Integrative and Comparative Biology Advance Access originally published online on June 30, 2006
Integrative and Comparative Biology 2006 46(4):508-518; doi:10.1093/icb/icj051
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Distribution of segment regeneration ability in the Annelida
Biology Department, University of Maryland College Park, MD 20742, USA
Correspondence: 1E-mail: abely{at}umd.edu
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The annelids are an excellent group in which to investigate the evolution of regeneration abilities. They exhibit qualitative and quantitative variation in regeneration ability, including among closely related species, and their segmental body organization makes comparing results among species relatively straightforward. Here, I compile information on the presence/absence of segment regeneration ability across the annelids. The ability to regenerate posteriorly appears to be nearly universal in the annelids. It is almost certainly ancestral for the phylum and may have been lost only a few times. The ability to regenerate anteriorly is common but less widespread. It is absent in about a dozen groups, almost surely representing multiple independent losses of this ability. Several non-regenerating species are closely related to regenerating species, indicating very recent losses (or gains). Despite the fact that lack of this ability is unusual, there is a publication bias against reporting the lack of regeneration ability, and in many cases the judgment that a particular species is unable to regenerate is based on incomplete or unpublished data. Thus, in order to build rigorous frameworks for future comparative studies of annelid regeneration, there is a need for published studies clearly documenting the lack of regeneration abilities in annelid species. The review of regeneration data presented here is especially useful in highlighting annelid groups that possess both regenerating and non-regenerating representatives. Investigations of these groups may be particularly useful for elucidating the mechanisms leading to the loss (or perhaps gain) of segment regeneration ability.
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Introduction |
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SynopsisIntroductionAnnelids as a model...Presence/absence of segment...ConclusionsReferences |
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Animals vary dramatically in their ability to replace lost body parts through regeneration (Vorontsova and Liosner 1960
; Goss 1969; Brusca and Brusca 2003), and understanding why is a central question in biology (Morgan 1901; Goss 1969; Elder 1979; Reichman 1984). The phylogenetic distribution of regeneration ability across animals implies that this capability has been gained and/or lost many times. And yet, despite the recent surge in interest in regeneration biology and the clear evidence for the evolutionary lability of regeneration abilities, comparative studies of regeneration are exceedingly rare. To date, regeneration studies have focused almost exclusively on a few, very distantly related species such as hydra, planarians, and amphibians). The deep evolutionary separation between these model systems and the important morphological differences between them make it nearly impossible to reconstruct which evolutionary and developmental mechanisms are responsible for variation in regeneration abilities among such groups. In order to elucidate mechanisms involved in the evolution of regeneration abilities, groups of relatively closely related species must be identified that possess largely similar body plans and vary in regeneration abilities. |
Annelids as a model for comparative regeneration studies |
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SynopsisIntroductionAnnelids as a model...Presence/absence of segment...ConclusionsReferences |
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Annelids are an excellent group in which to investigate regeneration abilities in a comparative context. Although annelids have the general (and well earned) reputation of having extensive regeneration capabilities, this ability actually varies widely among representatives of the phylum, ranging from species completely incapable of any regeneration such as leeches) to species capable of regenerating an entire individual from a single mid-body segment (such as some sabellids, chaetopterids, lumbriculids: Morgulis 1907
; Berrill 1928; Okada 1934). Even a cursory overview of annelid regeneration abilities makes it clear that there have been multiple losses and/or gains of regeneration potential and that these losses or gains are scattered through a long period of evolutionary history.
Regeneration variation may take many forms in the annelids (Hyman 1940; Berrill 1952; Herlant-Meewis 1964). Species may be capable or incapable of regenerating anterior segments, posterior segments, and/or terminal asegmental structures. They may also differ in the maximum number of segments that will regenerate (especially anteriorly), in the axial position from which regeneration can take place, and in the overall extent of tissue removal that can be tolerated. Because their bodies are composed of repeated segments which largely possess the same structures (segmental nerve ganglia and fibers, musculature, gut, blood vessels, chaetal bundles, nephridia, and so on), cuts made at different axial positions along the body result primarily in the removal of different amounts of a given organ system, rather than the removal of different organ systems or unique structures, facilitating comparisons among annelid species.
It is relatively straightforward to score for the ability/inability to regenerate anterior segments, posterior segments, or asegmental terminal structures and to compare findings across multiple species. These "qualitative" differences are much less likely to be influenced by the nutritional or physiological state of a worm than are some of the other types of variation mentioned above. Qualitative variation is expected to reflect differences in the actual developmental potential of species, and as such will map onto a phylogeny as clear gains and losses. For all these reasons, comparative studies of the presence/absence of regeneration abilities will be fruitful avenues of research for investigating the underlying forces shaping regeneration potential. The ability to regenerate anterior and posterior segments is the focus of this review.
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Presence/absence of segment regeneration ability |
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SynopsisIntroductionAnnelids as a model...Presence/absence of segment...ConclusionsReferences |
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Despite the promise of annelids for revealing mechanisms underlying the evolution of regeneration, variation in segment regeneration ability in annelids has not been summarized in over half a century. The classic references on annelid regeneration, such as Hyman (1940)
, Berrill (1952), and Herlant-Meewis (1964), serve as the most recent summaries of such comparative information. Though excellent, these are broad overviews describing general trends and were never intended as rigorous compilations of the presence/absence of segment regeneration ability. In these works, information on the lack of segment regeneration, if even mentioned, is not only primarily unpublished but is primarily unreferenced. A number of cases of non-regenerating annelids have also come to light subsequent to the publication of these references. In Tables 1 and 2, I present compilations of information on segment regeneration abilities in annelids. This summary assembles evidence that for the most part has not previously been reviewed. Information was sought for all major groups of annelids to provide a phylum-wide view of segment regeneration abilities. In addition to gleaning information from key references, I searched literature databases (back to 1970) to recover regeneration information on all families and many large genera. Since examples of the failure to regenerate are frequently unpublished, I made a special effort to obtain information through personal communications with relevant researchers. Still, these compilations are not exhaustive: some older literature and obscure or unpublished data have surely been missed (I would welcome information on any such overlooked sources). Furthermore, for brevity, posteriorly regenerating species are omitted from Table 1.
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The data for Tables 1 and 2 come primarily from laboratory amputation studies. Reports of regeneration during the normal course of asexual reproduction (fragmentation, fission, and epitoky) are not included since there is evidence that some species capable of "regeneration" during (endogenously induced) asexual reproduction may, surprisingly, be incapable of regeneration following amputation (Bely 1999
).
Evidence for the presence of segment regeneration ability is unambiguous. For example, if a species is found to regenerate segments anteriorly, from any position along the body, then the capacity for regenerating anterior segments is demonstrated. It is less straightforward, however, to demonstrate that segment regeneration ability is absent. With respect to anterior regeneration, for example, it is common for a species capable of anterior regeneration to regenerate if few segments are removed but to fail to regenerate if many segments are removed (for example, Berrill 1928). Thus, ideally studies to determine whether segment regeneration ability is present or absent should include cuts that remove a range of number of segments and should also include minimal challenges, such as removing just a single segment. In practice, many species are suspected of being incapable of regenerating (anteriorly or posteriorly) based on the finding that they fail to regenerate following cuts at just one or a few axial positions. Only a few species (for example, Streblospio benedicti, Paranais litoralis) have been subjected to detailed regeneration studies including minimal-challenge amputations (Bely 1999; S. M. Lindsay and J. L. Jackson, unpublished data). Such studies should be performed on the remainder of species suspected of not regenerating in order to confirm the absence of this ability.
Posterior segment regeneration
The capacity for regenerating new posterior segments is extremely common among annelids (Hyman 1940; Herlant-Meewis 1964). Posterior regeneration has been documented in numerous annelid groups, including essentially all taxa listed in Table 2 for which anterior regeneration has been documented, as well as many others. (Because posterior regeneration ability is so common, references to studies documenting this ability have not been included in Table 1.) I have identified only five groups that appear to be incapable of posterior regeneration: the polychaetes Arenicola marina (Arenicolidae), Polyophthalmus pictus (Opheliidae), and Myxicola infundibulum (Sabellidae); the Hirudinida (leeches); and the close allies of the leeches, the Branchiobdellida (Table 1).
Arenicola marina (Arenicolidae) is an infaunal polychaete that frequently loses the tip of its tail to browsing predators (De Vlas 1979b). Although many articles refer to posterior "regeneration" in this species, it in fact appears to be completely incapable of regenerating posterior segments. After losing posterior segments, this species regrows its tail by lengthening remaining tail segments, not by adding new segments (De Vlas 1979b). Individuals that have lost many posterior segments thus possess extremely elongated tail segments (an individual segment may measure several centimeters in length!). This fascinating phenomenon of segment lengthening has been well characterized in part because arenicolid tail tips (and, specifically, regrowing tail tips) can comprise a significant food source for juvenile flatfish (De Vlas 1979a). The body of A. marina is comprised of three regions, the abranchial anterior segments, the branchial central segments, and the posterior achaetous tail segments. The segment-lengthening process is known to occur only in the tail region following amputation within this region; no studies could be found describing the result of cuts within the anterior or central region of the body. Other species of Arenicola and species of the closely related genus Abarenicola also have a three-part body and similar tail morphology to that of A. marina (Rouse and Pleijel 2001) and it seems likely that these species regrow their tails through a similar process not involving segment regeneration, though this needs to be confirmed. The other two genera of Arenicolidae, Branchiomaldane and Arenicolides, possess only the abranchial anterior region and the branchial region that follows (that is, there is no achaetous tail), and no studies of their regeneration abilities could be found.
The polychaete P. pictus (Opheliidae) is capable of posterior wound healing but appears to be incapable of any posterior regeneration (Stolte 1929 in Hyman 1940). At the time of Hyman's review, P. pictus was the only polychaete recognized as being incapable of posterior regeneration. I was unable to find any information on the posterior regeneration abilities of close relatives of P. pictus or any other Opheliidae. Therefore, the size of this posteriorly non-regenerating clade is unknown. In the Maldanidae, the family thought to be most closely related to the Opheliidae (Rouse and Pleijel 2001), several species are known to regenerate posteriorly (for example, Sayles 1932; Sayles 1936; Wilson 1979; Clavier 1984) and none have been shown to be incapable of posterior regeneration.
Myxicola infundibulum (Sabellidae) appears to be yet another non-regenerating polychaete. Experiments by Wells (1952) and unpublished data by J. A. C. Nicol in Wells (1952) suggest it is incapable of both posterior and anterior regeneration. It should be noted, however, that these authors performed cuts at only a few positions along the body. M. infundibulum in laboratory cultures has not been observed to regenerate segments; damaged worms not only fail to repair damage but often succumb to infection and die (R. Abercrombie, personal communication). Interestingly, other sabellids (Berrill 1931) and even a congener, M. aesthetica (unpublished data by J. A. C. Nicol in Wells 1952) can regenerate posteriorly. Thus, it is likely that the posteriorly non-regenerating clade represented by M. infundibulum is quite small, involving only one or a few species.
That leeches cannot regenerate segments posteriorly (or anteriorly) is undisputed and is commonly stated in the literature (for example, Hyman 1940), though no primary data sources could be located to reference this claim. At least some leeches can wound heal (Le Gore and Sparks 1971; Huguet and Molinas 1994, 1996) and undergo limited nervous system repair (through axon regeneration and reformation of synapses) (von Bernhardi and Muller 1995), but there is no regeneration of tissues or whole segments. There are also no published studies of segment regeneration (or lack thereof) in the closely related Branchiobdellida, but based on observations of individuals that were experimentally wounded, it is almost certain that this process does not occur (S. R. Gelder, personal communication). When a branchiobdellidan is bisected at any point along its body, the internal organs and coelomic fluid in that segment (and possibly adjacent segments) are pushed out of the wound and the individual parts of the body show signs of autolysis within 1 h. A partial breach of the body wall into the coelomic cavity has a similar result. Thus, branchiobdellidans appear to be incapable not only of regenerating but of even surviving amputation. It seems likely that the Acanthobdellida, close relatives of leeches and branchiobdellidans (and the third group within the Hirudinoidea clade), are similarly incapable of regenerating segments, but there are no studies confirming this. Collectively, leeches and their close allies almost surely represent the largest annelid clade incapable of posterior regeneration. Interestingly, the clitellate group thought to be most closely related to the Hirudinida + Branchiobdellida + Acanthobdellida is the Lumbriculidae (Siddall and others 2001), some of which are known to have extensive regeneration abilities, being capable of regenerating biaxially from a fragment comprised of only a few segments (Hyman 1916).
The widespread distribution of posterior regeneration ability suggests that this ability is almost certainly an ancestral feature for annelids that has been lost only a few times. This may be related to the fact that in many respects the process resembles adult growth by segment addition (Herlant-Meewis 1946a; Bely and Wray 2001), which itself is very common in the phylum. The likely ages of posterior regeneration losses range from quite old, as in the case of leeches and branchiobdellidans (none of which are known to regenerate), to very recent, as in the case of M. infundibulum (close relatives of which can regenerate posteriorly).
Anterior segment regeneration
The ability to regenerate segments anteriorly is widespread among the annelids (Table 2), though less so than posterior regeneration ability. Interestingly, all taxa identified as being incapable of posterior segment regeneration (Table 1) are similarly incapable of anterior segment regeneration (Table 2) (although the converse is not true). Thus, A. marina (Arenicolidae), P. pictus (Opheliidae), M. infundibulum (Sabellidae), leeches and branchiobdellidans all appear to be incapable of any segment regeneration at all. In addition, several taxa that can regenerate segments posteriorly cannot do so anteriorly. These include at least some representatives of the Capitellidae, Polynoidae, Nereididae, Dorvilleidae, Eunicidae, Oweniidae, Sabellidae, Spionidae, and Tubificidae.
Amputation experiments in Capitella sp. I (Capitellidae) show that this species is incapable of anterior regeneration (S. Hill, personal communication) although it can regenerate segments posteriorly. If worms are cut at a range of positions in the thorax and abdomen, the wound is sealed over but worms fail to regenerate and eventually starve to death. Even after minimal cuts removing only the dorsal part of the (asegmental) prostomium and peristomium, wound healing occurs but no obvious regeneration ensues. Less comprehensive exploratory experiments on two other capitellid species, Capitella sp. II and Mediomastus sp., suggest that they are similarly incapable of anterior regeneration, although capable of posterior regeneration (S. Hill, personal communication), and indeed there is currently no evidence for anterior regeneration in any of the Capitellidae.
Among the nereids, dorvilleids, and polynoids, there is similarly no evidence for anterior segment regeneration, despite the fact that species in these polychaete families have been shown to regenerate posteriorly. The nereid Platynereis dumerilii does not regenerate anteriorly following cuts that remove anterior segments or even just the prostomium (Hauenschild 1960 in Pfannenstiel 1974). Only when some of the prostomium remains does regeneration (of the rest of the prostomium) occur. A similar situation is found in Ophryotrocha puerilis and Ophryotrocha notoglandulata (Dorvilleidae) (Pfannenstiel 1973, 1974) in that no anterior segments are regenerated and part of the prostomium must remain in order to elicit any regeneration (of the prostomium). In the Polynoidae, also, no evidence of anterior regeneration could be found. When Harmothoe imbricata worms are cut roughly in half (around segment 20), the posterior half fails to regenerate anteriorly, although the anterior half does regenerate new posterior segments (Daly 1973).
While the arenicolids, opheliids, capitellids, nereids, dorvilleids, and polynoids lack any evidence of anterior segment regeneration, a number of other annelid families possess both anteriorly regenerating and anteriorly non-regenerating species. Although Hyman (1940) states that eunicid, oweniid, and phyllodocid polychaetes are generally incapable of anterior regeneration, there is evidence of anterior regeneration in at least a few species from these groups (Table 2). Specifically, anterior segment regeneration has been observed in the eunicids Lysidice spp. and Nematonereis unicornis (M. C. Gambi, personal communication), the oweniid Owenia fusiformis (Coulon and others 1989; Dupin and others 1991), and the phyllodocid Eulalia viridis (Olive 1975). Further studies are needed to determine whether these species have retained ancestral regeneration abilities or evolved them de novo.
Conversely, while many sabellid polychaetes, spionid polychaetes, and tubificid oligochaetes are known to undergo anterior segment regeneration, each of these groups also includes at least one species that clearly cannot regenerate segments anteriorly (Table 2). Among the Sabellidae, M. infundibulum cannot regenerate anterior segments, even if just a single anterior segment is removed (Wells 1952; J. A. C. Nicol, unpublished data in Wells 1952). It can, however, regenerate the feeding crown, which is derived from the asegmental prostomium. A number of other sabellids, including the congener M. aesthetica, can regenerate segments anteriorly (Berrill 1931), suggesting that the anteriorly non-regenerating clade is quite small, perhaps including only one or a few species. In the Spionidae, while many species can regenerate segments anteriorly, recent evidence suggests that S. benedicti cannot regenerate if even a single anterior segment is removed, although it can regenerate segments posteriorly (S. M. Lindsay and J. L. Jackson, unpublished data). Like M. infundibulum, Streblospio benedicti is capable of regenerating anterior asegmental structures, in its case the feeding palps. Again, it seems likely that S. benedicti represents a small anteriorly non-regenerating clade. Finally, among the Tubificidae, many species regenerate segments anteriorly but the naidine Paranais litoralis does not, although it is capable of posterior regeneration (Bely 1999). In experiments in which one, three, five, or seven anterior segments are removed, worms wound heal but never regenerate segments anteriorly, although in some cases they do regenerate the asegmental prostomium and peristomium. Interestingly, this species reproduces asexually through paratomic fission, a process in which worms develop a new head and tail in the middle of the body to form transiently linked chains of individuals. Paratomic fission and regeneration appear to be based on very similar developmental programs (Bely and Wray 2001) and most fissiparous species have extensive regenerative abilities (Berrill 1952). P. litoralis appears to be an exception to this correlation, and demonstrates that regeneration abilities can be lost even in a species that retains asexual reproduction by fission. Although many naidines can regenerate anteriorly, preliminary evidence suggests that several additional naidines have lost the ability for anterior segment regeneration (A. E. Bely and J. M. Sikes, unpublished data).
The phylogenetic distribution of anterior segment regeneration across the phylum clearly suggests that this feature has been gained or lost multiple times in the annelids. Based on the fact that anterior regeneration ability appears to be far more common and widespread than lack of this feature, and the reasoning that losing regeneration ability is presumably easier (that is, more likely) than gaining this feature, it seems reasonable to posit that anterior regeneration ability is ancestral for the Annelida and has been lost multiple times. However, given the major questions regarding annelid phylogeny that remain unresolved (McHugh 2005) and the fact that no published data on anterior regeneration are available for many annelid families, it is too early to conclude this with certainty. In only a few cases, specifically the anteriorly non-regenerating S. benedicti and P. litoralis, are multiple close relatives known to regenerate, making these relatively clear cases of loss of regeneration.
Assuming that absences do indeed represent losses, anterior segment regeneration ability must have been lost on the order of at least a dozen times within annelids. Some of these losses are likely to be quite old, such as those represented by the leeches and possibly the Arenicolidae, Capitellidae, Dorvilleidae, Nereididae, Opheliidae, and Polynoidae. Others are probably very recent, perhaps involving only one or a few closely related species, such as the losses represented by M. infundibulum (Sabellidae), S. benedicti (Spionidae), and P. litoralis (Tubificidae). Investigations of recent losses will be particularly fruitful avenues for uncovering mechanisms underlying the evolution of regeneration abilities.
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Conclusions |
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SynopsisIntroductionAnnelids as a model...Presence/absence of segment...ConclusionsReferences |
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Annelid regeneration is clearly evolutionarily labile. While the ability to regenerate both anterior and posterior segments is widespread and probably ancestral for the phylum, data reviewed here highlight the fact that many species or groups appear to have lost one or both of these abilities. Losses are not phylogenetically restricted but rather are reported in all major subdivisions of annelids, namely the Scolecida, the Aciculata (Palpata), the Canalipalpata (Palpata), and the Clitellata. While many aspects of annelid phylogeny remain unresolved (McHugh 2005
), it seems likely that posterior segment regeneration has been lost at least four times and that anterior segment regeneration has been lost on the order of a dozen times within the annelids. Given that no published information on regeneration could be found for the majority of annelid families, it is very likely that there have been additional losses of segment regeneration ability beyond those indicated here. Comparative studies of regenerating and closely related non-regenerating species are needed to uncover the proximal developmental mechanisms and ultimate evolutionary explanations responsible for the loss or retention of regeneration abilities. Identifying non-regenerating species is also necessary for reconstructing an accurate picture of how regeneration ability has evolved within a group. For both these reasons there is a clear need to document the lack of regeneration in annelid species. Yet there is a publication bias against reporting the lack of regeneration abilities, highlighted by the fact that the source of information for almost all non-regenerating species in Tables 1 and 2 is unpublished data. Such data are not only unpublished but also are generally derived from incomplete studies of regeneration potential. Thus, rigorous and complete experimental studies are needed not only to identify new non-regenerating species but also to confirm the lack of regeneration ability in many of the candidates listed in Tables 1 and 2.
Identifying the factors correlated with or ultimately driving the loss of segment regeneration will require comparative analyses of independent losses, and preferably recent losses. Several possible correlates of regeneration loss already present themselves, however. First, while most annelids grow indeterminately, adding segments throughout life or well into the adult phase (Hyman 1940), a number of non-regenerating species exhibit segment constancy or an early cessation of post-embryonic segment addition. These include the arenicolid A. marina, opheliid polychaetes (including P. pictus), the polynoid H. imbricata, leeches, and branchiobdellidans (Rouse and Pleijel 2001; Brusca and Brusca 2003). While some groups that stop adding segments as adults can regenerate segments (for example, the Maldanidae), and some non-regenerating groups do add segments indeterminately, it may be that a disproportionate number of non-regenerating groups have a fixed number of segments as adults. Second, if amputation causes the loss of a structure critical to the survival of an organism, this could also lead to a loss of regeneration ability (Reichman 1984). Such may be the case for the anteriorly non-regenerating S. benedicti, which loses the critical branchiae of the first anterior segment if even just one head segment is lost (S. M. Lindsay and J. L. Jackson, unpublished data). In this species, the branchiae may be so critical for survival that animals die before being able to regenerate. Third, low amputation rates could also be expected to lead to loss of regeneration. This could be the case for species such as M. infundibulum, which has a very rapid head-withdrawal response mediated by its giant nerve fibers (Nicol 1948) and thus possibly a low frequency of anterior amputation in nature. And finally, although fissioning species tend to have high regeneration abilities (Berrill 1952), being able to fission may also decrease the selective advantage of regeneration (Bely 1999). This may be the case for P. litoralis, individuals of which can reproduce by fission even if they fail to regenerate anteriorly. Surely, multiple factors can drive the evolution of regeneration, and annelids hold great promise for identifying these factors rigorously through comparative analyses of independent losses of regeneration.
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Acknowledgements |
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I am grateful to Sara Lindsay, Sue Hill, Stuart Gelder, Maria Cristina Gambi, Gabriele Conti, Sally Woodin, Ron Abercrombie, Judy Grassle, Larry Goldman, and Maroko Myohara for generously sharing unpublished data and/or helpful discussions, and to Leo Shapiro and two anonymous reviewers for useful comments on the manuscript. I also thank Ken Halanych for the invitation to participate in this symposium; information gleaned during fruitful discussions at this meeting significantly broadened the scope of this review.
Conflict of interest: None declared.
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Footnotes |
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From the symposium "WormNet: Recent Advances in Annelid Systematics, Development, and Evolution" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, at San Diego, California.
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