Biol. Bull. 208: 213-220. (June 2005)
© 2005 Marine Biological Laboratory
Holopelagic Poeobius meseres ("Poeobiidae," Annelida) Is Derived From Benthic Flabelligerid Worms
Adriene B. Burnette,
Torsten H. Struck and
Kenneth M. Halanych*
Auburn University, Department of Biological Sciences, Auburn, AL 36830, USA
* To whom correspondence should be addressed. E-mail:ken{at}auburn.edu
 |
Abstract
|
|---|
Phylogenetic relationships among and within the more than 70 recognized families of Annelida are poorly understood. In some cases, such as the monotypic Poeobiidae, derived morphology hinders the ability to find convincing synapomorphies that help elucidate evolutionary origins. In such cases, molecular data can be useful. Poeobiidae consists of the holopelagic polychaete Poeobius meseres, which is typically found in midwater depths off California. Morphologists have speculated that it is close to or within Flabelligeridae, but definitive evidence was lacking. Herein we use maximum likelihood phylogenetic reconstruction methods to examine the nuclear 18S rDNA (SSU) gene and the mitochondrial cytochrome b gene. Our results strongly support the hypothesis that P. meseres is a highly derived flabelligerid annelid closely related to Therochaeta. Thus, Poeobiidae is a junior synonym for Flabelligeridae. This result raises interesting questions about the evolution of the holopelagic P. meseres from a benthic ancestral flabelligerid.
|
Introduction
|
|---|
The holopelagic polychaete Poeobius meseres, which is up to 27 mm in length and has 11 poorly defined segments, is the sole recognized representative of Poeobiidae (Annelida; Fig. 1). It has been recorded from the eastern Pacific at depths of 350–1300 m (Rouse and Pleijel, 2001). The body is largely gelatinous with a thick mucus sheath, and segmentation is not clearly visible. The anterior end bears retractable pale green "tentacles," which consist of a pair of grooved palps and branchiae. Individuals of this species can be overlooked when taken because they are easily damaged by net tows and are amorphous out of water. However, some aspects of their biology are known (e.g., metabolism—Thuesen and Childress, 1993; diet—Uttal and Buck, 1996). A second species, Enigma terwillei, has been attributed to Poeobiidae (Rouse and Pleijel, 2001), but it has only been collected once and the type material was lost. Therefore, it should be considered incertae sedis (of uncertain taxonomic position) as suggested by Fauchald (1977). The evolutionary origins of P. meseres are unclear, but there is speculation of a relationship to or within Flabelligeridae.
View larger version (25K):
[in this window]
[in a new window]
|
Figure 1. Individual of Poeobius meseres floating in the water column. Photo credit: MBARI ROV Tiburon and Karen Osborn.
|
|
Flabelligeridae, known as bristle-cage worms, contains about 130 species in 14 recognized genera. These occupy many habitats ranging from intertidal zones to deep-sea muds, and are from 5 mm to 220 mm in length (Rouse and Pleijel, 2001). Members of Flabelligeridae are typically recognized by their unique and complex anterior end. The prostomium and peristomium are fused, forming a retractable head that in most cases (e.g., Flabelligera, Pherusa, and Diplocirrus) is protected by a cage of modified setae from the first few parapodia (Spies, 1975; Blake, 2000). The body is often coated with sediment granules or a mucus sheath (Fauchald and Rouse, 1997).
Information on flabelligerid biology is limited. Spies (1977) found that Flabelligera commensalis retains gametes in the coelomic peritoneum until just before spawning. For comparison, many polychaetes shed their gametes directly into the coelom to mature. Studies of flabelligerid and P. meseres larvae are lacking (but see Spies, 1977). Some flabelligerids (e.g., Flabelligera affinis) are motile surface-deposit feeders, whereas most others (e.g., Pherusa plumosa and Brada villosa) are discretely motile, feeding in cracks and crevices (Fauchald and Jumars, 1979). Grooved palps and current-generating branchial fields are thought to be used in feeding (Fauchald and Jumars, 1979). Flabelligerids have a fossil record from about 295 million years ago in the Francis Creek Shale of Illinois (Carbondale Formation, Desmoinesian Series, Middle Pennsylvanian System of North America; Hay, 2002). Fossils have been placed into one species, Mazopherusa prinosi, which is most similar to the extant Pherusa on the basis of the cephalic cage. One additional worm that deserves mention is Flota flabelligera, another pelagic polychaete. Hartman (1967) initially considered it a flabelligerid, but she later transferred it to Fauveliopsidae (1971). Recently, Flota has been considered to be closely related to taxa in Terebellida and especially to Poeobius (Rouse and Pleijel, 2001, 2003). Under the Linnean system, Flota is still considered a separate family. Neither F. flabelligera nor P. meseres is known to have a fossil record.
To our knowledge, a formal phylogenetic hypothesis has never been proposed for relationships within Flabelligeridae. The first flabelligerid (Amphitrite plumosa, now Pherusa plumosa) was formally described in 1776 by Müller, and the family was erected in 1894 by Saint-Joseph. The current taxonomic scheme for the group is based largely on the works of Haase (1915), Fauvel (1927), Støp-Bowitz (1948), Day (1961, 1967), and Hartman (1961, 1969). Recent morphological cladistic analyses (Rouse and Fauchald, 1997; Rouse and Pleijel, 2001) place Flabelligeridae within Cirratuliformia, Terebellida, and Canalipalpata. Relationships within this putative clade (also including Acrocirridae, Cirratulidae, Ctenodrilidae, Fauveliopsidae, Poeobiidae, and Sternaspidae) remain unclear.
With the recognition of Poeobiidae Heath 1930, the monophyly of Flabelligeridae has been called into question. There are morphological similarities between these two groups, such as the presence of a retractable head, a pair of grooved palps, an anterior ring of branchiae, and a gelatinous mucus sheath, although some of these features are not exclusive to these taxa. Fauchald and Jumars (1979) also thought that these two groups belong to the same feeding guild—filter-feeding, discretely motile, tentacular—because the palps of Poeobiidae resemble those of flabelligerids. P. meseres was originally thought by Heath (1930) to be the link between the Annelida and "Echiuroidea," but later Pickford (1947, cited in Robbins, 1965) labeled it an aberrant polychaete. Hartman (1955) first pointed out the remarkable resemblance P. meseres has to flabelligerids—for example, the cephalic structure and the thick gelatinous membrane around the trunk region. Dales (1962) considered P. meseres to be an offshoot of the flabelligerids, leading Robbins (1965) to suggest that the relationship between Flabelligeridae and P. meseres be assessed in detail due to morphological similarities. Rouse and Fauchald’s (1997) morphological cladistic analysis consistently placed Flabelligeridae closer to Fauveliopsidae and Sternaspidae than to Poeobiidae. Later, Rouse and Pleijel (2003) suggested that the recognition of Poeobiidae renders Flabelligeridae paraphyletic by presenting a strict consensus tree in which Poeobius and Flota are nested among three flabelligerid taxa (Brada, Pherusa, and Flabelligera). They present an anterior branchial cluster as the only non-homoplastic morphological apomorphy to support the Poeobius/Flota/flabelligerid clade. Rouse and Pleijel acknowledge that "the exact nature of ...[the extreme anterior branchial cluster] is still unresolved" (p. 181), and given that several other polychaete taxa have anterior branchiae/palps/tentacles, the nature of this apomorphy is tenuous. Furthermore, their analysis fails to assess the robustness of their recovered topologies over alternative hypotheses. Thus, the question of whether P. meseres falls within Flabelligeridae is still open to debate.
The purpose of this study is to examine the position of P. meseres. In doing so, we hope to begin examining relationships within Flabelligeridae. We examined data from two molecular markers, 18S rDNA and cytochrome b, using maximum likelihood. Our phylogenetic results will allow us to look for changes that accompany the transition from a benthic to a holopelagic mode of life.
|
Materials and Methods
|
|---|
Specimens
The taxa sampled in this study, their collection locality, voucher specimen number, and GenBank numbers are listed in Table 1. Limited taxon sampling in this study was due to the difficulty in obtaining samples from deeper waters. Three outgroups, Sternaspis sp., Fauveliopsis glabra, and Cirratulus spectabilis were chosen on the basis of recent studies (Rouse and Fauchald, 1997; Rouse and Pleijel, 2001). All specimens were stored at –80° C or at 4 °C in ethanol immediately after collection. For most specimens, species identification was made at the time of collection and subsequently confirmed by Sergio Salazar-Vallejo (Unidad Chetumal, Mexico). Fredrik Pleijel identified the three specimens that he kindly provided (Table 1). Herein we have decided to follow the taxonomy of Blake (2000). However, Salazar-Vallejo has noted that both Brada villosa and Fabelligera affinis may be over-synonymized. He mentioned that, given the older literature, the following designations are probably correct and may be re-erected in the near future: our Brada villosa 1 = B. pluribranchiata and our Flabelligera affinis 1 = F. infundibularis. Also B. villosa from Norway is probably referable to B. pilosa. Voucher specimens have been deposited in the Smithsonian Museum of Natural History (Washington DC).
Data collection
For most tissues, DNA was extracted using the DNeasy Tissue Extraction Kit (Qiagen, Valencia, CA) according to the manufacturer’s protocol. However, for Poeobius meseres, a standard phenol/chloroform with proteinase K extraction procedure was used (Hillis et al., 1996). The 18S rDNA gene and approximately 420 basepairs of the cytochrome b (cyt b) mitochondrial gene were amplified and sequenced using the primers listed in Table 2. Amplification via HotStart-PCR of 18S (thermocycler profile: 3 min 94 °C; addition of polymerase; 3 min 94 °C; 40 cycles: 1 min 94 °C, 1 min 30 s 40 °C, 2 min 30 s 72 °C; 1 cycle: 7 min 72 °C; reaction-mix: 10 mM Tris-HCl pH 9.0, 50 mM KCl, 0.1% Triton X-100, 2.5 mM MgCl2, 
1 ng/µl genomic DNA, 0.4 mM dNTPs, 0.8 µM of each primer, 0.03 U/µl Taq DNA Polymerase (Promega, Madison, WI)) was carried out in a volume of 25 µl. The cyt b protocol used the same recipe but a different thermocycling protocol (3 min 94 °C; addition of polymerase; 2 min 94 °C; 15 cycles: 30 s 94 °C, 30 s 42 °C, 30 s 72 °C; 20 cycles: 30 s 94 °C, 30 s 37 °C, 45 s 72 °C; 1 cycle: 7 min 72 °C). PCR products were isolated on 1% agarose gels. The appropriate-sized bands were excised and purified using the QIAquick Gel Extraction Kit (Qiagen, Valencia, CA). Purified products were quantified using a mass standard on 1% agarose gels. Bi- directional Sequences were determined on an ABI Prism 3100 (using the BigDye ver. 3.0 kit, Applied Biosystems, Foster City, CA) or a Beckman CEQ 8000 (using one-half reactions of the CEQ DTCS Quick Start Kit, Beckman Coulter, Fullerton, CA).
Sequences were assembled and edited using the LaserGene package (DNAStar, Inc., Madison, WI). The sequences were then aligned using ClustalX (Thompson et al., 1997). The alignment was corrected by eye in MacClade ver. 4.06 (Maddison and Maddison, 2003). Regions of the 18S data that could not be unambiguously aligned were excluded from the analyses. The cyt b alignment was translated to inferred amino acid sequence using the Drosophila mitochondrial DNA code to check for sequencing errors. Alignments (Accession #S1268 and #M2212-2214) are available at TREEBASE (www.treebase.org).
Phylogenetic analysis
Phylogenetic analyses used maximum likelihood (ML) methods for both data sets individually and for combined data. For cyt b, nucleotide data with and without third positions were analyzed. Combined analyses used cyt b without third positions. ML analyses with a heuristic search of 100 random sequence addition replicates and tree-bisection-reconnection (TBR) were conducted using PAUP* 4.0b10 (Swofford, 2002). ModelTest 3.06 (Posada and Crandall, 1998) was used to select the model of evolution with the best fit for each data set (see below). Nodal support was estimated using a bootstrap analysis consisting of 1000 heuristic iterations with random sequence addition.
In addition, using MrBayes (Huelsenbeck and Ronquist, 2001), we conducted a Bayesian inference analysis on the inferred amino acid data to determine if there was additional phylogenetic information in the cyt b data. To do this, we inferred amino acid residues using the Drosophila mtDNA translation code. The Bayesian search employed the amino acid model with all the priors set to default settings. Two million generations were run with four chains (3 cold and 1 hot) that were sampled every 200 generations.
The constraints option within an ML heuristic search (as above) was used to generate topologies consistent with alternative hypotheses. Resultant trees were compared with unconstrained ML results using the Shimodaira-Hasegawa test (Shimodaira and Hasegawa, 1999) implemented in PAUP* 4.0b10. Only the 18S data set was used because multiple outgroups allowed for testing the monophyly of Flabelligeridae, including P. meseres.
|
Results
|
|---|
The 18S rDNA data set included 13 terminal taxa and 2106 characters. Of the 1474 nucleotide positions that could be unambiguously aligned, 28.1% (414 positions) were variable and 18.3% (270 positions) were parsimony informative. ModelTest indicated a TrNef+
model (nucleotide frequencies equal; rates A
C 1.0000, AG 2.2477, AT 1.0000, CG 1.0000, CT 3.6285, GT 1.000; gamma shape parameter = 0.2552) for the ML analysis. The single best ML tree (Ln likelihood = –6283.79641) is shown in Figure 2. A monophyletic Flabelligeridae clade including Poeobius meseres was recovered with a bootstrap value of 100%. Specifically, P. meseres falls as a sister taxon to Therochaeta collarifera (bootstrap 100%). The result that Ilyphagus octobranchus appears to be very closely related to Diplocirrus glaucus (bootstrap = 98%) is noteworthy.
View larger version (27K):
[in this window]
[in a new window]
|
Figure 2. The single best 18S maximum likelihood tree (Ln likelihood = –6283.79641) based on 18SrDNA data set (see text for details). Bootstrap support values (>50%) out of 1000 iterations are represented at each node.
|
|
The cytochrome b nucleotide data set consisted of 11 terminal taxa and 404 characters; the number of characters was reduced to 318 once the ends were trimmed. Of those, 57.2% (182 positions) were variable and 42.1% (134 positions) were parsimony informative. ModelTest indicated a TVM + + I model (nucleotide frequencies A = 0.28290, C = 0.24680, G = 0.09230, T = 0.37800; rates AC 3.3592, AG 34.9373, AT 15.4450, CG 8.4295, CT 34.9373, GT 1.000; proportion of invariant sites = 0.3275; gamma shape parameter = 0.9565) for this analysis. When third positions were included, a single best ML tree (Ln likelihood = –2157.13859) placed P. meseres within Flabelligeridae, but there was only weak (50%) bootstrap support (not shown). However, third positions appeared saturated because 94.3% (100 of 106 positions) of them displayed variation. Therefore, an ML analysis minus the third position was also performed, using a K81uf + model with nucleotide frequencies A = 0.24400, C = 0.22550, G = 0.15250, T = 0.37800, rates AC 1.0000, AG 5.2849e+06, AT 2.0229e+06, CG 2.0229e+06, CT 5.2849e+06, GT 1.000, and gamma shape parameter = 0.2079. This tree (Ln likelihood = –962.14976; Fig. 3A) also grouped P. meseres with Therochaeta collarifera, but with a low bootstrap value (62%). As in the 18S analysis, Ilyphagus octobranchus and Diplocirrus glaucus are sister taxa, but with a bootstrap support less than 50%. Similarly, the Bayesian analysis of the amino acid data was poorly supported. Thus, for the sake of simplicity, that analysis is not described herein.
View larger version (16K):
[in this window]
[in a new window]
|
Figure 3. (A) The single best maximum likelihood tree (Ln likelihood = –962.14976) based on the cyt b nucleotide data set minus third positions (see text for details). (B) The single best maximum likelihood tree (Ln likelihood = –5810.60410) based on a combined data set of 18SrDNA and cyt b minus third positions (see text for details). For both trees, bootstrap support values (>50%) out of 1000 iterations are represented at each node.
|
|
For the cyt b dataset, the percent divergence of the European and North American Pherusa plumosa is notable (10.8% for uncorrected distance). Further analysis is needed to assess whether the current nomen "Pherusa plumosa" represents multiple species.
The combined dataset consisted of 10 taxa with 2424 nucleotide characters. When ambiguously aligned positions and cyt b third positions were excluded (1687 nucleotides remaining), 28.1% (474 positions) were variable and 14.5% (245 positions) were parsimony informative. Because of data availability, only one outgroup (Cirratulus spectabilis) was used, accounting for the lower number of variable sites when compared to the 18S dataset. The model for the combined data was a GTR + + I using the following parameters: nucleotide frequencies A = 0.26400, C = 0.21870, G = 0.25330, T = 0.26400; rates AC 1.2605, AG 2.4146, AT 3.2160, CG 0.7243, CT 7.5504, GT 1.000; proportion of invariant sites = 0.393; gamma shape parameter = 0.5704. Given the absence of Fauveliopsis glabra, Sternaspis sp., and Flabelligera affinis, the topology of the combined data tree (Ln likelihood = –5810.60410; Fig. 3B) was identical to the 18S results, with a monophyletic Flabelligeridae including P. meseres as sister to Therochaeta collarifera. There was also strong support for Ilyphagus octobranchus with Diplocirrus glaucus (bootstrap = 92%).
Table 3 presents Shimodaira-Hasegawa results of the hypotheses tested. The alternative hypotheses that P. meseres is neither a flabelligerid ingroup taxon nor the sister taxon of Therochaeta collarifera are significantly worse than the best hypothesis. However, the hypothesis that Ilyphagus octobranchus and Diplocirrus glaucas are not sister taxa to each other is not significantly worse than the best tree.
|
Discussion
|
|---|
All analyses described herein are consistent with placement of the holopelagic Poeobius meseres within Flabelligeridae, and specifically as sister taxon to Therochaeta collarifera. Even though only about half (6) of the recognized flabelligerid genera are included in our study, support that P. meseres is within the Flabelligeridae is very strong on the basis of bootstrap proportions (100%) and a Shimodaira-Hasegawa test (P < 0.001). Morphological studies suggest that P. meseres falls within or close to the flabelligerids (Hartman, 1955; Robbins, 1965; Rouse and Fauchald, 1997; Rouse and Pleijel, 2001, 2003; S. Salazar-Vallejo, Unidad Chetumal, Mexico, pers. comm.). Because of the agreement in morphological and molecular data, we formally propose that Poeobius meseres be referred to Flabelligeridae Saint-Joseph, 1894. This action makes "Poeobiidae" (Heath, 1930) a junior synonym of Flabelligeridae Saint-Joseph, 1894.
Two additional holopelagic worms, Enigma terwillei and Flota flabelligera, deserve mention in making this placement of P. meseres. First, as stated earlier, E. terwillei should be considered incertae sedis. However, if the initial and only description was accurate, it should also be referred to Flabelligeridae in the spirit of Rouse and Pleijel (2003). Second, although the suggestion that Flota is closely related to Poeobius (Rouse and Pleijel, 2003) awaits confirmation by definitive synapomorphies or a well-supported phylogenetic hypothesis, if it is correct, we must consider the possibility that there has been a radiation of holopelagic forms within Flabelligeridae.
The placement of P. meseres within Flabelligeridae is evolutionarily interesting because it suggests that this holopelagic species evolved from a benthic form. A notable change that presumably accompanied this transition was a reduction in thickness of the body wall that allowed P. meseres to be largely transparent. Many animals have transparent planktonic forms in which subcellular structures are arranged to reduce their reflectivity and scattering of light (Johnsen, 2001). For example, many transparent organisms cover the external surface with microscopic protrusions to reduce reflectivity. "Extracellular tissues" also help to lower scattering. On the basis of Johnsen’s work, we predict that similar subcellular rearrangement will be observed in P. meseres.
The evolutionary origins of P. meseres may be the result of heterochrony during development. Although little is known about larval development in most flabelligerids, Spies (1977) investigated Flabelligera commensalis and concluded that there was evidence for midwater spawning. During the 11-setiger stage of F. commensalis, bristles form on the anterior end, and development of adult setae progresses from the anterior to the posterior. Additionally, F. commensalis has feeding larvae (Spies, 1977). How much similarity exists between the adult form of P. meseres and, for example, a larval stage of Therochaeta is not clear, and more complete larval and developmental studies need to be completed. Nonetheless, what is known is suggestive of heterochrony, specifically progenesis. P. meseres, in the transition from a benthic to a pelagic form, has lost all obvious external segmentation, including setae. Hartman (1955) observed that the only evidence of segmentation is the midventral ganglia with 11 apparent segments (see also Heath, 1930). If the development of F. commensalis can be generalized to other flabelligerids, then the ancestor of Poeobius may have been a benthic flabelligerid with midwater spawning and relatively late development of setae (i.e., at or after the 11-setiger stage). Given a feeding larvae as seen in F. commensalis, then selective forces favoring a prolonged planktonic stage (e.g., lower risk of predation than metamorphosed juveniles, more consistent food supply, better opportunity to encounter mates) could have easily favored the evolution of a Poeobius-like organism.
Among annelids, there are presumably other examples of transition from benthic to pelagic form; these include Flota, alciopids, lopadorhynchids, isopilids, Pontodora, typhloscolecids, and tomopterids. All of these forms have retained segments with well-developed parapodia. Most of them are presumed to be active swimmers in the water column. These attributes are characteristic of Phyllodocida, the major annelid clade in which these taxa are placed (except Flota; Rouse and Pleijel, 2001). Because we do not understand the exact phylogenetic placement of these groups, it is hard to hypothesize the mechanism by which they evolved a holopelagic lifestyle. Although progenesis cannot be ruled out, some of these organisms may have evolved directly from an adult form (e.g., tomopterids). In the case of P. meseres, the lack of adult structures argues for a larval origin.
Even though cyt b data are largely unresolved, 18S provides information that allows us to begin to address flabelligerid systematics. Ilyphagus groups with Diplocirrus, a result consistent with observed morphology (Hartman, 1965; S. Salazar-Vallejo, pers. comm.). Furthermore, these taxa displayed the lowest cyt b intergeneric divergence values (7.08%, range of others 9.0%–19.3%) within Flabelligeridae. In the Shimodaira- Hasegawa tests, the best tree that did not have Ilyphagus octobranchus and Diplocirrus glaucus as sister taxa made them a polytomy rather than splitting them apart. This may explain the disparity between high bootstrap support and a nonsignificant Shimodaira- Hasegawa value. To better elucidate the relationships within Flabelligeridae, we are currently working on obtaining a wider representation of taxa for molecular analyses.
We had hoped that the combination of a more conserved gene (18S) and a more quickly evolving gene (cyt b) would provide phylogenetic information at several levels. Unfortunately, cyt b seems to provide little information at either the nucleotide or amino acid levels. For the question at hand, synonymous positions have apparently experienced saturation by multiple mutations, thereby obliterating the phylogenetic signal, and the nonsynonymous positions have not changed enough to record shared history. This situation has been reported previously in cyt b (Halanych and Robinson, 1999). The only other polychaete paper that we know to have employed cyt b for evolutionary history is Breton et al. (2003), but those authors used mainly third positions to infer history within a species in a phylogeographic context. Cyt b was not useful in our study, but it has potential for being a useful phylogentic marker, and we would encourage others to explore the gene in other annelid groups.
In summary, our results provide strong support for placement of P. meseres within a monophyletic Flabelligeridae. Thus, "Poeobiidae" (Heath, 1930) is an invalid name because it is a junior synonym to Flabelligeridae Saint-Joseph, 1894.
|
Acknowledgments
|
|---|
The crews of the R/V Point Sur and R/V Oceanus were most helpful in obtaining samples. For both cruises, we also acknowledge the help of the scientific crews (which are too numerous to list here). We are grateful for research support at Friday Harbor Laboratories, University of Washington. Fredrik Pleijel kindly provided samples, and Karen Osborn helped with the figures. Early drafts of this paper were greatly improved by discussion with Sergio Salazar-Vallejo. Constructive comments from Jim Blake, an anonymous reviewer, and a not-so- anonymous reviewer were most helpful. This work was supported by the WormNet grant (EAR-0120646) from the National Science Foundation to KMH. This work is AU Marine Biology contribution #1.
|
Footnotes
|
|---|
Received 17 September 2004; accepted 22 February 2005.
|
Literature Cited
|
|---|
Blake, J. A. 2000. Family Flabelligeridae Saint Joseph, 1894. Pp. 1–23 in Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel. Volume 7 - The Annelida Part 4, Polychaeta: Flabelligeridae to Sternaspidae, J. A. Blake, B. Hilbig, and P. V. Scott, eds. Santa Barbara Museum of Natural History, Santa Barbara, CA.
Boore, J. L., and W. M. Brown. 2000. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol. Biol. Evol. 17: 87–106.[Abstract/Free Full Text]
Breton, S., F. Dufresne, G. Desrosier, and P. U. Blier. 2003. Population structure of two northern hemisphere polychaetes, Neanthes virens and Hediste diversicolor (Nereididae), with different life-history traits. Mar. Biol. 142: 707–715.
Dales, R. P. 1962. The polychaete stomodeum and the interrelationships of the families of the Polychaeta. Proc. Zool. Soc. Lond. 139: 289–328.
Day, J. H. 1961. The polychaete fauna of South Africa. Part 6. Sedentary species dredged off Cape coasts with a few new records from the shore. J. Linn. Soc. Lond. (Zool.) 10: 463–560.
Day, J. H. 1967. A monograph on the Polychaeta of southern Africa. Part 1. Errantia. British Museum of Natural History, London.
Fauchald, K. 1977. The Polychaete Worms: Definitions and Keys to the Orders, Families, and Genera. Los Angeles County Natural History Museum, Los Angeles.
Fauchald, K., and P. Jumars. 1979. The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar. Biol. 17: 193–284.
Fauchald, K., and G. W. Rouse. 1997. Polychaete systematics: past and present. Zool. Scr. 26: 71–138.
Fauvel, P. 1927. Polychetes Sedentaires. Addenda aux Errantes, Archiannelides, Myzostomaires. Faune Fr. 16: 1–494.
Haase, P. 1915. Boreale und arkische Chloraemiden. Wiss. Meeresunters. Kiel 17: 169–228.
Halanych, K.M., and T.J. Robinson. 1999. Multiple substitutions affect the phylogenetic utility of cytochrome b and 12S rDNA data: examining a rapid radiation in leporid (Lagomorpha) evolution. J. Mol. Evol. 48: 369–379.[ISI][Medline]
Halanych, K. M., R. A. Lutz, and R. C. Vrijenhoek. 1998. Evolutionary origins and age of vestimentiferan tube-worms. Cah. Biol. Mar. 39: 355–358.
Hall, K. A., P. A. Hutchings, and D. J. Colgan. 2004. Further phylogenetic studies of the Polychaeta using 18S rDNA sequence data. J. Mar. Biol. Assoc. UK 84: 949–960.
Hartman, O. 1955. Endemism in the North Pacific Ocean, with emphasis on the distribution of marine annelids, and descriptions of new or little known species. Pp. 39–57 in Essays in the Natural Sciences in Honor of Captain Allan Hancock, University of Southern California Press, Los Angeles.
Hartman, O. 1961. Polychaetous annelids from California. Allan Hancock Pacific Exped. 25: 1–226.
Hartman, O. 1965. Deep-water Benthic Polychaetous Annelids off New England to Bermuda and Other North Atlantic Areas. University of Southern California Press, Los Angeles.
Hartman, O. 1967. Poychaetous annelids collected by the USNS Eltanin and Staten Island cruises, chiefly from Antarctic seas. Allan Hancock Monogr. Mar. Biol. 2: 1–387.
Hartman, O. 1969. Atlas of Sedentariate Polychaetous Annelids from California. Allan Hancock Foundation, University of Southern California, Los Angeles.
Hartman, O. 1971. Abyssal polychaetous annelids from the Mozambique basin off Southeast Africa, with a compendium of abyssal polychaetous annelids from world-wide areas. J. Fish. Res. Board Can. 28: 1407–1428.
Hay, A. A. 2002. Flabelligerida from the Francis Creek Shale of Illinois. J. Paleontol. 76: 764–766.[Free Full Text]
Heath, H. 1930. A connecting link between the Annelida and the Echiuroidea (Gephryea Armata). J. Morphol. 49: 223–249.
Hillis, D. M., and M. T. Dixon. 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 66: 411–453.[Medline]
Hillis, D. M., B. K. Mable, A. Larson, S. K. Davis, and E. A. Zimmer. 1996. Nucleic acids IV: sequencing and cloning. Pp. 321–381 in Molecular Systematics, D. M. Hillis, C. Mortiz, and B. K. Mable, eds. Sinauer Associates, Sunderland, MA.
Huelsenbeck, J. P., and F. Ronquist. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.[Abstract/Free Full Text]
Jennings, R. M., and K. M. Halanych. 2005. Mitchondrial genomes of Clymenella torquata (Maldanidae) and Riftia pachyptila (Siboglinidae): evidence for conserved gene order in Annelida. Mol. Biol. Evol. 22: 210–222.[Abstract/Free Full Text]
Johnsen, S. 2001. Hidden in plain sight: the ecology and physiology of organismal transparency. Biol. Bull. 201: 301–318.[Abstract/Free Full Text]
Maddison, D., and W. Maddison. 2003. MacClade 4.06: a tool for phylogenetic analysis and character evolution. Sinauer Associates, Sunderland, MA.
Müller, O. F. 1776. Zoologicae Danicae prodromus, seu Animalium Daniae et Norvegiae indigenarum characteres, nomina et synonyma imprimis popularium. Hallageriis, Copenhagen.
Pickford, G. E. 1947. Histological and histochemical observations upon an aberrant annelid, Poeobius meseres Heath. J. Morphol. 80: 287–319. (Cited in Robbins, 1965.)
Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14: 817–818.[Abstract/Free Full Text]
Robbins, D. E. 1965. The biology and morphology of the pelagic annelid Poeobius meseres Heath. J. Morphol. 146: 197–212.
Rouse, G. W., and K. Fauchald. 1997. Cladistics and polychaetes. Zool. Scr. 26: 139–204.
Rouse, G. W., and F. Pleijel. 2001. Polychaetes. Oxford University Press, Oxford.
Rouse, G. W., and F. Pleijel. 2003. Problems in polychaetes systematics. Hydrobiologia 496: 175–189.
Saint-Joseph, A. 1894. Les Annelides polychetes des cotes de Dinard. Troisieme partie. Ann. Sci. Nat. Zool. Paleontol. Ser. 7 17: 1–395.
Shimodaira, H., and M. Hasegawa. 1999. Multiple comparisons of Log-likelihoods with applications to phylogenetic inference. Mol. Biol. Evol. 16: 1114–1116.[ISI]
Spies, R. B. 1975. Structure and function of the head in flabelligerid polychaetes. J. Morphol. 147: 187–207.
Spies, R. B. 1977. Reproduction and larval development of Flabelliderma commesalis. Pp. 323–345 in Essays on Polychaetous Annelids in Memory of Dr. Olga Hartman, D. J. Reish, and K. Fauchald, eds. The Allan Hancock Foundation, University of Southern California, Los Angeles.
Støp-Bowitz, C. 1948. Sur les polychètes arctiques. Tromsø Mus. Årsh. 66: 1–58.
Struck, T. H., R. Hessling, and G. Purschke. 2002. The phylogenetic position of Aeolosomatidae and Parergodrilidae, two enigmatic oligochaete-like taxa of the "Polychaeta," based on molecular data from 18S rDNA sequences. J. Zool. Syst. Evol. Res. 40: 155–163.
Swofford, D. L. 2002. PAUP* Phylogenetic Analysis Using Parsimony (*and other Methods). Version 4. Sinauer Associates, Sunderland, MA.
Thompson, J. D., T.J. Gibson, F. Plewniak, F. Jeanmougin, and D.G. Higgins. 1997. The ClustalX windows interface: flexible stategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acid. Res. 24: 4876–4882.
Thuesen, E. V., and J. J. Childress. 1993. Metabolic rates, enzyme activities and chemical compositions of some deep-sea pelagic worms, particularly Nectonemertes mirabilis (Nemertea; Holonemertinea) and Poeobius meseres (Annelida: Polychaeta). Deep-Sea Res. Part I 40: 937–953.
Uttal, L., and K. R. Buck. 1996. Dietary study of the midwater polychaete Poeobius meseres in Monterey Bay, California. Mar. Biol. 125: 333–343.
This article has been cited by other articles:
|
|
|
|
 
K. M. Halanych, L. N. Cox, and T. H. Struck
A brief review of holopelagic annelids
Integr. Comp. Biol.,
December 1, 2007;
47(6):
872 - 879.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. H. Struck
Progenetic species in polychaetes (Annelida) and problems assessing their phylogenetic affiliation
Integr. Comp. Biol.,
August 1, 2006;
46(4):
558 - 568.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. M. Halanych and A. M. Janosik
A review of molecular markers used for Annelid phylogenetics
Integr. Comp. Biol.,
August 1, 2006;
46(4):
533 - 543.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
Abstract
Introduction
