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Phylogeny and genetic diversity of palolo worms (Palola, Eunicidae) from the tropical North Pacific and the Caribbean.

  With the first taste of palolo I understood the Samoans' love for it.
Certainly it suggested a salty caviar, but with something added, a
strong, rich whiff of the mystery and fecundity of the ocean depths.
--R. Steinberg. Pacific and Southeast Asian cooking. Time-Life Books,
New York, 1970


Introduction

Early reports of swarming palolo worms and their use as a food source by the native populations of Samoa, Tonga, Fiji, and other South Pacific islands originated from European missionaries dispatched to these remote regions (e.g., Codrington, 1891; MacDonald, 1858; Gray, 1847, cited in Stair, 1897). These authors were primarily interested in the anthropological aspects of the "rising," but the Reverend J.B. Stair provided the British Museum with specimens of the swarming stages from the Samoan islands, which Gray (1847) used as the basis for the species description of the Pacific palolo worm, Palola viridis (he chose a feminine ending for the genus name). Considering that the swarming stages were epitokes and no heads were present, this original description is very short. Friedlaender (1898, 1904) and Woodworth (1903, 1907) both retrieved complete worms and independently assigned them to Eunice viridis. The segments of the swarming epitokes of Eunice viridis each bear one dark pigment spot on the ventral surface. The pigment spots were examined histologically by Schroder (1905), who concluded that they were light sensors.

The common name, palolo, is based on the Samoan name for the worms. The Fijian name mbalolo and the Tongan name balolo are very similar. Other names are, or were, used in other swarming locations throughout the South Pacific (Table 1).

Later authors emphasized the regularity of the swarming, which is correlated with the lunar cycle and happens in October, November, or December in the South Pacific (Burrows, 1945, 1955; Caspers, 1961, 1984; Korringa, 1947). Annual risings of palolo worms have also been reported from the island of Ambon in Indonesia. In contrast to the South Pacific risings, in Ambon the event takes place in March or April. The worms are here known as wawo (Table 1), but the swarming stages are actually a mix of 13 polychaete species (Martens et al. 1995). The wawo was identified as Lysidice oele by Horst (1904, 1905), but Martens et al. (1995) reported that the mix primarily contained Palola viridis.

Two other polychaetes have been described as "palolos." Both also form epitokes and swarm annually. The "Atlantic palolo" is Eunice fucata. Its swarming periodicity was described by Mayer (1908). The "Japanese palolo" is the brackish water nereidid Tylorrhynchus heterochaetus, which has been used as a model organism in physiology and embryology (e.g., Osanai, 1978; Sato and Osanai, 1990). As neither is a Palola, I will not consider them further in this study.

Palola is morphologically characterized by the presence of two palps and three antennae, peristomial cirri, and scoop-shaped calcified mandibles, and by the absence of subacicular hooks (Fauchald, 1992). Branchial filaments, if present, are usually simple. Thus, many characters used in other eunicids to distinguish species, such as the shape and coloration of the subacicular hooks and the branching patterns of the branchial filaments, are not useful in Palola. Characters used by Fauchald in his review are mostly size ratios: length to maximum width of the specimen, relative length of antennae, palps, peristomial and notopodial cirri, as well as length ratios of appendages and shafts of compound falicigers. These differences are subtle and some of the type material was incomplete or poorly preserved, so Fauchald regarded his taxonomy as only a first step.

Three of the fourteen Palola species have wide geographic distributions (Table 2). P. viridis occurs all over the South Pacific, while P. siciliensis has been reported in all major oceans, roughly between latitudes 43 [degrees]N and 32 [degrees]S. P. edentulum might have a general subantarctic distribution. Apart from its type location on the Juan Fernandez Islands, it has also been reported from the North Island of New Zealand and the Chatham Islands in the Southwest Pacific and from the Magellanic Islands in the Southeast Pacific (Glasby and Alvarez, 1999). All other species are exclusively known from their type locations (Table 2).

Because morphological characters to distinguish species are limited and no information exists about intraspecific variation, I am here using a molecular approach to reconstruct the phylogeny within Palola and to assess genetic diversity and historical biogeography. Toward these goals, I sampled Palola species from the Caribbean and across the tropical North Pacific, sequenced them for two mitochondrial markers, and analyzed the sequence data in a phylogenetic and phylogeographic context.

Material and Methods

Collections

To retrieve specimens of Palola spp., Eunice antennata, Eunice cariboea, and Dorvillea similis, coral rubble was collected from seven Pacific and two Caribbean locations from depths varying from 0 to about 23 m, if necessary by snorkeling or scuba diving (see Appendix for collection information). Specimens were removed by breaking the rubble with hammer and chisel and pulling the worms out with forceps. In this process, most of the worms fragmented. In case of doubt whether two fragments belonged to the same individual, only one of the fragments (usually the one containing the head, or if no head was retrieved, the bigger fragment) was used. Usually, a small portion of each individual was fixed in 95%-100% ethanol for DNA studies. The remainder was treated as a voucher sample, fixed in 4% formalin in seawater, and later transferred to 70% ethanol. The voucher specimens are stored at the National Museum of Natural History in Washington, DC (USNM 1084310-USNM 1084406).

Sequence generation

Total genomic DNA was extracted using a CTAB protocol (Thollesson, 2000) or a DNeasy kit (Qiagen). Gene regions of the mitochondrial genes for large subunit ribosomal RNA (16S rRNA) and for cytochrome c oxidase subunit I (COI) were amplified by polymerase chain reaction (PCR). PCR reactions were performed in a volume of 25 or 50 [micro]l. For each 25-[micro]l reaction, 5-10 ng DNA (CTAB protocol) or 1 [micro]l of the extractions (Qiagen protocol) and 0.625 units of taq polymerase (Promega) were used. The concentration of other reagents were 200 [micro]M each of dATP, dGTP, dCTP, and dTTC, 0.5-1 [micro]M of each primer, and 1X sequencing buffer. If amplification was unsuccessful even at lower annealing temperatures, it could often be achieved using the MasterTaq kit (Eppendorf), according to the manufacturer's instructions. The following primers were employed: 16Sa(5'-CGCCTGTTTATCAAAAACAT-3' [Xiong and Kocher, 1991]) and 16Sbr (5'-CCGGTCTGAACTCACATCACGT-3' [Palumbi, 1996]) for 16S rRNA; the primer pairs LCO (5'-GGTCAACAAATCATAAAGATATTGG-3') and HCO (5'-TAAACT TCAGGGTGACCAAAAA-ATCA-3') (Folmer et al., 1994) and COI-7 (5'-ACNAAYCAYAARGAYATYGGNAC-3') and COI-D (5'-TCNG-GRTGNCCRAANARYCARAA-3') (Saito et al., 2000) in all possible combinations for COI. PCRs were performed according to standard protocols with annealing temperatures of 42[degrees] to 45[degrees] C. PCR products were visualized in 1%-1.5% agarose gels stained in ethidium bromide and cleaned using the GENECLEAN II kit (Bio 101) or the QIAquick PCR purification kit (Qiagen).

Sequence reactions were performed in 10-[micro]l volume, using 1 [micro]l (if cleaned with GENECLEAN) or 5 [micro]l (if cleaned with QIAquick) of the sample, 1 [micro]M of primer, 2 [micro]l of ABI BigDye Terminator ver. 3.1 (Applied Bio-systems) and 2 [micro]l halfTERM Dye Terminator reagent (Genpak).

Sequence reactions were performed with the same thermal cycler as for PCR reactions, using standard protocols. After cleanup of the sequence reactions using gel filtration cartridges from Edge Biosystems, the sequences were analyzed with an ABI 377 or 3100 automatic sequencer. Electrochromatograms from the sequencer were visualized in Sequencher 4.0. Forward and reverse fragments were assembled and primer regions cropped and discarded. Outgroup sequences for Marphysa belli, Marphysa sanguinea, Ophryotrocha gracilis, Lumbrineris funchalensis, and Hyalinoecia tubicola were from Struck et al. (2005), Dahlgren et al. (2001), and Siddall et al. (2001). All sequences have been deposited in GenBank with accession numbers DQ317807 to DQ317917 (Table 3).

Analysis

The alignment of the COI sequences produced no ambiguities. The ribosomal sequences were submitted to the MAFFT server in Kyoto (http://www.biophys.kyotou.ac.jp/webmafft/ [Katoh et al., 2002]) for complete alignment. In addition to the taxa included in this study, the alignment also included the sequence for the chiton Katharina tunicata 2 (GenBank accession code U09810), downloaded with secondary structure annotations from the European ribosomal database (http://www.psb.ugent.be/rRNA/ [Van de Peer et al., 2000]). The hypervariable loop between the stem regions G3 and G3' (positions 247-288 in the alignment) was excluded from the phylogenetic analysis. The analysis files with the aligned sequences have been deposited with Tree BASE and are available through the World Wide Web at http://www.treebase.org.

Phylogenetic analysis was performed using Bayesian statistics in MrBayes 3.1 (Ronquist and Huelsenbeck, 2003) and parsimony analysis in PAUP* (Swofford, 2003). The genes were analyzed separately and in combination.

For the stem regions of the 16S rRNA sequences, a list of nucleotide pairings was assembled manually using the annotated sequence of Katharina tunicata as a reference for secondary structure. The stem regions were analyzed under a doublet model with a single rate parameter and 16 states (Schoninger and von Haeseler, 1994), representing all possible nucleotide pairings. The 16S loop regions and the COI sequences were separately submitted to MrModeltest 2.2 (Nylander, 2004), which tests 24 models of sequence evolution using four hierarchical likelihood ratio tests (hLRTs) and the Akaike information criterion. For COI, all four hLRTs as well as the Akaike information criterion favored a general time reversible model (Tavare, 1986) with a correction for a gamma distribution of substitution rates and a proportion of invariable sites (GTR+G+I). For the 16S loop regions, the Akaike information criterion and two of the likelihood ratio tests (hLRT2 and hLRT4) favored an HKY+I+G model (Hasegawa et al., 1985); the default hLRTl favored a GTR+G+I model; hLRT3 favored GTR+G. As it is the more general model, GTR+I+G was implemented for both gene regions. Dorvillea similis was set as the outgroup. For the Bayesian analyses, two runs, with four Monte Carlo Markov chains each, were performed simultaneously for 5,000,000 generations each, sampling trees every 500 generations. The temperature parameter was set to 0.07. The initial 2,500,000 trees from each run were discarded as "burn-in." The remaining 5000 trees from each run were combined and summarized in a majority rule consensus tree.

Parsimony bootstrap analysis was performed with 1000 bootstrap replicates, using the heuristic search option in PAUP*. For each heuristic search, 10 replicates of random taxon addition were performed with tree bisection/reconnection as the branch-swapping algorithm. Branches with less than 50% bootstrap support were discarded.

Haplotypes were collapsed using the program Collapse 1.2 (Posada, 2004). Uncorrected genetic distances were calculated in PAUP* (Swofford, 2003). Molecular diversity indices were calculated in Arlequin 2.000 (Schneider et al., 2000). Nucleotide diversity was calculated under the Kimura 2-parameter model. Geographic surface distances between sample locations were calculated using the airports of the respective locations as reference points--with the exception of Ant Atoll, for which the position was obtained from the website of the U.S. Geological Survey, and Carrie Bow Cay in Belize, for which the location was obtained from the CCRE program, Smithsonian Institution.

Results

Phylogenetic analysis

For 16S rRNA, sequence length varied between 362 bp and 509 bp. These differerences are based on complete sequences, that is, not on sequences with missing end regions. For five of the eight outgroups (Hyalonoecia tubicola, Lumbrineris funchalensis, Ophryotrocha gracilis, Marphysa belli, and Marphysa sanguinea), the 16S sequences were markedly shorter than all others. The alignment with secondary structure annotations indicates that these five species are missing entire stem/loop regions: the complementary strands of G3/G3', G8/G8', G9/G9', and G15/G15' are absent, as are the loop regions between the respective pairs. The region that aligns with the G7 region in other species is partially present but does not seem to have a complement.

In the combined analysis there was no conflict between the Bayesian and the bootstrap parsimony analysis, but the Bayesian analysis gave better resolution in some parts of the tree, especially in the deeper nodes. Palola appeared as monophyletic, with 99% posterior probability and 69% bootstrap support (Fig. 1). The sister group to Palola remains unresolved. Within Palola, two major clades can be distinguished: clade A contains eastern and western Pacific samples, plus one sample from Bocas del Toro in the Caribbean. Clade B contains a mix of Caribbean and western Pacific samples. The clades are further subdivided into nine subclades each, A1-A9 and B1-B9, respectively.

When both genes were analyzed separately (Fig. 2), all subclades remained supported, with one exception: there was no support for clade A2 in the Bayesian analysis of 16S (however, the clade had 70% parsimony bootstrap support). There are some discrepancies between the separate analyses and the combined analysis, but in all cases of discrepancies the alternative arrangement to the combined analysis has low support, both in posterior probabilities and bootstrap values. The 16S rRNA analysis supports the monophyly of Palola and resolves clade B. The COI analysis gives low resolution in the deeper nodes but resolves clade A.

Morphological observations

Due to the incompleteness of much of the material and the high degree of morphological conservation within the genus, the clades shown in Figure 1 cannot be clearly delineated morphologically. However, in some cases characters are restricted to certain clades, although they were not necessarily observed in every individual. In particular, in clade B, seven individuals (marked with asterisks in Fig. 1) showed ventral eyespots in their posterior body regions (Fig. 3A). In no case have ventral eyespots been observed in clade A. Clade A8 contains three individuals that were unusual with respect to morphology and habitat: they have unusually long and tapering antennae, palps, and parapodial cirri (Fig. 3B); and unlike all other samples, they were not infaunal, but inhabited crevices under rocks. Another morphologically distinct clade is clade A7, containing two specimens from Pohnpei. These are characterized by dark brown pigment on the dorsal side; in other samples, body pigmentation is usually restricted to the ventral eyes and the parapodial pigment spots. In addition, the two specimens have a median sulcus in the prostomium that is markedly shallow and barely visible dorsally (Fig. 3C).

Haplotype diversity and distribution

The 50 COI sequences grouped into 26 haplotypes; the 55 16S sequences grouped into 32 haplotypes. Number and percentage of singleton (only found in a single individual), private (occurring in more than one individual but a single location), and shared haplotypes (occurring in more than one location) are listed in Table 4.

No haplotype or nucleotide diversity was found in Ant Atoll or in Las Perlas for either COI or 16S, indicating that all individuals from these locations were identical (however, only three individuals were sequenced from Ant Atoll). The highest haplotype diversity (1 for both genes) was in Pohnpei, where each sampled individual represented a different haplotype. Haplotype diversity was also high in each of the remaining locations (Table 5). Nucleotide diversity was higher in the Caribbean samples than in any of the Pacific samples for both of the genes. Mean nucleotide divergences among and within clades are listed in Table 6.

All shared haplotypes spanned distances of over 2000 km (Tables 7, 8). The most widespread haplotypes covered the complete east-west expansion of the tropical North Pacific, from Las Perlas in the east to Palau in the west (15,826 km). Private haplotypes occurred in Belize, Bocas, Kosrae, and Yap.

Discussion

Despite a high degree of morphological uniformity, the phylogenetic analyses reveal deep genetic divergences within Palola. 16S rRNA is an appropriate marker to resolve the deeper branches within the genus (Fig. 2A), but even more conserved genes, such as the nuclear 18S rRNA, might be necessary to resolve outgroup relationships. Cytochrome c oxidase subunit I (COI) provides better resolution than 16S rRNA within the more derived groups in clade A (Fig. 2B), but faster evolving markers would be necessary to address some phylogeographic questions.

Morphological examinations of the voucher material revealed that few morphological characters distinguish the clades. The only likely morphological distinction between clades A and B are the ventral eyespots, as described in Palola viridis. They are only present in some individuals of clade B but occur in five of the nine subclades. One obvious explanation for why they were not present in every specimen is that often only anterior fragments were collected and examined, the posterior body regions being missing. Another explanation is that eyespots only develop during reproductive time. Schroder (1905) examined the ventral eyespots of P. viridis histologically, using the swarming epitokes, but never studied nonreproductive individuals. It is a strong possibility that eyespots are a synapomorphy for clade B. Reproductive specimens in clade A never had ventral eyespots. No morphological synapomorphy for clade A has been detected.

At present, it is impossible to determine which, if any, of the subclades in clade B is P. viridis. All of the subclades are morphologically similar and, whenever relevant characters were observable, more or less conform to the description of P. viridis given in Fauchald (1992): palps and antennae are arranged in a horseshoe; the size of the head appendages increases from the palps to the median antenna; the prostomium is about as wide as the peristomium; the prostomium in some specimens is dorsally excavate around the palps and the lateral antennae. Characters of the parapodia and setae widely overlap with the descriptions of other species and have limited value for species identification. Fauchald (1992) describes brown pigmentation in the anterior dorsum of P. viridis that was not observed in any samples belonging to clade B. Because of the uncertainties associated with designating any of the subclades of clade B as P. viridis, it is desirable to generate DNA sequences for samples originating from the type location of this species in Samoa and throughout the species' geographic range to determine its true distribution and genetic diversity. Attempts to obtain material from Samoa have so far been unsuccessful.

No clear morphological distinction is apparent among the closely related clades Al, A2, and A3. They may represent a single species with a distribution across the entire east-west expansion of the Pacific and even the Caribbean. If the identification key in Fauchald (1992) is used, the species is identified as P. siciliensis; however, the specimens can be distinguished from P. siciliensis by their earlier onset of branchiae. In clades A1-A3, branchiae start between setigers 48 and 60 whenever a long enough anterior fragment can be observed. In P. siciliensis, the earliest appearance of branchiae is setiger 92 and can be as far posterior as setiger 180 (Fauchald, 1992). As with P. viridis, P. siciliensis lacks sequence data from the type location in Sicily to test the species designation.

All subclades except A1-A3 may represent distinct species. The species generally seem to be cryptic, although clades A7 and A8 show some characteristic morphological features (Fig. 3) not observed in other specimens or described from any of the known species. However, for clearer morphological delineations, it would be necessary to examine more complete material for all subclades.

The age of Palola as a genus is unknown, but the probability is high that it arose in the Paleozoic. Fossil mandibles and maxillae of eunicidan polychaetes date back to the Ordovician (Kielan-Jaworowska, 1966), including the lapidognath jaw type found in the Eunicidae. However, the typical scoop-shaped mandibles of Palola have not been described from the fossil record. A paleozoic origin would explain the high degree of intrageneric genetic divergence.

Although COI and 16S rRNA are considered two of the more conserved genes in the mitochondrial genome, the relatively high degree of divergence--averaging 14.5% and 12.4% respectively--is not unusual in polychaetes. For 16S rRNA, mean sequence divergence in the syllid genus Autolytus is approximately 21% (Nygren and Sundberg, 2003), based on 16 species. For the dorvilleid genus Ophrytrocha it is 12%, based on 17 species (Dahlgren et al., 2001). For COI, mean within-family divergence in the Terebellidae is over 20% based on the nine available sequences from GenBank (Colgan et al., 2001; Siddall et al., 2001). For the two terebellid genera of which two species are represented in GenBank, sequence divergence was 20% for the two Loimia species and 19% for the two Amphitrite species. In view of the fact that taxonomic ranks are arbitrary, these comparisons can be only a rough guide, but they convey that the genetic variation within Palola is within a normal range for polychaetes. The genetic variation is only surprising compared with the high degree of morphological conservation among the species.

Most haplotypes (76.9% for COI; 75% for 16S rRNA) detected in this study are singletons (Table 4) and uninformative with respect to phylogeographic questions. Only a small percentage of the haplotypes (7.7% for COI; 12.5% for 16S) are shared among locations, but they represent a large percentage of the sampled individuals (40% for both markers) and cover six of the nine collecting locations (Tables 7 and 8). Several recent studies have shown strong geographic population structure in marine shallow-water invertebrates, even in taxa with high dispersal capabilities (e.g., Kirkendale and Meyer, 2004, and references therein). It is therefore surprising to find widespread, in some cases extremely widespread, haplotypes and clades in Palola, especially considering that all known eunicid larvae are short-lived and lecithotrophic (Richards, 1967). In clades A1-A3 with very short branches, the lack of geographic structure may be due to incomplete lineage sorting, suggesting that the islands have been colonized relatively recently in terms of the age of the genus and not enough time has passed for distinct lineages to be established on each island (e.g., Harrison, 1991; Avise, 2000).

Haplotype diversity and nucleotide diversity are both high in all but two collecting locations (Table 5). The phylogenetic reconstructions show that the high nucleotide diversity is not due to local radiations (in which case all haplotypes in one location would form a clade) but to repeated colonization of the islands by members of genetically divergent Palola clades. This effect is most pronounced in the Caribbean locations and is probably related to the complex geological history of the Caribbean region. Multiple models exist for the tectonic history of the Caribbean (Graham, 2003, and references therein), but whichever theory is favored, it is likely that shallow-water marine taxa such as Palola have had numerous opportunities for dispersal and vicariance within the region, allowing divergent clades to co-occur within the same location. Exchange with Pacific waters was possible until approximately 3.5 million years ago, explaining why the two major Palola clades contain samples from both the Caribbean and the Pacific.

No nucleotide and haplotype diversity was detected in Ant Atoll or the Las Perlas Archipelago. Although this might be an artifact of small sample size (only three individuals sampled from Ant Atoll) or a single collecting spot at each island group, it could also indicate that these locations were only recently colonized. If a population had been established for a long time, some local haplotype diversity would be expected. More extensive sampling would be necessary to investigate this question.

More rapidly evolving markers should add resolution to clade A, but the current data indicate that long-distance dispersal has taken place repeatedly in both major clades of Palola. Despite long-held opinions on eunicid development, long-lived planktotrophic larvae might exist in at least some Palola lineages.

Acknowledgments

This research was conducted at the National Museum of Natural History under a Smithsonian Institution postdoctoral fellowship and continued in the Department of Organismic and Evolutionary Biology at Harvard University and at the Smithsonian Marine Station at Fort Pierce, Florida (contribution Nr 630). Additional funding was provided by Caribbean Coral Reef Ecosystems (contribution Nr 738) and the Nando Peretti Foundation. The Smithsonian Tropical Research Institute hosted a short-term visit. I owe special thanks to Kristian Fauchald and Jon Norenburg as postdoctoral advisors; Megan Schwartz for help with molecular methods; Torsten Struck for contributing previously unpublished sequences; Gonzalo Giribet for continued lab support; Len Hirsch, Sebia Hawkins, and Gustav Paulay for helping with travel arrangements; Jennifer Dorton, Raphael Ritson-Williams, Pat and Lori Collin, Simpson Abraham, Ahser Edward, Don Buden, Ray Verg-in, Andy Tafileichig, and many other helpers in Micronesia for their support in the field. Grazia Cantone provided specimens of P. siciliensis from the type location for morphological comparison. I also thank two anonymous reviewers whose comments have significantly improved this manuscript.

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Appendix

Collecting Stations: Geographic co-ordinates refer to airports, with the exception of Ant Atoll and Carrie Bow Cay

Station 1: Carrie Bow Cay area, Belize (16 [degrees]48'N, 88 [degrees]05'W)

1A: Carrie Bow Cay, reef flat, 0.5-1 m, Feb. 2001

1B: Carrie Bow Cay, reef drop-off, 8-10 m, Feb. 2001

1C: Blue Ground Range, 0.5-1 m, Feb. 2001

1D: Twin Cays, 0.5-1 m, Feb. 2001

1E: Southwater Cay, 1.5 m

Station 2: Saboga Island, Las Perlas Archipelago, Panama (8 [degrees]35'N, 79 [degrees]35'W): 2.5-3 m, June 2001

Station 3: Bocas del Toro Archipelago, Panama (9 [degrees]21'N, 82 [degrees]15'W)

3A: Hospital Point, Isla Solarte, 2.5 m, June 2001

3B: Mangrove Inn, Isla Colon, 1-2 m, June 2001

3C: Drago Beach, Isla Colon, Panama, 2 m, June 2001

Station 4: Guam, USA (13 [degrees]29'N, 144 [degrees]47'E)

4A: Double Reef, 15-20 m, Oct. 2001

4B: Shark's Pit, 15-23 m, Oct. 2001

4C: Cocos Island, 1.5-3 m, Oct. 2001

4D: Mangilao, 1 m, Oct. 2001

Station 5: Republic of Palau (7 [degrees]22'N, 134 [degrees]32'E)

5A: Lighthouse Reef, 1.5-2 m, Oct. 2001

5B: Western Channel, 2 m, Oct. 2001

5C: Short drop-off, 13 m, Oct. 2001

5D: Turtle Island, 0.5-2 m, Oct. 2001

5E: Ngerikuul Channel, 13-17 m, Oct. 2001

Station 6: Yap, Federated States of Micronesia (9 [degrees]29'N, 138 [degrees]40'E)

6A: Colonia, 3-5 m, Nov. 2001

6B: Mill Channel, 5-15 m, Nov. 2001

Station 7: Pohnpei, Federated States of Micronesia (6 [degrees]59'N, 158 [degrees]12'E)

7A: The Village Hotel, 0.3-1.5 m, Nov. 2001

7B: Nahpali, 2 m, Nov. 2001

7C: Black Coral Island, 1.5-3 m, Nov. 2001

Station 8: Tolonmurui Island, Ant Atoll, Pohnpei, Federated States of Micronesia (6 [degrees]46'N, 157 [degrees]55'E), 0.1-5 m, Nov. 2001

Station 9: Kosrae, Federated States of Micronesia (5 [degrees]21'N, 162 [degrees]57'E)

9A: Mwot, Kosrae, Federated States of Micronesia, 2-3 m, Nov. 2001

9B: Buoy 21, Kosrae, Federated States of Micronesia, 13-20 m, Nov. 2001

9C: Buoy 5, Kosrae, Federated States of Micronesia, 10-15 m, Nov. 2001

ANJA SCHULZE

Smithsonian Marine Station, 701 Seaway Drive, Fort Pierce, Florida 34949

Received 22 February 2005; accepted 5 December 2005.

Email: schulze@sms.si.edu
Table 1 Occurrences of Palola viridis risings and common names where
known

Location               Local name                References

Samoa                  palolo                    Burrows (1945, 1955);
                                                   Hauenschild et al.
                                                   (1968); Woodworth
                                                   (1903, 1907)
Fiji                   mbalolo                   Woodworth (1903);
                                                   Burrows (1955)
Tonga                  balolo                    Burrows (1955)
Papua New Guinea       vaien, lamaha, kaama      Bartlett (1947);
                                                   Burrows (1955)
Australia, east coast  --                        Burrows (1955); Brown
                                                   (1877)
Solomon Islands        orku, parenga or parena   Burrows (1955)
Vanuatu                ayby (?), un              Burrows (1955);
                                                   Codrington (1891);
                                                   Seeman (1862)
New Caledonia          --                        Burrows (1955)
Kiribati               Te nmatamata, te          Burrows (1955); Powell
                         kawariki (?), te o (?)    (1882)
Cook Islands           --                        Burrows (1955)
Ambon                  wawo                      Burrows (1955); Horst
                                                   (1904, 1905); Martens
                                                   et al. (1995)

Dash (--) signifies that the local name is unknown.

Table 2 Currently valid Palola species and their type locations

                                                    Reported
Species                             Type location   distribution*

P. accrescens (Hoagland, 1920)      Philippine      --
                                      Islands
P. brasiliensis Zanol et al., 2000  Brazil          --
P. ebranchiata (Quatrefages, 1866)  Palermo, Italy  --
P. edentulum (Ehlers, 1901)         Juan Fernandez  South Australia, NZ
                                      Island          North Island,
                                                      Chatham Islands,
                                                      Magellanic Islands
P. esbelta Morgado & Amaral, 1981   Sao Sebastiao,  --
                                      Brazil
P. leucodon (Ehlers, 1901)          Juan Fernandez  --
                                      Island
P. madeirensis Baird 1869           Madeira         --
P. pallidus Hartman, 1938           Laguna Beach,   --
                                    California
P. paloloides (Moore, 1904)         San Diego,      --
                                      California
P. siciliensis (Grube, 1840)        Palermo, Italy  Mediterranean, SE
                                                      USA, Mexico
                                                      (Caribbean),
                                                      Argentina,
                                                      Venezuela,
                                                      Galapagos Islands,
                                                      Guam, South
                                                      Australia,
                                                      Thailand
P. simplex Peters, 1854             Mozambique      --
P. valida (Gravier, 1900)           Djibouti        --
P. vernalis (Treadwell, 1922)       Fiji            --
P. viridis Gray, 1847               Samoa           SW Pacific (s.
                                                      Table 1)

Species                             References[dagger]

P. accrescens (Hoagland, 1920)      NA
P. brasiliensis Zanol et al., 2000  NA
P. ebranchiata (Quatrefages, 1866)  NA
P. edentulum (Ehlers, 1901)         Glasby & Alvarez (1999)
P. esbelta Morgado & Amaral, 1981   NA
P. leucodon (Ehlers, 1901)          NA
P. madeirensis Baird 1869           NA
P. pallidus Hartman, 1938           NA
P. paloloides (Moore, 1904)         NA
P. siciliensis (Grube, 1840)        Augener (1913); Gardiner
                                    (1976); Hofmann (1972,
                                    1974, 1975); Kohn &
                                    Lloyd (1973); Kohn &
                                    White (1977); Linero
                                    Arana (1985); Orensanz
                                    (1975); Salazar-Vallejo &
                                    Carrera-Parra (1997);
                                    Westheide (1977)
P. simplex Peters, 1854             NA
P. valida (Gravier, 1900)           NA
P. vernalis (Treadwell, 1922)       NA
P. viridis Gray, 1847               s. Table 1

* Dashes (--) indicate that the species is known only from the type
location.
[dagger] NA indicates that no further references exist after the species
description.

Table 3 Collection information and COI and 16S GenBank accession numbers
for Palola samples

                                   COI accession   16S accession
Sample name*              Station  number[dagger]  number[dagger]

Belize14                   1A      DQ317809        DQ317863
Belize32                   1B      DQ317810        DQ317864
Belize34                   1B                      DQ317865
Belize37                   1C      DQ317811        DQ317866
Belize38                   1C      DQ317812
Belize39                   1C      DQ317813        DQ317867
Belize43                   1B                      DQ317868
Bocas68                    3A      DQ317814        DQ317869
Bocas70                    3A      DQ317815        DQ317870
Bocas77                    3A      DQ317816        DQ317871
Bocas78                    3B      DQ317817        DQ317872
Bocas79                    3B      DQ317818        DQ317873
Bocas85                    3A                      DQ317874
Bocas86                    3C                      DQ317875
Bocas87                    3C                      DQ317876
Perlas52                   4       DQ317838        DQ317897
Perlas53                   4       DQ317839
Perlas54                   4       DQ317840        DQ317898
Perlas55                   4       DQ317841        DQ317899
Perlas57                   4       DQ317842        DQ317900
Perlas58                   4       DQ317843
Perlas59                   4       DQ317844        DQ317901
Perlas61                   4       DQ317845        DQ317902
Perlas63                   4       DQ317846        DQ317903
Guam89                     5A      DQ317823        DQ317881
Guam92                     5B      DQ317824        DQ317882
Guam94                     5C      DQ317825        DQ317883
Guam100                    5C      DQ317819        DQ317877
Guam101                    5C      DQ317820        DQ317878
Guam102                    5D      DQ317821        DQ317879
Guam103                    5D      DQ317822        DQ317880
Palau105                   6A      DQ317831
Palau111                   6A      DQ317832        DQ317891
Palau115                   6B      DQ317833        DQ317892
Palau117                   6B      DQ317834        DQ317893
Palau118                   6C      DQ317835        DQ317894
Palau124                   6D      DQ317836        DQ317895
Palau125                   6D      DQ317847        DQ317896
Yap129                     7A      DQ317852        DQ317911
Yap130                     7A      DQ317853        DQ317912
Yap131                     7A      DQ317854        DQ317913
Yap138                     7A      DQ317855
Yap141                     7B      DQ317856        DQ317914
Pohnpei142-1               8A      DQ317847        DQ317904
Pohnpei142-2               8A                      DQ317905
Pohnpei151-1               8B                      DQ317906
Pohnpei151-2               8B      DQ317848        DQ317907
Pohnpei151-3               8B      DQ317849        DQ317908
Pohnpei157-1               8C      DQ317850        DQ317909
Pohnpei157-2               8C      DQ317851        DQ317910
Ant158-1                   9       DQ317807        DQ317860
Ant158-3                   9                       DQ317861
Ant160                     9       DQ317808        DQ317862
Kosrae161                 10A      DQ317826        DQ317884
Kosrae165                 10B      DQ317827        DQ317885
Kosrae166                 10B      DQ317828        DQ317886
Kosrae168                 10B      DQ317829        DQ317887
Kosrae169                 10B                      DQ317888
Kosrae170                 10B                      DQ317889
Kosrae176                 10C      DQ317830        DQ317890
Eunice antennata           1D      DQ317858        DQ317916
Eunice cariboea            1E      DQ317859        DQ317917
Marphysa belli                                     AY838835
Marphysa sanguinea                 AY040708.1      AY838836
Dorvillea similis                  DQ317857        DQ317915
Ophryotrocha gracilis                              AF321424
Lumbrineris funchalensis                           AY838831
Hyalonoecia tubicola                               AY838830

* Sample names for Palola refer to the collecting locations, followed by
individual identifiers that refer to the vials of the voucher material;
sample names with dashes refer to several specimens from the same vial.
The outgroups are specified by their full species names.
[dagger] Empty cells indicate that no sequence was obtained.

Table 4 Number and percentages of singleton, private and shared
haplotypes for COI and 16S rRNA

                                Haplotypes    Individuals
                                Number  %     Number  %

Cytochrome c oxidase subunit I
  Singletons                    20      76.9  20      40
  Privates                       4      15.4  10      20
  Shared                         2       7.7  20      40
  Total                         26            50
16S rRNA
  Singletons                    24      75.0  24      43.6
  Privates                       4      12.5   9      16.4
  Shared                         4      12.5  22      40.0
  Total                         32            55

Table 5 Haplotype (h) and nucleotide diversity ([pi]) for both genes by
location

                            COI
         Haplotype             Nucleotide
         diversity (h)         diversity ([pi])

Belize   0.900 [+ or -] 0.161  0.143 [+ or -] 0.087
Bocas    0.700 [+ or -] 0.218  0.164 [+ or -] 0.099
Palau    0.952 [+ or -] 0.095  0.115 [+ or -] 0.065
Yap      0.900 [+ or -] 0.161  0.087 [+ or -] 0.053
Guam     0.900 [+ or -] 0.095  0.113 [+ or -] 0.064
Pohnpei  1.000 [+ or -] 0.126  0.126 [+ or -] 0.077
Ant      0                     0
Kosrae   0.700 [+ or -] 0.218  0.117 [+ or -] 0.072
Perlas   0                     0

                            16S
         Haplotype             Nucleotide
         diversity (h)         diversity ([pi])

Belize   0.933 [+ or -] 0.122  0.108 [+ or -] 0.063
Bocas    0.964 [+ or -] 0.077  0.165 [+ or -] 0.090
Palau    0.867 [+ or -] 0.129  0.052 [+ or -] 0.031
Yap      0.833 [+ or -] 0.222  0.102 [+ or -] 0.067
Guam     0.952 [+ or -] 0.095  0.059 [+ or -] 0.034
Pohnpei  1.000 [+ or -] 0.076  0.099 [+ or -] 0.056
Ant      0                     0
Kosrae   0.857 [+ or -] 0.137  0.136 [+ or -] 0.077
Perlas   0                     0

Table 6 Mean nucleotide divergence and range (in parentheses) in COI
(uncorrected) and 16S rRNA (uncorrected) within and between clades for
individuals and haplotypes

                                Individuals (%)  Haplotypes (%)

Cytochrome c oxidase subunit I
  Within Palola                 14.5 (0-24.2)     17.1 (0.2-24.2)
  Within clade A                 9.8 (0-20.0)     13.2 (0.2-19.7)
  Within clade B                16.6 (0-21.4)     17.4 (0.1-21.2)
  Between clades A and B        20.7 (14.6-24.3)  20.0 (14.7-24.2)
16S rRNA
  Within Palola                 12.4 (0-21.9)     14.6 (0.2-21.9)
  Within clade A                 6.4 (0-13.9)      9.2 (0.2-18.8)
  Within clade B                15.3 (0-21.9)     15.4 (0.2-21.9)
  Between clades A and B        18.2 (3.1-21.8)   18.0 (3.6-21.8)

Table 7 List of shared (COI-S1 and COI-S2) and private haplotypes
(COI-PI through COI-P4) for COI with geographic extensions of shared
haplotypes

                                  Maximum surface
COI Haplotype name  Samples       distance (km)

CO1-S1              Ant158-1       2,202
                    Ant160
                    Guam102
                    Guam103
                    Pohnpei157-2
                    Yap130
                    Yap138
CO1-S2              Guam94        15,826
                    Palau115
                    Palau117
                    Pohnpei151-3
                    Perlas52
                    Perlas53
                    Perlas54
                    Perlas55
                    Perlas57
                    Perlas58
                    Perlas59
                    Perlas61
                    Perlas63
CO1-P1              Belize14
                    Belize32
CO1-P2              Bocas68
                    Bocas70
                    Bocas79
CO1-P3              Kosrae165
                    Kosrae166
                    Kosrae168
CO1-P4              Yap129
                    Yap131

Table 8 List of shared (16S-S1 through 16S-S4) and private haplotypes
(16S-P1 through 16S-P4) for 16S rRNA with geographic extensions of
shared haplotypes

16S Haplotype                Maximum geographic
name           Samples       distance (km)

16S-S1         Ant158-1       2,202
               Ant158-3
               Ant160
               Guam102
               Guam103
               Pohnpei157-1
               Pohnpei157-2
               Yap130
16S-S2         Palau115      15,826
               Palau117
               Perlas52
               Perlas54
               Perlas55
               Perlas57
               Perlas59
               Perlas61
               Perlas63
16S-S3         Bocas79        8,888
               Kosrae169
16S-S4         Palau124       7,406
               Palau125
               Pohnpei151-2
16S-P1         Belize14
               Belize34
16S-P2         Bocas85
               Bocas86
16S-P3         Kosrae165
               Kosrae166
               Kosrae168
16S-P4         Yap129
               Yap131
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