for a newly created benthic stage.
The second proposal for the origin of the pelago-benthic life cycle, the intercalation hypothesis, reconstructs the first bilaterians as holobenthic organisms. These ancestral bilaterians secondarily acquired a planktonic larva when a stage of early development sprouted cilia and became temporarily pelagic before returning to the benthos (Sly et al., 2003). The intercalation hypothesis predicts that planktotrophy is a derived larval condition for bilaterians and probably evolved multiple times. Several authors have suggested that the intercalation hypothesis, specifically its prediction that planktotrophic larvae are derived, is supported by mapping of life-history data onto molecular phylogenetic hypotheses for bilaterian relationships (Jenner, 2000; Sly et al., 2003; Peterson, 2005; Peterson et al., 2005). However, less support is given by a recent phylogenetic reconstruction based on a large number of expressed sequence tags from a wide sample of metazoans (Dunn et al., 2008). Nevertheless, the intercalation hypothesis does accommodate a shared ancestor for bilaterians that was itself a benthic adult bilaterian. Therefore, specification of differentiation fate along the anterior-posterior axis by Hox genes need not have evolved independently in Protostomia and Deuterostomia, as required under Nielsen's rendition of the larval-first hypothesis.
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Defining a Larva: Transient Larval Traits or Distinct Larval Body Plan?
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Wrangling with definitions is not a trivial exercise. Definitions frame how we conceptualize problems and therefore what sorts of research questions are asked and how results are interpreted. Definitions of biological entities and concepts are very much influenced by the historical development of ideas and by intensively studied model systems.
McEdward and Janies (1993), among others, discussed the challenge of formulating a globally applicable definition of the term "larva." They ultimately defined a larva as an intermediate stage during ontogeny that is characterized by transitory structural features (see also Strathmann, 1993; Hadfield et al., 2001), with the caveat that "the transitory structures are not developmentally necessary for morphogenesis of the juvenile." Loss of the transitory structures marks the end of the larval phase, an event known as metamorphosis (McEdward and Janies, 1993; Strathmann, 1993) (for additional views on metamorphosis see Bishop et al., 2006). This definition of a larva provides a suitable platform for framing questions about evolution of morphogenesis because the defining criteria are primarily morphological rather than genetic, behavioural, functional, or ecological.
If a larva is an ontogenetic stage during the process of building a sexually mature, multicellular organism and this larval stage is distinguished by transitory structures, then what exactly is a "larval body" or "larval body plan"? The term "larval body" may imply something much more than a stage of development with transitory structures, particularly when it is contrasted with a "juvenile body" or "adult body." A potential implication is that most if not all structural components of the larval stage of ontogeny are transitory and ultimately replaced by structures of the juvenile/adult body. It has often been the case that structures or organ systems are called larval merely because they co-exist with transitory larval traits, even though the structures persist after loss of the larval traits. This application of the adjective "larval" may create ambiguity and confusion when considering the evolution of morphogenesis. The globally applied concept of a larval body that is qualitatively distinct from the body of other life-history stages and is largely replaced by body components of a subsequent stage can be traced to two factors: (1) the historical precedence of the larva-first hypothesis for the evolution of the pelago-benthic life cycle, and (2) numerical dominance of studies on echinoderm development.
The larva-first hypothesis as interpreted by Nielsen (1985, 1995) requires that the larval stage be an entire body plan with a full kit of structures for swimming, feeding, digestion, and waste elimination, because this organism preceded the juvenile/adult stage during evolution (Fig. 1). Under this hypothesis, appearance of juvenile structures within a larval stage is said to be secondarily evolved (Jägersten, 1972; Nielsen, 1985), and yet the rules for recognizing which structures were originally larval and which were originally juvenile are not always clearly defined.
Development of echinoderms has received more research attention than development of lophotrochozoan phyla, possibly because echinoderms are highly amenable organisms for this type of research. The echinoderm bias and a tendency to extrapolate features of echinoderm development to other organisms may have obscured some important differences. The statement: "Most phyla have a second body plan" (Raff, 2008, p. 1473), meaning that the larval and juvenile/adult stages represent two different body plans during a single life history, should be critically assessed when applied to lophotrochozoans such as annelids and molluscs. I suggest that the concept of a larva as an entity with a unique body plan, rather than simply a developmental stage with transitory larval traits, may confound interpretations of developmental evolution among molluscs and possibly other lophotrochozoans.
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Asking the Right Questions About Larval Evolution
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Knowing the polarity of change for life-history evolution among marine invertebrates is essential for asking the right questions about the evolution of development. For example, Lacalli's (1984, p. 123) observations on neurogenesis in the polychaete Spirobranchus sp. led to the suggestion that neurites within the neuropil of the apical sensory organ of this species may play a pathfinding role for neurites of the cerebral commissure of the developing juvenile/adult nervous system. A follow-up study on this proposal would be appropriate if the larva-first hypothesis was correct. However, under the intercalation hypothesis a more appropriate question might ask how elements of the juvenile/adult nervous system have been co-opted or embellished to serve as innervators of novel swimming effectors for a planktonic larva. Similarly, conclusions about direction of heterochronic shifts relative to metamorphosis may be profoundly mistaken, depending on whether the larval stage or the juvenile/adult stage was the novelty within a pelago-benthic life cycle. If the original developmental pattern was direct rather than indirect, then the many examples of what Jägersten (1972) interpreted as temporal shifting of adult structures to the larval stage (a type of heterochrony that he called "adultation"), might simply be direct development unfolding in an organism that secondarily acquired swimming and possibly feeding devices during a short period of its early life history. Under the intercalation hypothesis, these swimming and feeding effectors are transient traits that have been superimposed on a developing juvenile/adult body to facilitate a temporary planktonic lifestyle.
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Defining a Trochophora
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Larvae of deuterostomes and lophotrochozoans are often represented as archetypes, the dipleurula and trochophora, respectively, which have features that are hypothetically ancestral for the larval forms of these two groups. Other hypotheses have also been suggested (e.g., Salvini-Plawen, 1980; Ivanova-Kazas, 1985). Historical overviews by Rouse (1999) and Nielsen (2004) identify Hatschek (1878) as the first to propose that a type of feeding trochophore found among extant polychaete annelids typified features of the ancestral larval form for annelids, molluscs, sipunculans, and echiurans. According to Nielsen (1995), the ancestral, feeding trochophore is defined by six characters: prototroch (pre-oral ciliary band), metatroch (post-oral ciliary band), ciliated food groove between the prototroch and metatroch, apical sensory organ, functional gut, and pair of protonephridia. The prototroch and metatroch together form an opposed-band feeding mechanism for capture of small, suspended food particles, and the ciliated food groove carries these particles to the mouth.
Other authors have noted that larvae of polychaete annelids display a diversity of feeding mechanisms, not all involving a metatroch (Strathmann, 1978; Ivanova-Kazas, 1985). A survey by Rouse (1999, 2000) indicated that only five polychaete families include species with a larval metatroch for opposed-band feeding, although Pernet (2003) added sabellarids to this list and gave evidence that sabellid larvae arose from a form with opposed-band feeding. By individually mapping traits that defined Nielsen's ancestral trochophore type on a phylogenetic hypothesis for polychaete families, Rouse (1999, 2000) concluded that only the prototroch, the apical sensory organ, and a pair of protonephridia are plesiomorphic characters for annelid larvae. He further suggested that the original function of the prototroch was exclusively for locomotion, but it has been incorporated multiple times into a mechanism for food capture (with or without involvement of a metatroch).
A girdle of multiciliated cells (the prototroch), an apical cluster of sensory neurons, and a pair of protonephridia conform to McEdward and Janies’ (1993) definition of larval structures because they exist transiently during post-embryonic development. However, these three components do not constitute a whole body plan. Much of the remainder of polychaete trochophores, including epidermal epithelium of the hyposphere, the generative zone for metameres, the gut (whether functional in the trochophore or not), derivatives of the mesoderm, and ingressing neurons of the cerebral ganglia, continue to develop during larval, metamorphic, and juvenile development as components of the definitive adult body (e.g., Seaver et al., 2005; Kulakova et al., 2007).
In a description of development beyond the trochophore stage of polychaete annelids, Jägersten (1972, p. 167) noted that "the organization of the growing larva gradually changes to become more like that of the adult." Antennae, palps, and initial metameres bearing parapodia often differentiate prior to metamorphic loss of the prototroch. He attributed this to a shifting of adult characters into the larval stage ("adultation"). Similarly, Nielsen (2004, p. 47) stated: "polychaete metamorphosis is usually a gradual process because a few to many segments, which must be considered adult structures, develop in the planktonic stage in most species." An alternative interpretation should also be considered: the polychaete gastrula basically embarks on development towards a juvenile, but the early stages of this process co-exist with transient structures to allow a temporary pelagic life and possibly the ability to capture food.
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Molluscan Larvae—Acceleration of Juvenile Traits vs. Intercalation of Larval Traits
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Proponents of the larva-first hypothesis have interpreted laval feeding as the plesiomorphic condition among molluscs and many other invertebrate phyla (Jägersten, 1972; Nielsen and Nørrvang, 1985). Alternatively, Haszprunar et al. (1995) argued that larval planktotrophy is derived among molluscs because, according to some morphology-based phylogenies, the most basal clades of molluscs have nonfeeding larvae (Salvini Plawen, 1985; Salvini Plawen and Steiner, 1996; Haszprunar, 2000) as do basal clades of both gastropods and bivalves (Ponder and Lindberg, 1997; Waller, 1998). Nevertheless, relationships within the Mollusca are far from certain and more recent molecular phylogenies have not yet corroborated earlier conclusions about the most basal clades, nor have they resolved either the bivalves or gastropods as monophyletic (Winnepenninckx et al., 1996; Passamaneck et al., 2004; Giribet et al., 2006).
In theory, a resolved phylogeny should be helpful for recognizing the ancestral or derived status of feeding larvae within the Mollusca, but several authors have pointed out that rates of character evolution for larvae and adults may not be tightly linked (Strathmann, 1993; Strathmann and Eernisse, 1994; Wray, 1996). Fortunately, to answer the question of whether the larval body of molluscs is qualitatively different from the juvenile/adult body, it may not be necessary to know if feeding forms are ancestral or derived. Instead, observations on the fate of cells and tissues during embryogenesis, larval development, and metamorphosis among molluscan groups may be more revealing than a resolved phylogeny.
Molluscs, like most other lophotrochozoans, exhibit a highly conserved pattern of spiral cleavage that generates four macromeres surmounted by four tiers of micromere quartets. Gastrulation occurs when the embryo consists of only 70–200 cells, at least among gastropods (Verdonk and Van den Biggelaar, 1983). Subsequent development among non-cephalopod molluscs proceeds along one of two pathways. The first involves a trochophore-like stage followed by a veliger stage (Fig. 2A, B). This group includes the scaphopods, gastropods, polyplacophorans, chaetodermomorphs (= caudofoveates), and non-protobranch bivalves. Detailed cell lineage information based on microinjection of intracellular dyes is available for several gastropods (Render, 1991, 1997; Dictus and Damen, 1997; Hejnol et al., 2007) and a chiton (Henry et al., 2004). The second pathway involves a pericalymma larva (= test-cell larva) and is found among protobranch bivalves and neomeniomorphs (= solenogastres) (Fig. 2C, D). Development of the extremely yolk-rich eggs of cephalopods has been highly modified to the extent that even spiral cleavage has been lost (Arnold, 1965).
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Figure 2. Sketches of representative trochophore, veliger, and pericalymma (=test cell) larvae of molluscs. (A) Lateral views of the trochophore-like and late veliger stages of the chiton (polyplacophoran) Katharina tunicata. (B) Lateral views of the trochophore-like and late veliger stages of the gastropod Tectura (Lottia) scutum. (C) Ventral views of the pericalymma larva and a metamorphic stage of the neomineomorph Epimenia babai (redrawn from Okusu, 2002). (D) Lateral view of the pericalymma larva of the protobranch bivalve Acila castrensis; dashed line indicates the internal juvenile shell valves (redrawn from fig. 17 of J. D. Zardus and M. P. Morse. 1998. Embryogenesis, morphology and ultrastructure of the pericalymma larva of Acila castrensis (Bivalvia: Protobrnachia: Nuculoida). Invertebrate Biology. 117: 221–244. Copyright ©1998, American Microscopical Society. Reproduced with permission of Blackwell Publishing Ltd.). Sketches are not drawn to the same scale.
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The trochophore-like stage of molluscs arises soon after gastrulation (Verdonk and Van den Biggelaar, 1983; Van den Biggelaar et al., 1997), when a prototroch consisting of 1 to 6 rows of pre-oral, multiciliated cells differentiates. At least among gastropods and chitons, the prototroch is formed from the same group of lineage founder cells (the trochoblasts) that generate the prototroch of polychaete larvae (reviewed by Nielsen, 2004; Henry et al., 2007). In addition, an apical sensory organ, often associated with a tuft of long cilia, arises from cells generated from the 1st micromere tier, and additional cells anterior to the mouth may bear short cilia. In some cases the trochophore-like stage is free-living, but there are no confirmed cases of feeding by the trochophore-like larvae of molluscs (Hadfield et al., 1997).
The trochophore-like stage progresses to the veliger stage when the foot and shell begin to form, and the prototroch may become elaborated into two or more lobes extending from the head area (velar lobes). Feeding veligers acquire a metatroch and food groove, which in Crepidula fornicata originate from progeny of a group of 2nd tier micromeres (Hejnol et al., 2007). The prototroch, metatroch, and food groove are lost at metamorphosis (see Fretter, 1969), and loss of the apical sensory organ has been reported in those species where this has been examined (Marois and Carew, 1997; Page, 2002; Gifondorwa and Leise, 2006). The prototroch, metatroch, food groove, and apical sensory organ all arise from subclones of the 1st and 2nd micromeres.
Clonal contribution maps for molluscs (Render, 1991, 1997; Dictus and Damen, 1997; Henry et al., 2004; Hejnol et al., 2007; earlier studies reviewed by Verdonk and Van den Biggelaar, 1983) have shown that most progeny of the remaining lineage founder cells generate the entire body of the veliger that will not be destroyed at metamorphosis. In other words—the body of the juvenile. This includes the entire gut, epidermal epithelium of the foot and shell-secreting mantle, neural and non-neural derivatives of mantle epithelium, the renopericardial complex, and muscle systems derived from both ecto- and endomesoderm. The cerebral ganglia, eyes (except in chitons), and cephalic tentacles arise from pre-trochal epithelium. As Dictus and Damen (1997, p. 214) stated in their paper on embryonic cell lineage of Patella vulgata: "The region anterior to the prototroch, the so-called pretrochal area, gives rise to the head" and "the region posterior to the prototroch, the so-called postrochal area, gives rise to the rest of the adult body" (italics added).
The prototroch, metatroch, and apical sensory organ are not the only transient larval structures among molluscs. Gastropods, for example, also generate protonephridia, a larval heart, and a group of shell-anchored muscles that do not typically survive through metamorphosis. These structures might be relics of an ancient larval body that was distinct from the juvenile body, or they might be caenogenetic structures of the larval stage. For example, among gastropods, the velar lobes are a major insertion site for muscles that are lost during metamorphosis (Page, 1997, 1998).
Data on molluscan embryogenesis and cell lineage suggest that the trochophore-like stage of molluscs is little more than a ciliated gastrula when it first forms and the juvenile body differentiates from this as development progresses through the veliger stage. This conclusion is strengthened by the observation that veligers within each molluscan class are more similar to their respective juvenile stage than to veligers of other molluscan classes, largely because the basic forms of the foot and biomineralized exoskeleton (shell or epidermal spicules) are similar in the veliger and juvenile life-history stages (see Fretter, 1967; Moore, 1983; Wanninger and Haszprunar, 2001, 2002; Okusu, 2002; Nielsen et al., 2007; Lesoway and Page, 2008). This is a general statement, and certainly there may be changes in shell and foot following metamorphosis. Ontogenetic changes in the gastropod shell are a good example.
The second molluscan larval type is the nonfeeding pericalymma or test-cell larva found in Neomeniomorpha (Solenogastres) and protobranch bivalves. In this instance, the external surface of the post-gastrula is formed by a layer of large cells that fully or partially surrounds the remainder of the developing body (Fig. 2D). Multiciliated cells of this test may be uniformly distributed or organized into several bands (Gustafson and Reid, 1988; Gustafson and Lutz, 1992; Zardus and Morse, 1998). Results of an important study on the neomeniomorph Epimenia babai (Okusu, 2002), when compared to observations on species with a more typical test-cell larva, corroborate an early interpretation of the test as an expanded pretrochal area and prototroch of a trochophore-like form, with the juvenile body developing from more vegetal (posterior) blastomeres of the embryo. In cases where the test completely covers the developing juvenile body, the juvenile eventually ruptures out of this encasement and discards or ingests the test cells that facilitated a temporary planktonic life.
For echinoderms, evolutionary loss of a feeding larva from the life history is accompanied by drastic remodeling of early development (Wray and Raff, 1990; Raff, 1992). This is consistent with the notion that larvae and juveniles/adults of echinoderms represent almost entirely separate bodies with distinctive embryological derivations. Among molluscs however, cell lineage studies on gastropods with different life-history patterns show remarkably little change in fates of cell clones arising from lineage founder cells (Dictus and Damon, 1997; Render 1991, 1997; Hejnol et al., 2007). Embryological differences do exist within the Gastropoda, including differences in relative timing of cleavages (Van den Biggelaar and Haszprunar, 1996; Guralnick and Lindberg, 2001), novel asymmetric cleavages (Henry and Martindale, 1999), and differences in mechanisms of dorsal quadrant specification (Freeman and Lundelius, 1992). These differences often correlate with phylogenetic groupings, but correlation with presence or absence of a larval stage is not strong. For example, the mesentoblast of both pulmonates without a larval stage and opisthobranchs with a feeding larva arises when the embryo consists of 24 cells (Van den Biggelaar and Haszprunar, 1996). The reason for conservation of embryological features despite life-history differences among gastropods may relate to the fact that transient larval structures originate from only a small group of lineage founder cells. The remainder of the gastrula gives rise to the juvenile body, which may or may not spend a transient period as a planktonic veliger.
Davidson et al. (1995) proposed that recruitment of Hox genes to pattern regional specification along the anterior-posterior axis was an innovation that accompanied evolution of bilaterians. In echinoderms these genes are expressed in a collinear pattern within tissues of the future juvenile/adult, but not in larval tissues (Arenas-Mena et al., 2000). If larvae of extant molluscs represent a body plan that is qualitatively different from that of the juvenile body because it predates the bilaterally symmetric benthic stage, then collinear expression of Hox genes should not occur during early stages of molluscan larval development. However, Hinman et al. (2003) found that orthologs of five anterior Hox genes are expressed in a collinear pattern within ganglia of the developing nervous system during larval development of the gastropod Haliotis asinina. Larvae of H. asinina do not feed, so it will be important to examine patterns of Hox gene expression in gastropods with a planktotrophic larva.
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Molluscan Metamorphosis
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The metamorphosis that irreversibly commits a planktonic molluscan larva to life on or in the benthos is often an unspectacular event dominated by simple loss of transient larval structures. As noted by Hadfield (2000) and Hadfield et al. (2001), absence of a catastrophic metamorphosis for most molluscan larvae is due to pre-metamorphic differentiation of essential juvenile structures. However, appearance of juvenile structures prior to the plankton-to-benthos transition is interpreted very differently under the "larva first" and "intercalation" hypotheses. The larva-first hypothesis invokes heterochrony; components of what was originally the "juvenile compartment" of the life history have been shunted to the larval stage. Alternatively, the intercalation hypothesis suggests that the plankton-to-benthos transition requires little body remodeling because, from the outset, development has built a juvenile body along with transient larval structures to allow swimming and, in some cases, feeding.
Hadfield (2000) and Hadfield et al. (2001) have suggested that metamorphic competence is an adaptive response that has evolved convergently in many marine invertebrates in response to selection for minimizing the vulnerable period of metamorphic transition. Their definition of metamorphic competence is "the developmental capacity to undergo complete metamorphosis when triggered by internal or external factors" (Hadfield et al., 2001, p. 1123). Certainly the need for an external cue to trigger irreversible conversion to the benthic stage (loss of transient larval traits) could be interpreted as an adaptation with obvious survival value. However, the capacity to undergo rapid and complete metamorphosis, what Hadfield (2000) called the "need for speed hypothesis," was explained by shunting of juvenile traits into the larval stage. If the larval body of molluscs is essentially a developing juvenile with additional transient traits to allow a temporary planktonic habitat, then the speed of the transformation from larval to juvenile body is primarily a consequence of ancestry rather than adaptation. In essence, if development from egg to juvenile was the ancestral pattern, then the gradual morphogenesis of the juvenile body during development is not a phenomenon requiring an adaptive explanation. If transitory structures that allow an initial pelagic lifestyle have been superimposed on this basically direct developmental pattern, then it is only the loss of these transitory structures that needs to be "speedy."
Among adult molluscs, the gastropods have undergone the greatest amount of diversification. Extensive evolutionary change to adult morphology has often required a more drastic metamorphosis. Nudibranch gastropods are the classic example. Larval nudibranchs have a shell, shell-anchored retractor muscle, operculum, and style sac that are all lost during metamorphosis (see Bonar, 1978). The presence of larval planktotrophy may have little impact on metamorphosis if the adult stage is a herbivorous grazer or suspension feeder, because the complex stomach morphology within these types of adults is basically the same as the stomach morphology of planktotrophic molluscan larvae (Fretter and Montgomery, 1968). More drastic revisions to larval and metamorphic morphogenesis have accompanied the evolution of predatory feeding habits among gastropods with planktotrophic larvae (see Fretter, 1969; Page, 2005).
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Conclusion
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Davidson et al. (1995) underlined the independence of larval and juvenile bodies in sea urchins with an image of an aberrant larva that appeared fully normal, except that the juvenile rudiment had failed to form. This larva was capable of feeding and swimming and was clearly identifiable as a pluteus with larval epidermis, larval arms with ciliary tract, and digestive tract. In contrast to the situation in echinoderms, it would be impossible to generate a recognizable molluscan veliger that lacked all prospective juvenile components. A pericalymma would be superficially normal-looking but completely hollow—nothing but a shell of ciliated cells. Unlike echinoderms, molluscs do not have a larval body separate from the juvenile/adult body; molluscan larvae have only transient larval traits. Heterochrony is not needed to explain the appearance of juvenile structures prior to loss of the transient larval structures. Larvae gradually acquire the appearance of juveniles for each respective class not because juvenile traits have been accelerated, but rather because most cells of the gastrula differentiate directly toward the juvenile/adult body plan that is characteristic of each molluscan class.
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Acknowledgments
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I gratefully acknowledge research funding from NSERC of Canada.
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Footnotes
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Received 12 November 2008; accepted 17 February 2009.
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Abstract
Introduction
