Integrative and Comparative Biology Advance Access originally published online on August 30, 2006
Integrative and Comparative Biology 2006 46(6):827-837; doi:10.1093/icb/icl032
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Qualitative shift to indirect development in the parasitic sea anemone Edwardsiella lineata
Department of Biology, Boston University 5 Cummington Street, Boston, MA 02215, USA
Correspondence: 1E-mail: reitzel{at}bu.edu
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Synopsis
Introduction: defining...Direct development lies at 1 end of a continuum that encompasses various degrees of indirect development. Indirect development exists where a larval stage is interposed between the embryo and the adult and undergoes metamorphosis, though the ecological and morphological distinctiveness of the larval stage relative to the adult stage can vary tremendously. There are numerous empirical examples where direct development has evolved from indirect development, but little empirical evidence describing a recent transition from direct to indirect development. Here, we suggest 4 criteria for defining indirect, and therefore metamorphic, life histories. We then apply these criteria to address the planula–polyp transition in cnidarians, focusing on 2 species in the anthozoan family Edwardsiidae. The lined sea anemone, Edwardsiella lineata, has made a qualitative shift towards indirect development that coincides with, and was potentially facilitated by, the evolution of endoparasitism. We compare E. lineata's development with that of a closely related sea anemone, Nematostella vectensis, where the nonfeeding planula gradually develops the morphology of the adult polyp. In E. lineata, a novel parasitic life history stage is interposed between the planula and the polyp. We discuss how the evolution of endoparasitism could facilitate the evolution metamorphic life histories.
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Introduction: defining metamorphic criteria |
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Animal life histories can be broadly categorized into 2 classes: direct development and indirect development. Indirect development encompasses a larval stage that undergoes a metamorphic transition into a juvenile. Direct development by definition lacks a larval stage. Despite such an apparently clear dichotomy, defining sharp limits for what is and is not a larva remains difficult due to a continuum of developmental strategies (reviewed by Hickman 1999
). Emphasis for making life history classifications has been placed on both morphological (McEdward and Janies 1993) and ecological plus morphological criteria (Chia 1974).
Metamorphic transitions between larval and adult stages are frequently accompanied by dramatic shifts in (1) morphology, (2) feeding ecology, and (3) habitat. The designations of metamorphic life histories in animals is therefore dependent on delineating what are and are not distinct, intermediate stages (Heyland and others 2005). The recognition of distinct intermediate stages is difficult in many cases because larvae may differ in the degree to which they are ecologically and/or morphologically distinct from the adult, and indirect life histories may differ substantially with respect to the duration of the larval stage. For these reasons, a graded classification scheme that recognizes degrees of indirect development may be more representative of the diversity of organismal life histories than a dichotomous classification scheme (for example, Hanken 1999; Nagy and Grbi
1999; Webb 1999).
In general, we suggest that 4 criteria will prove useful in delineating metamorphic events: (1) unique morphological structures and/or developmental regulatory genes involved in body plan patterning in a preadult stage, (2) tissue remodeling between stages involving apoptosis, (3) specific exogenous and endogenous signaling that elicits and/or coordinates a transition between stages, and (4) qualitative niche shift characterized by changes in ecologically relevant characters such as feeding method or habitat.
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Evolutionary shifts between direct and indirect development |
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Phylogenetic analyses suggest that many, if not all clades with direct and indirect developing species, direct development is derived, in some cases occurring independently multiple times (Jägersten 1972
; Strathmann 1978, 1985). Indirect life histories are considered primitive in most phyla (Nielsen 1998), even where the basal group within the phylum is composed of direct developing species (for example, Nemertea, Maslakova and others 2004) The common ancestor of crown group metazoans is widely thought to have been an indirect developer although the exact route by which this ancestral life history evolved is disputed (Jägersten 1972; Nielsen 1998, 2000; Collins and Valentine 2001).
The developmental innovations underlying evolutionary shifts between direct and indirect life histories have been studied extensively. Cornerstone examples include the evolution of direct development in echinoderms (Wray 1995; Raff 1999; McEdward and Miner 2001; Sly and others 2003), particularly within the echinoid genus Heliocidaris (Wray and Raff 1989; Raff 1992; Emlet 1995), ascidians (Huber and others 2000) and amphibians. Direct developing amphibians have evolved from indirect developing ancestors both through the loss of the larval stage (Callery and others 2001) the loss of the adult stage (Voss and Shaffer 1997, 2000). In each of these systems, closely related species represent divergent life histories with the direct developing species being derived.
Due to the ancient origins of indirect development in extant phyla, and the relative rarity with which indirect development has evolved from direct development in recent times, very few studies have investigated the causes and consequences of such a life history shift. One group of organisms where the evolution of indirect life history from direct developing ancestors has been studied is the insects (Truman and Riddiford 2002). However, holometabolous insects are a monophyletic group that diverged from hemimetabolous ancestors 
300 Mya (Kristensen 1999), so this transition from direct to indirect development happened only once, and it happened long ago.
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Metamorphosis in the Cnidaria |
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Applying the term metamorphosis to species' life histories within the Cnidaria is a challenge because cnidarians display remarkable diversity in life histories, representing a spectrum of sexual and asexual reproductive patterns (Fautin 2002
). Some life history transitions involving asexual reproduction could be regarded as metamorphosis, especially where 2 stages differ dramatically in morphology and ecology (for example, strobilation in scyphozoans, cubomedusae formation, Straehler-Pohl and Jarms 2005). However, much of the discussion over cnidarian metamorphosis has focused on the transition from pelagic larva (planula) to benthic polyp (juvenile/adult form; Müller and Leitz 2002).
The transition from planula to polyp has been intensively studied in certain colonial hydrozoans, especially Hydractinia (Frank and others 2001; Müller and Leitz 2002) and Pennaria (Martin and Archer 1986, 1997). In these taxa, 3 of the 4 criteria that we have suggested for designation of metamorphosis are clearly met. First, there is some evidence that these hydrozoans are characterized by unique morphological structures and developmental regulatory genes (criterion 1). The transition from the planula to the polyp is characterized by the loss of some larval-specific cell types (Martin and Archer 1997)—for example, RFamide-positive neural network (Martin 2000). The patterning of the primary oral–aboral axis appears to be established in the planula stage and maintained in the primary polyp. Very little data are available to assess whether there are distinctive larval versus polyp gene expression patterns. Only a few developmental regulatory genes have been studied in multiple stages (ems: Mokady and others 1998; Cnox-2: Cartwright and others 1999; Masuda-Nakagawa and others 2000; Cnox-1: Kamm and others 2006). The expression of Cnox-2 is consistent between planula and polyp in Podocoryne carnea (Masuda-Nakagawa and others 2000), but the expression of Cnox-1 undergoes a qualitative shift during this transition in another hydrozoan, Eleutheria dichotoma (Kamm and others 2006).
Despite the modest morphological and changes during the planula to polyp transition, these hydrozoans undergo extensive tissue remodeling and apoptosis at settlement (criterion 2). There are cell migrations along the oral–aboral axis, particularly in the aboral region where the base or stolon forms. Apoptosis is also widespread and particularly prominent in the aboral portion of the larva, beginning shortly after metamorphosis is induced and continuing until adult patterning commences with tentacle formation (Seipp and others 2001). Indeed, apoptosis is essential for this shift because inhibition of caspase-mediated apoptosis results in a failure to develop the polyp (Seipp and others 2006).
Work with Hydractinia has shown that both specific exogenous and endogenous signaling elicits and coordinates a transition between planula and polyp (criterion 3). Hydractinia planulae are induced for settlement through (1) a number of positively charged ions (Spindler and Müller 1972; Müller 1973) or (2) other direct activators of protein kinase C (Leitz and Müller 1987; Leitz 1993; Schneider and Leitz 1994) that stimulate excitable neurosensory cells in the aboral portion of the embryo. Following settlement, experimental work has shown that a particular class of neuropeptides orchestrates internal signaling for metamorphosis (Leitz 1998). These compounds are synthesized and released from the aboral end of the larva and are thought to travel along axonal fibers to induce oral cells. If settlement cues are eliminated, larvae will swim indefinitely and eventually die. Similarly, settlement inhibitors such as taurine and the betaines that are present in the larvae have also been identified (Müller and Leitz 2002). These inhibitors decrease in quantity when larvae begin settlement.
Finally, Hydractinia, Pennaria, and other hydrozoans with similar life histories in general show a qualitative niche shift characterized by changes in both habitat and feeding (criterion 4). Pelagic larvae undergo settlement to benthic, sessile polyps. Because these planulae are effectively nonfeeding, there is a transition in feeding mode to feeding in the adult stage, although this shift is of limited utility in defining metamorphic life histories.
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Family Edwardsiidae: direct to indirect development? |
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The family Edwardsiidae is a monophyletic group of largely burrowing sea anemones in the order Actinaria (class Anthozoa, phylum Cnidaria). A systematic study of relationships of genera in the Edwardsiidae by Daly (2002b)
supported 2 major clades in the family: the Edwardsiinae (Edwardsia, Scolanthus) and the Milneedwardsiinae (Paraedwardsia, Drillactis, Edwardsiella, and Nematostella). Although few studies have reported on the development and life history of species of Edwardsiid anemones, it appears likely that the life history exhibited by Edwardsia and Nematostella, and by most Anthozoa, is the ancestral life history: external fertilization is followed by the development of a ciliated planula, followed by a benthic juvenile and an adult polyp (Widersten 1972).
Nematostella vectensis: direct development?
Nematostella vectensis is a representative Actinarian species that is an emerging experimental system for studying evolution, development, and evolutionary genomics (Darling and others 2005). N. vectensis undergoes both sexual and asexual reproduction. During sexual reproduction, fertilized eggs undergo asynchronous development through a free-living planula into the polyp (Reitzel and others in review, and references therein). The gradual transition between planula and polyp stages is accompanied by the loss of the planula's sensory organ (the apical tuft) and the development of the adult's feeding structures (tentacles, pharynx, and mouth), digestive (mesentery), and gamete producing tissues (mesentery) (Fig. 1).
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By nearly any measure, N. vectensis's development from embryo to polyp is gradual and rather direct. From a morphological and developmental perspective, the transition from planula to polyp does not appear abrupt. Adult morphological characters (pharynx, mesenteries, and tentacles) begin to develop during the planula stage, well prior to settlement. The apical tuft, a bundle of long cilia at the aboral end of the planula, is the only planula structure lost prior to settlement, but its loss is not synchronous with settlement. It is not yet known whether certain larval cell types might be lost prior to or during the transition to the polyp stage, as in Hydractinia and Pennaria. For example, we might expect that neurons associated with the cilia of the apical organ would degenerate. As the only example of a qualitative structural distinction between planula and polyp, the apical tuft alone does not appear sufficient to designate N. vectensis as an indirect developer.
Consideration of additional developmental events from embryo to juvenile are consistent with the designation of N. vectensis as an essentially direct developing species. The principal body regions exhibited by the polyp are established early in development: pharyngeal regions, tentacular zone, body column, and physa. Concordantly, the expression territories of many axial patterning genes, including representatives from the Hox family of transcription factors (Finnerty and others 2004) and Wnt signaling peptides (Kusserow and others 2005), remain largely unchanged through the planula to polyp transition (Fig. 2).
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Consistent with the gradual developmental transition from embryo to polyp, there does not appear to be extensive tissue remodeling between stages as exhibited in the aforementioned hydrozoans. N. vectensis does not appear to undergo the tissue dynamics characterized by settling Hydractinia or Pennaria, showing only elongation from planula to polyp. For example, TUNEL-staining (as per Seipp and others 2001
) with N. vectensis specimens during various stages of development has indicated little, if any apoptosis in the developing planula or polyp. In addition, we did not observe TUNEL-positive cells during larval developmental stages that coincide with stages where the apical tuft is lost, suggesting that the widespread apoptosis observed in hydrozoans during transition to the polyp does not occur in N. vectensis.
Specific exogenous signaling is not required for the transition from planula to polyp. Solitary planulae will readily undergo differentiation to the benthic polyps in bowls of sterile artificial seawater. It is unclear if or how endogenous signals may operate during the planula to polyp transition. Neuropeptides play a prominent role in the metamorphosis of Hydractinia as well as in morphogenesis of Hydra (Steele 2002). In addition, endocrine-like signaling in addition to other bioregulatory molecules have been identified in a number of cnidarians (Tarrant 2005), but we know little about their involvement in life history processes.
Finally, it is uncertain if the planula to polyp transition for N. vectensis could be considered a qualitative shift in their niche. The ciliated planulae generally remain motionless on the bottom of culture dishes in the laboratory (Williams 1975; Hand and Uhlinger 1992). In the only potential field collection of planulae, Williams (1975) reported larvae residing in the same sediment occupied by the sessile adults. We have observed similar larval behavior in laboratory observations where larvae introduced to a dish containing sediment will passively settle and burrow below the surface. As such, there is little evidence to indicate that the planula would typically occupy the pelagic environment. Laboratory observations can only approximate the likely field behavior of these larvae and observations of natural larval behavior would be necessary to validate laboratory observations and studies. Recent population genetic studies of N. vectensis have supported our view that larvae are unlikely to be pelagic stages. Significant population genetic structure is evident between closely spaced subpopulations within a single salt marsh (Darling and others 2004; Reitzel and others in review).
There is currently little descriptive evidence of Edwardsiid development and until further studies with additional species are reported, we cannot definitively qualify N. vectensis' development as ancestral for the family Edwardsiidae. Although there are distinct similarities with reported stages from other Edwardsiids and anthozoans in general, the underlying tissue dynamics, signaling, and niche shifts may vary. There is some reason to suggest that N. vectensis may have followed a novel trajectory, potentially in response to specialization for a novel habitat (estuaries). N. vectensis is the only estuarine member of the Edwardsiidae. Its preferred habitat is very patchy in distribution. For this reason, N. vectensis may have evolved strategies to limit dispersal in order to prevent the offspring from being flushed out of suitable estuarine pools. Such strategies would include the evolution of benthic egg masses and possibly demersal development. Accelerating the development of adult characters so that they appear in the planula (adultation) would likewise serve to minimize dispersal and would result in the loss of a larval stage. Whether these developmental events are unique to N. vectensis and indeed represent heterochronic shifts is unclear and determination awaits further description of development from other Edwardsiid anemones.
Edwardsiella lineata: indirect development and endoparasitism
In stark contrast to N. vectensis, the lined sea anemone, Edwardsiella lineata, undergoes indirect development, with a biphasic life cycle that includes a parasitic stage (Crowell 1976). Recent phylogenetic analyses suggest that Nematostella and Edwardsiella are closely related genera with the family Edwardsiidae, perhaps even sister taxa (Daly 2002a; Daly 2002b). The lined sea anemone, E. lineata, lives in shallow ocean water in the northwestern Atlantic, from Cape Cod to Cape Hatteras (Daly 2002a). Adults reproduce both sexually and asexually and have been found in mats of hundreds of individuals; presumably these colonies are the result of local asexual reproduction (Crowell and Oates 1980).
Crowell (1976) and later Crowell and Oates (1980) described portions of the life history of E. lineata. We have added further observations for this species (Fig. 1). Free-living ciliated planulae selectively infect ctenophores of the species Mnemiopsis leidyi either through the epidermis (Crowell 1976) or through the gastrovascular cavity (Reitzel, Sullivan, and Finnerty unpublished data). The anemones position themselves along the pharynx or in the ciliated area near the esophagus with their oral end just inside the digestive cavity (Crowell 1976; Reitzel, Sullivan, and Finnerty unpublished data). The parasites elongate and assume a vermiform shape with a differentiated pharynx. The parasites occasionally possess thin mesenteries, sometimes numbering up to 4. Some time after infecting the host, the parasite assumes a more spherical shape and exits the host as a planula-like stage. At this point in the life history, E. lineata can either reinfect another ctenophore or settle as the benthic juvenile polyp. At this settling stage, tentacles emerge and all 8 mesenteries are present.
E. lineata's life history reflects a qualitative shift towards indirect life history—the parasite is clearly a novel life history stage, and it represents a detour from the ancestral planula-to-polyp developmental trajectory. At the morphological level, while the parasitic stage does not exhibit any unique structure, it does exhibit a novel combination of features. For example, like the polyp, it lacks the well-developed external ciliation characteristic of planula. However, like the planula, the parasite lacks the well-developed retractor muscles characteristic of the polyp. It lacks tentacles entirely, but it does possess a well-developed pharynx, and larger individuals may exhibit 1 or 2 pairs of thin mesenteries.
At 2 life stage transitions, E. lineata does undergo extensive tissue remodeling involving apoptosis (1) when the parasite re-assumes the planula form when exiting the host and (2) when the postparasite planula settles to form a polyp. In both instances, TUNEL-positive cells are found in the aboral ectoderm, reminiscent of Hydractinia larvae induced to settle (Fig. 3). In addition, TUNEL-positive cells are found in newly differentiated tentacles. Apoptosis in the parasite to planula transition correlates with the compaction of the vermiform-shaped parasitic body into the more rounded planula.
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While specific exogenous chemical cues have not been described for the infection of M. leidyi, the specificity of the host–parasite relationship suggests that E. lineata planula may rely on host cues for infection. Over 2 sampling seasons, we collected 871 E. lineata parasites from 4015 sampled M. leidyi at Woods Hole, MA, USA. Over the same period, we sampled 600 ctenophores of the genus Pleurobrachia and found no infections in any of these ctenophores. While M. leidyi tends to be larger than Pleurobrachia species, we have found many infected M. leidyi within the size range of Pleurobrachia. In addition, various cnidarian medusae are present in E. lineata's range and none have been reported to harbor E. lineata parasites.
As with N. vectensis, endogenous signals regulating the transitions between life history stages have not been identified in E. lineata, but any endogenous signal transduction pathways are likely sensitive to chemical signals from the host. In general, when parasites have the opportunity to infect multiple hosts they benefit from knowing the physiological status of the individual they are infecting (Ueno 1994). Results from our laboratory have shown that when hosts are exposed to stressful conditions, parasites begin to undergo the morphological modifications necessary to revert to a free-living state to exit the host. Postparasitic planula can follow 2 developmental trajectories: they may reinfect another ctenophore and re-assume the parasite body plan, or they may settle as a benthic polyp. Those developmental regulatory pathways that re-establish the parasite body plan must be downstream of some signal derived from the host.
E. lineata displays a clear shift in ecological niche between the parasite and polyp. The parasite feeds through ciliary suspension feeding in the ctenophore digestive system, typically the esophagus and more rarely the pharynx. The ctenophore esophagus is lined with dense bunches of cilia where ingested food is disrupted for extracellular digestion (Bumann and Puls 1997). In contrast, the polyp is a tentacular feeder, likely feeding on pelagic zooplankton although field dietary studies have not been completed. The pelagic parasite represents a potential dispersal stage because ctenophores travel great distances with the currents while the polyps are sessile benthic organisms.
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Molecular mechanisms underlying changes in ontogeny |
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Analysis of expression of development regulatory genes may provide fundamental insights regarding the evolution of an indirect life cycle from a direct developing ancestor (Raff and Sly 2000
). Morphological differences between the parasite and other life history stages suggest that the parasite may reasonably be regarded as a simplified version of the polyp—a simplified version of the polyp that does not develop tentacles and seldom mesenteries. Concordant with the lack of mesentery differentiation, the parasite does not appear to possess retractor muscles. If the parasite is missing pattern elements that are present in the adult polyp, it seems likely that the genes responsible for patterning the polyp body plan might underlie this evolutionary transformation. If the spatiotemporal expression of a particular patterning gene is compared during the planula-to-polyp transition (ancestral) and the planula-to-parasite transition (derived), the following 3 outcomes emerge as logical possibilities (Fig. 4). (1) The spatiotemporal expression of a particular patterning genes might be unaltered in the derived developmental pathway. The loss of structures in the derived ontogeny might then be attributable to downstream events: for example, changes in how these patterning genes interact with downstream target genes, changes in the function of the downstream targets themselves, or quantitative change in the number of transcripts produced at a particular time in development (for example, novel leg repressing activity in the Ubx protein of insects; Galant and Carroll 2002). (2) The expression territory of a particular gene might be altered—either expanded or contracted. Altered gene expression territories might cause the loss of particular structures during parasite development because co-expressed regulatory genes can collaborate to affect downstream cell-fate decisions in a kind of combinatorial code. Altering gene expression boundaries can perturb the ancestral code, resulting in a novel body plan (for example, shifting boundaries of Ubx/abdA expression in crustaceans and its effect on the form of the thoracic appendages; Averof and Patel 1997). (3) The expression territory of a particular gene might be deleted. The loss of particular structures might be caused by the deletion of particular gene expression territories during parasite development. If a key regulatory gene is switched off in the planula-to-parasite transition then downstream developmental events may not be initiated (for example, downregulation of the Manx gene in tailless ascidian embryos; Swalla and Jeffery 1996).
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Given the plethora of gene expression work reported from N. vectensis, there are a number of genes expressed in specific structures and body regions for both ectoderm and endoderm, thus providing a number of experimental tests for the hypotheses outlined above. For example, mef2, soxD1, and m-LIM are 3 genes with spatially segregated expression in the tentacles of N. vectensis (Martindale and others 2004
; Magie and others 2005). Studying these genes in E. lineata polyps and parasites might allow us to distinguish between hypotheses 2 and 3. If the genes were not expressed in the tentacles during polyp development, but they are not expressed during parasite development, this would suggest that these gene expression territories have been deleted concordant with the absence of tentacles (hypothesis 3). Alternatively, if the expression of these genes is altered relative to other patterning genes during parasite versus polyp development, this would support hypothesis 2. Studying gene expression between stages of E. lineata would also address if the planula stage that forms while exiting the host ctenophore could be best regarded as a reversion to the original postembryogenesis planula stage as observed during reverse development in other cnidarians (Sammarco 1982; Piraino and others 2004) or a unique intermediate stage. |
Metamorphosis and endoparasitism |
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The evolution of parasitism from free-living ancestors can result in dramatic changes in organismal life histories (for example, polyembryony in parasitoid wasps, Grbi
and Strand 1998; Grbi 2003). The evolution of parasitism, particularly endoparasitism, results in the necessity for the infecting species to (1) locate the appropriate host(s), (2) infect the host by entering and establishing at appropriate location(s), and (3) extract nutrition from the host, either through feeding on the host's tissues or the host's ingested food. Thus, many parasites fulfill a number of criteria for a metamorphic life history in that a stage parasitic on 1 host usually differs from the free-living stage or parasitic stage on another host in habitat, food sources, and morphology.
Endoparasitic flatworms, particularly digenean trematodes, exhibit remarkable evolutionary innovations resulting from the origin of obligate parasitism. Their life histories typically involve a series of stages (miracidium, sporocyst, redia, cercaria, metacircaria, reproductive adult), with 2 or more hosts, and at least 2 infective stages. Developmental transitions between these stages generally involve events characteristic of metamorphosis (miracidium to sporocyst: neodermis formation, shift to host habitat; cercaria to metacircaria: tail, digestive tract, and suckers formation, shift to free-living environment (Ruppert and others 2004). Cribb and others (2001) mapped various digean life cycles on phylogenies and found changes in life cycles and hosts is common and related. If each host gain is accompanied by the addition of a new parasitic stage adapted to living in the new host, then parasitism is an engine for the evolution of new metamorphoses.
We suggest that the evolution of endoparasitism was the precondition for the evolution of a novel metamorphosis in the life history of E. lineata. Prior to the origin of its parasitic life history, predation by M. leidyi may have selected for planula that could survive ingestion by lodging themselves in benign locations with the ctenophore's digestive tract until the ctenophore died or escape digestion by burrowing through host tissue. Once E. lineata planulae became able to survive ingestion, selection could have favored those individuals that could utilize caloric intake from the host. Regardless of the scenario that favored the evolution of parasitism, the insertion of a successful parasitic stage required coordinated spatio-temporal development in a specific ctenophore species. Although the suite of morphological characters exhibited by the parasite does not differ drastically from other stages in the life history, this may reflect the evolutionary recency of this novel stage. If the parasitic stage is maintained in E. lineata's life history, it will continue to experience different selection pressures than either the planula or the polyp, and it is likely to evolve greater distinctiveness. Similar arguments have been used in describing the evolution of the diversity in holometabolous insects where more radical metamorphic life histories may permit differential selection on different life history stages (Yang 2001).
Larvae of sea anemones from the genus Peachia are able to parasitize pelagic hydromedusae, and such infections appear to be obligate in the case of Peachia parasitica (= quinquecapitata, Spaulding 1972). The genus Peachia belongs to the family Haloclavidae, and the parasitism exhibited by these anemones almost certainly evolved independently from the parasitism of E. lineata. Like E. lineata, the parasitic Peachia lack tentacles, and they feed on predigested material in the hydromedusa gastrovascular cavity via ciliary currents. However, Peachia differs from E. lineata in that it also feeds on the gonads and potentially other body parts of its host (Spaulding 1972). In addition, Peachia differs from E. lineata by becoming ectoparasitic on the bell of its hydromedusa host after developing tentacles. Future studies on the development of Peachia species would provide an informative comparison with E. lineata.
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Conclusion |
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The evolution of indirect and direct life histories is a central question in organismal life history evolution, but studies on the transition from indirect to direct development greatly outnumber studies on the transition from direct to indirect. E. lineata provides valuable insights into the evolution of indirect development from a more direct developing ancestor because this parasitic anemone appears to have made an evolutionarily recent qualitative shift towards indirect development. In addition, E. lineata reveals parasitism to be an evolutionarily plausible route from direct to indirect development. A major challenge to understanding the evolution of indirect development is the following. How can exceedingly distinctive novel life history stages, requiring the evolution of complex new developmental pathways, become interposed in the ontogeny of a direct developing ancestor? If an existing life history stage (for example, a planula) can establish itself as a parasite through fortuitous preadaptations, subsequent selection on the parasite can lead to the evolution of a novel stage that may require a metamorphic transition. Ancient indirect developing lineages do not allow us to track the evolutionary mechanisms underlying the origin of novel metamorphoses. However, in the case of E. lineata, it is possible to make direct comparisons to a closely related, free-living relative, N. vectensis. By leveraging the molecular and genomic tools developed for the closely related anemone N. vectensis, we can begin to assess potential mechanisms for this change in life history. Future studies addressing expression of developmental regulatory genes in different life history stages as well as endogenous and exogenous signaling to coordinate the changes between stages will aid in identifying mechanisms for how the novel stage develops. In addition, such study may help elucidate steps in the evolution of indirect life history; a critical innovation acquired in many dominant animal taxa but something thought difficult to study.
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Acknowledgements |
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We would like to thank the symposium organizers for organizing this symposium. We would like to thank all audience-members from the platform and associated-sessions for constructive discussions. We are grateful to the Society for Integrative and Comparative Biology (SICB) for promoting and partially funding this symposium. 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). We would also like to thank 2 anonymous reviewers for insightful comments that improved this manuscript. A.M.R. was funded by an American Microscopical Society fellowship for the TUNEL-staining for Nematostella and Edwardsiella.
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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