Damhnait McHugh

A Biogeographical Perspective of the Deep-Sea Hydrothermal Vent Fauna

ABSTRACT Biogeography seeks to distinguish patterns in the distribution of species and to determine causal processes. Hydrothermal vent habitats have several properties that invite biogeographic studies: constrained to active deep-sea ocean ridges, known in most oceans and anticipated in the rest, patchy in distribution, extreme conditions and a limited group of inhabitants. Biologists have studied 30 vent sites mostly in the Pacific and Atlantic. Currently, 443 invertebrate species are known to generic level although many more are under study. Additionally, 32 octopus and fish species are observed in and around vents. The faunas of other sulphide-rich deep-water habitats such as margin cold seeps and organic masses (wood, carcasses) do not show great affinity at the species level to the vent fauna but the higher taxonomic affiliations suggest close evolutionary ties for many groups. Many studies address the formation of regional faunas using the first- known sites on the Galapagos Rift and northern East Pacific Rise as the major sites of comparison. Physical disjunction of ridge crests is a likely factor in promoting the extensive provinciality that currently exists. Nonetheless, faunas on two sides of the Pacific and in the Atlantic have closer relations to each other than to the nearby “normal” deep-sea fauna. At the individual ridge scale, extensive gene flow among separated populations occurs in many species and serves to maintain the regional species pool. However, major discontinuities between major ridges reduce or eliminate gene flow; vicariant processes appear to be important. The role of differing rates of spreading in different provinces and the concomitant effects on vent habitats and faunas need further investigation. Over 75% of vent species occur at only one site and none occur at all sites. Examination of the reproductive characters of some widespread species reveals no special dispersal strategy nor does reproductive strategy predict the extent of distribution. Vestimentiferan tubeworm species are highly endemic and found only at Pacific vents; their limited spread may be a result of recent entry into the habitat. Alvinellid polychaete cladogenetic pattern does not match geographic regions, indicating independent penetration by numerous lineages. Endemicity among vent gastropods is high with over 60% of genera limited to this habitat; many affiliations with other sulphide-rich habitats can be identified. Among the vent gastropods there are some lineages that may have entered the vent habitat in the Mesozoic. Hydrothermal vents provide a good testing ground for processes that control patterns in diversity. Ecological and historical controls at both local and regional scales can be discerned with further study.

Systematization of the Annelida: different approaches

Different approaches and different data sets are used to address questions about the phylogenetic relationships of the polychaete family taxa, the position of the Clitellata, the monophyletic nature of the Polychaeta and the Annelida, as well as the position of the Pogonophora and Echiura. In part, the authors of this contribution come to different conclusions regarding these questions: (1) The analysis of G. W. Rouse minimizes assumptions about any process concerning evolution in annelids and makes a detailed series of homology assessments, based on morphology, across the entire range of taxa concerned. A monophyletic taxon Polychaeta is found but there is no evidence of a sister group for the Clitellata among the polychaetes. The Pogonophora are positioned as members of the Polychaeta. A new classification of the polychaete families is provided. Problems with coding morphology for cladistic analysis are outlined and discussed. (2) D. McHugh uses the sequence of a nuclear gene, elongation factor-1α, for phylogenetic analysis by the parsimony and neighbour joining methods. The main message from phylogenetic analyses of molecular data is that there is no evidence for a monophyletic Polychaeta; instead, placement of the clitellates, pogonophorans and echiurans within the polychaete clade is supported, rendering the Polychaeta paraphyletic. (3) The phylogenetic system of W. Westheide and G. Purschke is based on Hennigian reasoning, and their character weighting is based on diverse, mainly functional considerations. Their annelid tree shows the Clitellata as a highly evolved monophylum and the polychaetes as paraphyletic. Special emphasis is placed on the demonstration that the Clitellata are of terrestrial origin. Advantages and disadvantages of the different approaches and open questions are discussed.

Myzostomida: a link between trochozoans and flatworms?

Myzostomids are obligate symbiotic invertebrates associated with echinoderms with a fossil record that extends to the Ordovician period. Due to their long history as host–specific symbionts, myzostomids have acquired a unique anatomy that obscures their phylogenetic affinities to other metazoans: they are incompletely segmented, parenchymous, acoelomate organisms with chaetae and a trochophore larva. Today, they are most often classified within annelids either as an aberrant family of polychaetes or as a separate class. We inferred the phylogenetic position of the Myzostomida by analysing the DNA sequences of two slowly evolving nuclear genes: the small subunit ribosomal RNA and elongation factor–1α. All our analyses congruently indicated that myzostomids are not annelids but suggested instead that they are more closely related to flatworms than to any trochozoan taxon. These results, together with recent analyses of the myzostomidan ultrastructure, have significant implications for understanding the evolution of metazoan body plans, as major characters (segmentation, coeloms, chaetae and trochophore larvae) might have been independently lost or gained in different animal phyla.

Life history evolution of marine invertebrates: New views from phylogenetic systematics

Established theories on the evolution of the diverse life histories of marine metazoans, specifically invertebrates, were developed in the absence of rigorous phylogenetic methods. With improved estimates of evolutionary relationships for various marine invertebrate groups, based on phylogenetic systematics, we can now critically evaluate the assumptions upon which these theories are based. Several studies emphasizing a phylogenetic systematics approach have recently examined the evolutionary transitions among reproductive traits and challenge us to reconsider the generality of the assumptions made about life history evolution. The results point towards exciting possibilities for a better understanding of the great diversity of reproductive and developmental modes we observe in marine invertebrates today.

Unsegmented Annelids? Possible Origins of Four Lophotrochozoan Worm Taxa

Abstract In traditional classification schemes, the Annelida consists of the Polychaeta and the Clitellata (the latter including the Oligochaeta and Hirudinida). However, recent analyses suggest that annelids are much more diverse than traditionally believed, and that polychaetes are paraphyletic. Specifically, some lesser-known taxa (previously regarded as separate phyla) appear to fall within the annelid radiation. Abundant molecular, developmental, and morphological data show that the Siboglinidae, which includes the formerly recognized Pogonophora and Vestimentifera, are derived annelids; recent data from the Elongation Factor-1α (EF-1α) gene also suggest that echiurids are of annelid ancestry. Further, the phylogenetic origins of two other lesser-known groups of marine worms, the Myzostomida and Sipuncula, have recently been called into question. Whereas some authors advocate annelid affinities, others argue that these taxa do not fall within the annelid radiation. With advances in our understanding of annelid phylogeny, our perceptions of body plan evolution within the Metazoa are changing. The evolution of segmentation probably is more plastic than traditionally believed. However, as our understanding of organismal evolution is being revised, we are also forced to reconsider the specific characters being examined. Should segmentation be considered a developmental process or an ontological endpoint?

Molecular systematics of polychaetes (Annelida)

Some progress has been made in the field of molecular systematics of polychaetes over the past couple of years. In particular, phylogenetic analyses of sequence data from the 18S rRNA gene have included increasing numbers of taxa, and explicit hypothesis testing of sister-group relationships is being incorporated into the most recent studies. An increasing number of analyses of relationships within polychaete groups are being undertaken, with specific inferences being drawn regarding the evolution of characters such as reproductive mode. Despite this progress, the unanswered questions regarding annelid relationships outlined by McHugh (2000, p. 1881) remain: “what are the relationships among the polychaete annelids, what group is sister to the Clitellata, what extant group is most basal on the annelid tree, and what group is sister to Annelida?” Continued expansion of taxon sampling and further combined investigation of conserved nuclear coding genes, in conjunction with rRNA genes, may help to resolve some of these issues. Furthermore, only by expanding molecular systematic studies of polychaetes to analyses of nuclear coding genes for comprehensive taxon samples will it become clear whether the lack of basal-node resolution observed in analyses of 18S rRNA reflects a rapid radiation of the group, or is a feature associated with the 18S rRNA gene itself. Genomic-level data (e.g., mitochondrial gene order) may also be informative, and the cautious use of gene copies in phylogenetic analyses may point to a root of the annelid tree.

A Comparative Study of Reproduction and Development in the Polychaete Family Terebellidae

The reproduction and development of four species of terebellid polychaetes from the west coast of North America were studied and compared with several other terebellid species to reveal the covariation of life history traits in the group, and assess any limitations on terebellid life history evolution that may be imposed by ancestry or body design. The four species in the present study span the range of reproductive and developmental modes known for the family Terebellidae. Eupolymnia crescentis and Neoamphitrite robusta are both free spawners that reproduce during discrete 3-month breeding periods. In E. crescentis, oogenesis takes from 5 to 8 months and spawning occurs from July to September, maximum oocyte diameter is 210 {mu}m, and fecundity reaches {approx}128,500 during a single breeding period. The E. crescentis larva develops near the bottom for about 7 days before settling as a five-setiger juvenile. Neoamphitrite robusta reproduces from April to July after a 12-month oogenic cycle; oocytes in this species measure up to 180 {mu}m, and fecundity reaches ~830,000. The two brooders in the study, Ramex californiensis and Thelepus crispus, brood their larvae in the maternal tube. T. crispus reproduces continuously for at least 6 months, and has up to 51,500 larvae in a single brood. The oocytes in this species (400 {mu}m) give rise to larvae that are brooded to the one-setiger stage and then emerge to undergo a one-day planktonic period before the larvae settle and become juveniles at eight setigers. Ramex californiensis reproduces continuously year round; larvae are brooded in cocoons that are laid sequentially in the tube, with up to 44 larvae in a single cocoon. Development from the 410 {mu}m oocytes is direct, and juveniles have 11 setigers. Unlike E. crescentis and N. robusta, in which oogenesis is synchronized within individuals to produce a peak of large oocytes during the discrete spawning period, R. californiensis and T. crispus females have a wide range of oocyte sizes throughout the year. Correlation analysis and analysis of variance of reproductive and developmental traits of these and several other terebellid species revealed some expected trends. For example, egg size varies according to the mode of reproduction (free spawning, extratubular brooding, or intratubular brooding), and is also correlated with juvenile size. However, egg size does not predict fecundity in terebellids when body size is held constant, and brooding is not restricted to small-bodied species. Indeed, the largest and smallest species in the study brood their larvae intratubularly, suggesting that allometric constraints may not be important in determining mode of reproduction in these polychaetes. The Terebellidae is a diverse family found in all marine habitats, yet all known terebellid larvae are non-feeding; this contrasts with the occurrence of both planktotrophy and lecithotrophy in other polychaete families, and leads to the proposal that larval development in terebellids has been constrained during the evolution of the lineage. The results of this study demonstrate that generalizations regarding complex relationships among life history traits are often inappropriate. The need for more comparative studies of marine invertebrate reproduction and development, and the integration of phylogenetic analyses into the study of life history evolution in marine invertebrates is highlighted.

Introduction to Symposium: Poecilogony—A Window on Larval Evolutionary Transitions in Marine Invertebrates

Poecilogony is the intraspecific variation in developmental mode that has been described in some marine invertebrates. Poecilogonous species produce different larval forms (e.g., free-swimming planktotrophic larvae as well as brooded lecithotrophic or adelphophagic larvae). Poecilogony can be a controversial topic, since it is difficult to identify and characterize the phenomenon with certainty. It has been challenging to determine whether poecilogony represents developmental polymorphism with a genetic basis or developmental polyphenism reflecting plastic responses to environmental cues. Other outstanding questions include whether common mechanisms underlie the developmental variation we observe in poecilogonous species, and whether poecilogony is maintained in different taxa through similar mechanisms or selective pressures. Poecilogonous species provide a unique opportunity to elucidate the cellular, developmental, and genetic mechanisms underlying evolutionary transitions in developmental mode, as well as to help clarify the selective pressures and possible ecological circumstances that might be involved. Here, we describe an integrative approach to the study of poecilogony and its role in larval evolutionary transitions highlighted during a symposium held at the 2012 annual meeting of the Society for Integrative and Comparative Biology.

Transcriptome analysis and SNP development can resolve population differentiation of Streblospio benedicti, a developmentally dimorphic marine annelid.

Next-generation sequencing technology is now frequently being used to develop genomic tools for non-model organisms, which are generally important for advancing studies of evolutionary ecology. One such species, the marine annelid Streblospio benedicti, is an ideal system to study the evolutionary consequences of larval life history mode because the species displays a rare offspring dimorphism termed poecilogony, where females can produce either many small offspring or a few large ones. To further develop S. benedicti as a model system for studies of life history evolution, we apply 454 sequencing to characterize the transcriptome for embryos, larvae, and juveniles of this species, for which no genomic resources are currently available. Here we performed a de novo alignment of 336,715 reads generated by a quarter GS-FLX (Roche 454) run, which produced 7,222 contigs. We developed a novel approach for evaluating the site frequency spectrum across the transcriptome to identify potential signatures of selection. We also developed 84 novel single nucleotide polymorphism (SNP) markers for this species that are used to distinguish coastal populations of S. benedicti. We validated the SNPs by genotyping individuals of different developmental modes using the BeadXPress Golden Gate assay (Illumina). This allowed us to evaluate markers that may be associated with life-history mode.

Evolutionary changes in the timing of gut morphogenesis in larvae of the marine annelid Streblospio benedicti

SUMMARY The planktonic larvae of marine invertebrates are diverse in their nutritional modes, suggesting that evolutionary transitions in larval nutritional mode have been frequent. One approach to identifying the developmental changes that play important roles in such transitions is to compare “intermediate” larval forms to closely related larvae representative of their common ancestor. Here we make such a comparison between obligately planktotrophic and facultatively feeding larvae of the poecilogonous polychaete annelid Streblospio benedicti. We used feeding experiments to show that the derived, facultatively feeding larvae of this species develop the ability to feed at a later developmental stage (five muscle bands) than planktotrophic larvae (two to three muscle bands). This delay in the onset of feeding ability does not appear to be caused by delay in the formation of particle capture structures, but instead by delay in the development of a continuous, functional gut. These observations are consistent with the hypothesis that evolutionary increases in egg size in annelids lead predictably to heterochronic delays in gut development, and hence to transitions in larval nutritional mode.