Integrative and Comparative Biology Advance Access originally published online on August 15, 2006
Integrative and Comparative Biology 2006 46(6):683-690; doi:10.1093/icb/icl028
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The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it?
School of Integrative Biology, The University of Queensland Brisbane, Queensland 4072, Australia
Correspondence: 1E-mail: s.degnan{at}uq.edu.au
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 Synopsis IntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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The biphasic (pelagobenthic) life cycle is found throughout the animal kingdom, and includes gametogenesis, embryogenesis, and metamorphosis. From a tangled web of hypotheses on the origin and evolution of the metazoan pelagobenthic life cycle, current opinion appears to favor a simple, larval-like holopelagic ancestor that independently settled multiple times to incorporate a benthic phase into the life cycle. This hypothesis derives originally from Haeckel's (1874) Gastraea theory of ontogeny recapitulating phylogeny, in which the gastrula is viewed as the recapitulation of a gastraean ancestor that evolved via selection on a simple, planktonic hollow ball of cells to develop the capacity to feed. Here, we propose an equally plausible hypothesis that the origin of the metazoan pelagobenthic life cycle was a direct consequence of sexual reproduction in a likely holobenthic ancestor. In doing so, we take into account new insights from poriferan development and from molecular phylogenies. In this scenario, the gastrula does not represent a recapitulation, but simply an embryological stage that is an outcome of sexual reproduction. The embryo can itself be considered as the precursor to a biphasic lifestyle, with the embryo representing one phase and the adult another phase. This hypothesis is more parsimonious because it precludes the need for multiple, independent origins of the benthic form. It is then reasonable to consider that multilayered, ciliated embryos ultimately released into the water column are subject to natural selection for dispersal/longevity/feeding that sets them on the evolutionary trajectory towards the crown metazoan planktonic larvae. These new insights from poriferan development thus clearly support the intercalation hypothesis of bilaterian larval evolution, which we now believe should be extended to discussions of the origin of biphasy in the metazoan last common ancestor.
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Introduction |
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SynopsisIntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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Extant metazoans exhibit a wide range of life cycles, but the biphasic life cycle, which includes distinct larval and adult phases, is by far the most common and widespread. Indeed, nearly all metazoan phyla—including basal metazoans, such as poriferans and cnidarians, and a wide range of bilaterian phyla—have marine representatives characterized by a specific kind of biphasy, namely the pelagobenthic life cycle (Pechenik 2004
). This is defined by a benthic, sexually reproductive adult phase that generates gametes which are either broadcast and fertilized in the water column, or fertilized and brooded internally. The resultant embryos and pelagic larvae, which are typically microscopic, live for a variable time in the plankton before settling down onto the benthic substrate. At this time, they undergo metamorphosis—which varies in speed and magnitude—back into a benthic adult form, which is usually sessile or sedentary.
Given the extremely widespread nature of the pelagobenthic biphasic life cycle throughout the Metazoa, its origins have received remarkably little attention in the literature. This is in contrast to the extensive and excellent body of literature that goes a long way toward explaining diversification of extant larval forms, and which is not addressed here. There exists a relatively small, and somewhat tangled, web of hypotheses on the origins of biphasy that continues to be discussed and debated (for example, see reviews in Bishop and Brandhorst 2003; Sly and others 2003). From these hypotheses, 2 general schools of thought are emerging—the "terminal addition" school (for example, Nielsen 1979, 1985, Nielsen 2000, Nielsen 2001, Nielsen 2003; Nielsen and Norrevang 1985; Davidson and others 1995; Peterson and others 1997, Peterson and others 2000) and the "intercalation" school (for example, Wolpert 1999; Valentine and Collins 2000; Sly and others 2003). A major limitation of these ideas is that they have been formed almost exclusively by perspectives and data from bilaterian metazoans, with only a cursory nod toward the basal, non-bilaterian phyla. It is now well accepted that Metazoa is a monophyletic group (Fig. 1; Collins 1998; Borchiellini and others 2001; Medina and others 2001; Glenner and others 2004) and that the basic concept of biphasy predates metazoan cladogenesis and already existed in the last common ancestor (LCA) of all extant animals. As such, we argue that there is little relevance to a debate about the ancestry of biphasy in the Bilateria. Instead, the focus should be on the origin of biphasy relative to the LCA of the Metazoa.
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To this end, current weight of opinion (for example, Martindale 2005
) on the origin of metazoan (as opposed to bilaterian) biphasy lies with a simple, larval-like holopelagic ancestor that independently settled multiple times to incorporate by "terminal addition" a benthic phase into the life cycle, as illustrated predominantly by the Trochaea hypothesis (Nielsen 1979, 2001; Nielsen and Norrevang 1985). This hypothesis derives in the general sense from Haeckel's (1874) Gastraea theory of ontogeny recapitulating phylogeny, an idea which has had a profound influence on considerations of animal evolution. Haeckel viewed the gastrula of all extant animals as the recapitulation of a gastraean ancestor that evolved invagination via selection on a simple, planktonic hollow ball of cells (Blastaea) LCA to develop the capacity to feed. The Gastraea theory fell from favor for almost a century, until it was resuscitated and elaborated by Jägersten (1955, 1972) and especially by Claus Nielsen's Trochaea theory in a series of thoughtful, and thought-provoking, papers beginning with Nielsen (1979) and Nielsen and Norrevang (1985) and continuing to the present day (for example, Nielsen 2001, 2003, Nielsen 2005). These hypotheses require that several conditions are met. First, they require multiple, independent incorporations of a "terminally added" benthic phase into an ancestral holopelagic life cycle. Moreover, the reproductive capacity of the holopelagic ancestor must have been transferred in each case into the new benthic phase, because this is the sexually reproductive stage in all extant metazoans that exhibit a pelagobenthic life cycle. Second, they require that the LCA to extant metazoans took the form of a small and simple, blastula-like, hollow ball of cells, and that the ontogeny of this ancestral Blastaea recapitulated metazoan evolution and phylogeny. Third, they require that the embryonic process of gastrulation, which is observed in all extant metazoans (Leys 2004; Martindale 2005), represents a recapitulation of the origin of the gastraea as a response to selection on a hollow balls of cells to develop the capacity to feed.
As exciting new data are now accumulating, hypotheses on the origin and evolution of biphasy can finally begin to take greater account of basal metazoans. Here, we present data from early branching (basal) metazoans, in particular sponges, that we believe shed significant light on this central issue of animal evolution. Although the phylogenetic relationships of the basal metazoans are still poorly resolved (see Fig. 1 for current alternative hypotheses), there is now general consensus that the Porifera diverged first from the rest of the Metazoa and is the most ancient of the extant animal phyla (Fig. 1A). Some recent analyses of 18S rRNA and protein coding genes suggest (albeit with rather weak support) that sponges may be paraphyletic, with the calcareous sponges (Calcarea) more closely related to the Eumetazoa (Cnidaria, Ctenophora, and Bilateria) than to the other sponge classes (Collins 1998; Zrzavy and others 1998; Borchiellini and others 2001; Medina and others 2001). In this scenario, siliceous sponges (demosponges and hexactinellids) comprise the most ancient lineage (Fig. 1B). In terms of considerations of the origin of metazoan biphasy, the basal position of the Porifera places the interest squarely on sponges. Indeed, the possible paraphyly of Porifera relative to the Eumetazoa raises the provocative idea that the ancestor of all metazoans may have been a sponge-like animal.
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The demosponge AMPHIMEDON and reconstruction of the LCA to extant Metazoa |
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SynopsisIntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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Amphimedon queenslandica (Hooper and Van Soest 2006; Porifera, Demospongiae, Haplosclerida, Haplosclerina, Niphatidae; formally referred to as Reniera sp.) is a demosponge and thus a representative of the most ancient animal lineage. Its biphasic pelagobenthic life cycle (Fig. 2) includes a ciliated parenchymella larva that is planula-like in form. Like most demosponges, Amphimedon has internal fertilization and broods its embryos in discrete brood chambers (Leys and Degnan 2001
, 2002). The swimming Amphimedon larva (Fig. 3) has a photosensory system at its posterior end (relative to swimming direction) that consists of a set of ciliated pigment cells organized into a ring (Fig. 3B and C). These cells respond to light in a stereotypic manner, such that the resultant effect is a rudder-like structure that directs movement of the larvae away from areas of higher light (Leys and Degnan 2001; Leys and others 2002). The surface of Amphimedon larvae also appears to have both chemosensory and mechanosensory cells that contribute to the detection of an appropriate location for settlement (Fig. 3D–F; Jackson and others 2002). Together, these sensory systems indicate that the Amphimedon larva is more complex than would be predicted by current theories of the origin of metazoan biphasy.
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The Amphimedon larva consists of a large number (at least 11) of different cell types that are organized into 3 discrete layers—an outer epithelial layer, a middle cell layer, and an inner cell mass (Fig. 3A; Leys and Degnan 2001
, 2002). Some of these cell types, of which the pigment ring cells are the most conspicuous, are patterned along an anterior–posterior axis relative to the swimming direction. Importantly, detailed analyses of Amphimedon embryology and larval formation are demonstrating beyond doubt that sponge development includes many of the hallmarks of eumetazoan embryogenesis (Leys and Degnan 2002; Degnan and others 2005; Larroux and others 2006). Of particular significance is the fact that fertilization is followed by a period of cell division that yields distinct cell populations that are allocated through a gastrulation process (Leys 2004) into different cell layers, and even patterned within these layers along an anterior–posterior axis. Further, gastrulation can lead to the formation of simple tissue-like structures such as the pigment ring (Leys and Degnan 2002). Remarkable and unexpected similarities between the development of this demosponge and that of eumetazoans leads us to infer that the metazoan LCA was likely to have required asymmetric cell division, organizers, morphogen gradients, and populations of cells with differing competencies to construct its body plan (Degnan and others 2005).
In addition to this suite of conserved cellular behaviors, a range of genes previously shown to be involved in eumetazoan development are expressed during Amphimedon embryogenesis and larval development (Larroux and others 2006). The Amphimedon genome in fact contains the same basic repertoire of developmental gene families as found in higher metazoans. These are expressed during embryogenesis and metamorphosis, suggesting that the regulatory architecture underlying eumetazoan development already existed in the metazoan LCA (Larroux and others 2006).
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Basal metazoan data are at odds with the Trochaea theory |
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SynopsisIntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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The ability of sponge cells to differentiate, migrate, and pattern during gastrulation in a manner akin to that in all other metazoans has important implications for the Trochaea theory (Nielsen 1985
; Nielsen and Norrevang 1985). Central to this hypothesis is the phylogenetic placement of the first gastrula-like form at the LCA of cnidarians and bilaterians, after sponges had split from the Eumetazoa (Nielsen 1985, 2000, Nielsen 2001, Nielsen 2005). Contrary to this, our analysis of sponge development leads us to infer that the LCA to all extant metazoans already had the capacity to form a multilayered embryo through the process of gastrulation (Leys and Degnan 2002; Leys 2004; Degnan and others 2005). Furthermore, sponge larvae that develop through the "gastrea stage" do not have any capacity to feed; there is no development of a gut in either sponge larvae or indeed in sponge adults. There simply is no evidence for an association between gastrulation and development of a gut, and no indication of phylogeny recapitulating ontogeny in this sense. In general, sponge embryogenesis appears to be directed by the same developmental gene families as those of eumetazoans. Indeed, the LCA of the Metazoa appears to have had all of the features of body plan currently shared by extant eumetazoans and sponges, namely tissue formation via gastrulation, sensory systems, and a metazoan developmental regulatory network (Fig. 4). Together, these features clearly demonstrate that the LCA was of a vastly more complex phenotype than widely appreciated, and that there is a shared developmental ancestry between the Porifera and the Eumetazoa (Fig. 4). The presence of this complexity and shared developmental ancestry preclude the notion of a simple, hollow ball of cells as a larval-like ancestor in which ontogeny recapitulates phylogeny. As such, there is no support for this aspect of the Trochaea theory.
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The intercalation theory meets the basal metazoans |
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SynopsisIntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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If the Trochaea theory is currently the most generally adopted explanation for the origin of metazoan biphasy, and if our new insights from sponges are at odds with this theory, where should we turn to seek alternative hypotheses? We need look no further than another feature clearly present in the LCA to all Metazoa—the existence of sexual reproduction via meiotically derived eggs and sperm. Although there is no dispute that the origin of sexual reproduction predates metazoan cladogenesis, and that meiosis may be as ancient as the eukaryote, most current discussions on the origin and evolution of biphasy surprisingly do not explicitly incorporate these facts. The fertilized egg is the first step in embryogenesis which, in all multicellular animals, includes a process of gastrulation that generates a multilayered embryo (Leys 2004
; Martindale 2005). At some point in its development, the embryo must separate from the adult, and this separation can itself be considered as the precursor to a biphasic lifestyle, wherein the embryo represents one phase and the adult another phase. Under this scenario, it is most likely that the first metazoan life cycles were direct—that is, they had no larval stage that required a metamorphosis back to the adult state and thus no larval stage that required a capacity to feed (Fig. 5A). It is also likely, although not essential to this hypothesis, that the ancestral adult form was benthic. This precludes the need to hypothesize multiple, independent origins for the "terminally added" sexual benthic form, because the LCA already exhibited a precursory pelagobenthic life cycle.
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As soon as embryos became independent from the adult phase, selection would have acted differentially on size and habitat differences that exist between these 2 phases. The multilayered nature of the first metazoan embryos would have enabled elaboration of different layers of cells, which in turn would have facilitated intercalation of novel morphologies and functions into a direct life cycle. This is because the multiple cell layers enable greater modularity in body plan, which then would facilitate evolvability (Gerhart and Kirshner 1997
) and thus would permit a greater range of morphological diversity and further evolution of dispersal and of phase/habitat-specific inventions (Fig. 5B). It is therefore reasonable to consider that embryos ultimately released into the water column from their putatively benthic parent would have been subject to natural selection for dispersal/longevity/feeding (which reduces susceptibility to local extinction) that would have set them on the evolutionary trajectory towards the crown metazoan planktonic larvae, as already discussed in an extensive and excellent body of literature on the evolution of larval forms (Wolpert 1999; McEdward 2000; Rouse 2000; Strathmann 2000; Collins and Valentine 2001; Bishop and Brandhorst 2003; Sly and others 2003). Each elaboration, in turn, would allow new modules to evolve, which could be incorporated into either the later larval or adult phase and further increase bauplan complexity.
These later novelties would have included the localized formation of larval sensory systems that allow for selection of a suitable habitat for settlement. As seen in extant sponges, such a sensory system does not require integration via neurons (Leys and Degnan 2001; Jackson and others 2002). Natural selection on these systems would be particularly strong, as any individual who settles in unsuitable habitat and/or away from congeners is not likely to contribute to future generations. The existence of sophisticated sensory systems in all extant metazoan larvae is compatible with the metazoan LCA having a pelagobenthic life cycle with a sensitive larva. The wide range of extant adult phenotypes reflects the increase in evolvability that is inherent in this second phase of the life cycle. Of course, the modular design of the metazoan body plan enables the heterochronic shifting of embryonic, larval, juvenile, and adult developmental programs relative to each other, and to metamorphosis, in an enormous variety of ways, as displayed by numerous extant taxa (for example, Wray and Lowe 2000; Sly and others 2003; Byrne 2006).
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Conclusion |
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SynopsisIntroductionThe demosponge AMPHIMEDON and...Basal metazoan data are...The intercalation theory meets...ConclusionREFERENCES |
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In summary, our sponge data permit discussions on the origin of biphasy of the most basal metazoans, beyond that previously possible. These data clearly dismantle the proposal that the LCA was a simple, hollow ball of cells. In contrast, the LCA appears to have been morphogenetically more complex than widely appreciated, employing a developmental regulatory repertoire similar to that used by all extant animals (Fig. 4). The LCA had a complex, multilayered embryo, which formed through an array of entrained intercellular interactions that were encoded in the genome and activated during embryogenesis. Furthermore, there is no evidence that the formation of these cell layers during gastrulation bears any relationship to the origin of feeding. As such, this new view precludes the need for ontogeny to recapitulate phylogeny.
We conclude then that gastrulation is more profitably considered as an ancestral embryonic stage that is a direct consequence of sexual reproduction. The modular design inherent in the multilayered gastrula enables evolvability from that stage onwards. We suggest that natural selection on the embryo would have acted in the first instance to select for a capacity for dispersal, rather than for feeding. Our data strongly support the intercalation hypotheses discussed previously in the context of bilaterian larval origins and evolution (for example, Wolpert 1999; Valentine and Collins 2000; Sly and others 2003) but not the gastraea/trochaea hypotheses (nor then the set-aside cell hypothesis of Davidson and others 1995; Peterson and others 1997, 2000) of the terminal addition school. Further, we suggest that the ancestral metazoan adult was more likely to have been benthic rather than pelagic, with direct rather than indirect development. We hope that these postulations provide a new starting point for consideration of the evolution of metazoan larval forms and embryonic development.
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Acknowledgements |
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We thank Sally Leys and Claire Larroux for providing images shown in this article. We are grateful to the Society for Integrative and Comparative Biology (SICB) for promoting and partially funding the symposium in which these ideas were first presented. We are very grateful to Andreas Heyland, Jason Hodin, Corey Bishop, and Leonid Moroz for organizing this symposium and for inviting us to contribute, and to all audience-members from the platform and associated-sessions for constructive discussions. Furthermore, we would like to thank the following organizations for their generous financial support: the University of Florida, The Whitney Laboratory for Marine Biosciences, the American Microscopical Society (AMS), and the SICB Division of Evolutionary Developmental Biology (DEDB). Research into the biology of Amphimedon sp. 2456 (formerly known as Reniera sp) has been supported by grants from the Australian Research Council and the United States Department of Energy Joint Genome Institute to B.M.D.
Conflict of interest: None declared.
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Footnotes |
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From the symposium "Metamorphosis: A Multikingdom Approach" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2006, at Orlando, Florida.
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