Whale falls, multiple colonisations of the deep, and the phylogeny of Hesionidae (Annelida)
Mindi Summers A C , Fredrik Pleijel B and Greg W. Rouse A CA Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, CA 92092 USA.
B University of Gothenburg, Department of Biological and Environmental Sciences – Tjärnö, SE-452 96, Strömstad, Sweden.
C Corresponding author. Email: mindi.summers@maine.edu; grouse@ucsd.edu
Invertebrate Systematics 29(2) 105-123 https://doi.org/10.1071/IS14055
Submitted: 6 October 2014 Accepted: 13 February 2015 Published: 11 June 2015
Abstract
Phylogenetic relationships within Hesionidae Grube, 1850 are assessed via maximum parsimony and maximum likelihood analyses of mitochondrial (cytochrome c oxidase subunit I and 16S rRNA) and nuclear (18S rRNA, and 28S rRNA) data. The analyses are based on 42 hesionid species; six of these being new species that are described here. The new species, all from deep (>200 m depth) benthic environments (including whale falls) in the eastern Pacific, are Gyptis shannonae, sp. nov., Neogyptis julii, sp. nov., Sirsoe sirikos, sp. nov., Vrijenhoekia ketea, sp. nov., Vrijenhoekia falenothiras, sp. nov., and Vrijenhoekia ahabi, sp. nov. The molecular divergence among the new members of Vrijenhoekia is pronounced enough to consider them cryptic species, even though we cannot distinguish among them morphologically. Our results also showed that the subfamily Hesioninae Grube, 1850, as traditionally delineated, was paraphyletic. We thus restrict Hesioninae to include only Hesionini Grube, 1850 and refer the remaining members to Psamathinae Pleijel, 1998. The present study increases the number of hesionid species associated with whale falls from one to six and markedly increases the number of described deep-sea hesionid taxa. There appear to have been multiple colonisations of the deep sea from shallow waters by hesionids, though further sampling is warranted.
Additional keywords: Annelida, deep-sea, eastern Pacific, polychaete.
References
Blake, J. A. (1985). Polychaeta from the vicinity of deep-sea geothermal vents in the eastern Pacific. I. Euphrosinidae, Phyllococidae, Hesionidae, Nereididae, Glyderidae, Dorvelleidae, Orbiniidae, and Maldanidae. Bulletin of the Biological Society of Washington 6, 67–101.Blake, J. A. (1991). A new species of Hesiocaeca (Polychaeta: Hesionidae) from hydrothermal vents at the Mariana back-arc basin with notes on other polychaetes. Proceedings of the Biological Society of Washington 104, 175–180.
Blake, J. A., and Hilbig, B. (1990). Polychaeta from the vicinity of deep-sea hydrothermal vents in the eastern Pacific. II. New species and records from the Juan de Fuca and Explorer Ridge systems. Pacific Science 44, 219–253.
Böggemann, M. (2009). Polychaetes (Annelida) of the abyssal SE Atlantic. Organisms, Diversity & Evolution 9, 251–428.
Borda E. Kudenov J. D. Chevaldonné P. Blake J. A. Desbruyères D. Fabri M.-C. Hourdez S. Pleijel F. Shank T. M. Wilson N. G. Schulze A. Rouse G. W. 2013
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=56e52cdc45a6782c195036d7af89ad92CAS | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=56e52cdc45a6782c195036d7af89ad92CAS | 10742046PubMed | 10742046PubMed |
Chevaldonné, P., Jollivet, D., Desbruyeres, D., Lutz, R., and Vrijenhoek, R. C. (2002). Sister-species of eastern Pacific hydrothermal vent worms (Ampharetidae, Alvinellidae, Vestimentifera) provide new mitochondrial COI clock calibration. Cahiers de Biologie Marine 43, 367–370.
Desbruyères, D., and Toulmond, A. (1998). A new species of hesionid worm, Hesiocaeca methanicola, sp. nov. (Polychaeta: Hesionidae), living in ice-like methane hydrates in the deep Gulf of Mexico. Cahiers de Biologie Marine 39, 93–98.
Fauchald, K., and Hancock, D. R. (1981). Deep-water polychaetes from a transect off central Oregon. Allan Hancock Monographs in Marine Biology 11, 1–73.
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=c84f72a2d796a7fee91c4e2e01175599CAS |
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=c84f72a2d796a7fee91c4e2e01175599CAS | 7881515PubMed | 7881515PubMed |
Giribet, G., Carranza, S., Baguñà, J., Riutort, M., and Ribera, C. (1996). First molecular evidence for the existence of Tardigrada + Arthropoda clade. Molecular Biology and Evolution 13, 76–84.
| First molecular evidence for the existence of Tardigrada + Arthropoda clade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtVylur8%3D&md5=3929e906bf01ea2e7297deed531bbc59CAS | 8583909PubMed | 8583909PubMed |
Glover, A. G., Goetze, E., Dahlgren, T. G., and Smith, C. R. (2005). Morphology, reproductive biology and genetic structure of the whale-fall and hydrothermal vent specialist, Bathykurila guaymasensis Pettibone, 1989 (Annelida: Polynoidae). Marine Ecology (Berlin) 26, 223–234.
| Morphology, reproductive biology and genetic structure of the whale-fall and hydrothermal vent specialist, Bathykurila guaymasensis Pettibone, 1989 (Annelida: Polynoidae).Crossref | GoogleScholarGoogle Scholar |
Grube, A. E. (1850). Die Familien der Anneliden. Archiv für Naturgeschichte 16, 249–364.
Halt, M. N., Kupriyanova, E. K., Cooper, S. J. B., and Rouse, G. W. (2009). Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida, Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology. Invertebrate Systematics 23, 205–222.
| Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida, Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXosleisLY%3D&md5=3fd279eb58715cf7a4ac10c08a78b5d2CAS |
Hartman, O. (1961). Polychaetous annelids from California. Allan Hancock Pacific Expeditions 25, 1–226.
Hessle, C. (1925). Einiges über die Hesioniden und die Stellung der Gattung Ancistrosyllis. Arkiv för Zoologi 17, 1–36.
Hilbig, B. (1992). New polychaetous annelids of the families Nereididae, Hesionidae, and Nephtyidae from the Santa Maria Basin, California, with a redescription of Glycera nana Johnson, 1901. Proceedings of the Biological Society of Washington 105, 709–722.
Hilbig, B. (1997). Family Hesionidae (Sars, 1862). In ‘Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel, Volume 4, The Annelida, Part. 2. Oligochaeta and Polychaeta: Phyllodocida (Phyllodocidae to Paralacydoniidae)’. pp. 235–260. (Eds J. A. Blake, B. Hilbig and P. H. Scott.) (Santa Barbara Museum of Natural History: Santa Barbara, CA.)
Hilbig, B., and Dittmer, J. D. (1979). Gyptis helgolandica. New species (Annelida, Hesionidae) of polychaetes from the sublittoral zone of the German Bight. Veröffentlichungen des Instituts für Meeresforschung in Bremerhaven 18, 101–110.
Hyland, J. (1990). Macroinfaunal assemblages in the Santa Maria Basin off the coast of southern California. In ‘California OCS Phase II Monitoring Program. Year-Three Annual Report, F-1’. (Eds M. Steinhauer and E. Imamura.) (US Department of the Interior Minerals Management Service: Los Angeles, CA.)
Hyland, J., and Neff, J. (1988). California OCS Phase II Monitoring Program. Year-One Annual Report, Appendix A. US Department of the Interior Minerals Management Service, Los Angeles, California.
Johnston, G. (1836). Illustrations in British zoology, Cl. Annélides, Ord. Errántes, Fam. Nerèides Genus Psa’mathe. Magazine of Natural History and Journal of Zoology, Botany, Mineralogy, Geology, and Meteorology 9, 14–17.
Katoh, K., Misawa, K., Kuma, K., and Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30, 3059–3066.
| MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslOqu7s%3D&md5=062ddb93ea5f1aa3de915bbe559e94aaCAS | 12136088PubMed | 12136088PubMed |
La Greca, M. (1946). Studii sui policheti del Golfo di Napoli. Pubblicazioni della Stazione Zoologica di Napoli 20, 270–280.
Lamarck, J. B. (1818). ‘Histoire Naturelle des Animaux sans Vertébres.’ (Ballière, Paris.)
Langerhans, P. (1880). Die Wurmfauna Madeiras. II. Zeitschrift fur Wissenschartliche Zoologie 33, 271–316.
Laubier, L. (1961). Podarkeopsis galagaui n. g., sp. nov., hésionide des vases cotières de Banyuls-sur-Mer. Vie et Milieu 12, 211–217.
Lê, H., Lecointre, G., and Perasso, R. (1993). A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms. Molecular Phylogenetics and Evolution 2, 31–51.
| A 28S rRNA-based phylogeny of the gnathostomes: first steps in the analysis of conflict and congruence with morphologically based cladograms.Crossref | GoogleScholarGoogle Scholar | 8081546PubMed | 8081546PubMed |
Lewis, P. O. (2001). A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology 50, 913–925.
| A likelihood approach to estimating phylogeny from discrete morphological character data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38zntVKlsQ%3D%3D&md5=9cdb01b992e37aeb8db59fce6c23434dCAS | 12116640PubMed | 12116640PubMed |
Linnaeus, C. (1758). ‘Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Generas, Species, cum Characteribus, Differentiis, Synonymis, Locis.’ Revised edition 10. Salvius, Stockholm.
Lissner, A., Phillips, C., Cadien, D., Smith, R., Bernstein, B., Cimberg, R., Kauwling, T., and Anikouchine, W. (1986). Assessment of long-term changes in biological communities of the Santa Maria Basin and Western Santa Barbara Channel. Phase I. Pacific OCS Region, Appendix D. US Department of the Interior Minerals Management Service, Los Angeles, CA.
Lundsten, L., Schlining, K. L., Frasier, K., Johnson, S. B., Kuhnz, L. A., Harvey, J. B., Clague, G., and Vrijenhoek, R. C. (2010). Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA. Deep-sea Research. Part I, Oceanographic Research Papers 57, 1573–1584.
| Time-series analysis of six whale-fall communities in Monterey Canyon, California, USA.Crossref | GoogleScholarGoogle Scholar |
Maddison, W. P., and Maddison, D. R. (2011). Mesquite: a molecular system for evolutionary analysis. Version 2.75. Available at http://mesqiteproject.org
Malm, A. W. (1874). Annulater i hafvet utmed Sveriges vestkust och omkring Göteborg. Göteborgs Kongliga Vetenskaps- och Vitterhetsamhälles Handlingar 14, 67–105.
Marion, A. F. (1874). Sur les annélides du Golfe de Marseille. Comptes Rendu de l’Academie des Sciences 79, 398–401.
Marion, A. F., and Bobretzky, N. (1875). Ètude des annelids du Golfe de Marseilles. Annales des Sciences Naturelles 2, 1–106.
Martin, D., Cuesta, J. A., Drake, P., Gil, J., Nygren, A., and Pleijel, F. (2012). The symbiotic hesionid Parasyllidea humesi Petibone, 1961 (Annelida: Polychaeta) hosted by Scrobicularia plana (da Costa, 1778) (Mollusca: Bivalvia: Semelidade) in European waters. Organisms, Diversity & Evolution 12, 145–153.
| The symbiotic hesionid Parasyllidea humesi Petibone, 1961 (Annelida: Polychaeta) hosted by Scrobicularia plana (da Costa, 1778) (Mollusca: Bivalvia: Semelidade) in European waters.Crossref | GoogleScholarGoogle Scholar |
Nygren, A. (2014). Cryptic polychaete diversity: a review. Zoologica Scripta 43, 172–183.
| Cryptic polychaete diversity: a review.Crossref | GoogleScholarGoogle Scholar |
Nygren, A., and Pleijel, F. (2011). From one to ten in a single stroke – resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex. Molecular Phylogenetics and Evolution 58, 132–141.
| From one to ten in a single stroke – resolving the European Eumida sanguinea (Phyllodocidae, Annelida) species complex.Crossref | GoogleScholarGoogle Scholar | 21034835PubMed | 21034835PubMed |
Nygren, A., Pleijel, F., and Sundberg, P. (2005). Genetic relationships between Nereimyra punctata and N. woodsholea (Hesionidae, Polychaeta). Journal of Zoological Systematics and Evolutionary Research 43, 273–276.
| Genetic relationships between Nereimyra punctata and N. woodsholea (Hesionidae, Polychaeta).Crossref | GoogleScholarGoogle Scholar |
Palumbi, S., Martin, A., Romano, S., McMillan, W., Stice, L., and Grabowski, G. (2002). ‘The Simple Fool’s Guide to PCR. Version 2.’ (University of Hawaii: Honolulu, HI.)
Pleijel, F. (1998). Phylogeny and classification of Hesionidae (Polychaeta). Zoologica Scripta 27, 89–163.
| Phylogeny and classification of Hesionidae (Polychaeta).Crossref | GoogleScholarGoogle Scholar |
Pleijel, F., Rouse, G. W., Ruta, C., Wiklund, H., and Nygren, A. (2008). Vrijenhoekia balaenophila, a new hesionid polychaete from a whale fall off California. Zoological Journal of the Linnean Society 152, 625–634.
| Vrijenhoekia balaenophila, a new hesionid polychaete from a whale fall off California.Crossref | GoogleScholarGoogle Scholar |
Pleijel, F., Rouse, G. W., and Nygren, A. (2009). Five colour morphs and three new species of Gyptis (Hesionidae, Annelida) under a jetty in Edithburgh, South Australia. Zoologica Scripta 38, 89–99.
| Five colour morphs and three new species of Gyptis (Hesionidae, Annelida) under a jetty in Edithburgh, South Australia.Crossref | GoogleScholarGoogle Scholar |
Pleijel, F., Rouse, G. W., Sundkvist, T., and Nygren, A. (2012). A partial revision of Gyptis (Gyptini, Ophiodrominae, Hesionidae, Aciculata, Annelida). Zoological Journal of the Linnean Society 165, 471–494.
| A partial revision of Gyptis (Gyptini, Ophiodrominae, Hesionidae, Aciculata, Annelida).Crossref | GoogleScholarGoogle Scholar |
Plouviez, S., Shank, T. M., Faure, B., Daguin-Theiebaut, C., Viard, F., Lallier, H., and Jollivet, D. (2009). Comparative phylogeography among hydrothermal vent species along the East Pacific Rise reveals vicariant processes and population expansion in the south. Molecular Ecology 18, 3903–3917.
| Comparative phylogeography among hydrothermal vent species along the East Pacific Rise reveals vicariant processes and population expansion in the south.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MnjtVOrtA%3D%3D&md5=d945a6bbcb9a6a4ee665848d19495aceCAS | 19709370PubMed | 19709370PubMed |
Pradillon, F., Schmidt, A., Peplies, J., and Dublier, N. (2007). Species identification of marine invertebrate early stages by whole-larvae in situ hybridization of 18S ribosomal RNA. Marine Ecology Progress Series 333, 103–116.
| Species identification of marine invertebrate early stages by whole-larvae in situ hybridization of 18S ribosomal RNA.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFemt7Y%3D&md5=87d4fc8ff7e0fd020759eaab442a7525CAS |
Rouse, G. W., and Pleijel, F. (2001). ‘Polychaetes.’ (Oxford University Press: Oxford.)
Ruta, C., Nygren, A., Rousset, V., Sundberg, V., Tillier, A., Wiklund, H., and Pleijel, F. (2007). Phylogeny of Hesionidae (Aciculata, Polychaeta), assessed from morphology, 18S rDNA, 28S rDNA, 16S rDNA and COI. Zoologica Scripta 36, 99–107.
| Phylogeny of Hesionidae (Aciculata, Polychaeta), assessed from morphology, 18S rDNA, 28S rDNA, 16S rDNA and COI.Crossref | GoogleScholarGoogle Scholar |
Silvestro, D., and Michalak, I. (2012). raxmlGUI: a graphical front-end for RAxML. Organisms, Diversity & Evolution 12, 335–337.
| raxmlGUI: a graphical front-end for RAxML.Crossref | GoogleScholarGoogle Scholar |
Stamatakis, A. (2006). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688–2690.
| RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfI&md5=df50a1f20f2be0cbcb0dff3c135f1b17CAS | 16928733PubMed | 16928733PubMed |
Stiller, J., Rousset, V., Pleijel, F., Chevaldonné, P., Vrijenhoek, R. C., and Rouse, G. W. (2013). Phylogeny, biogeography and systematics of hydrothermal vent and methane seep Amphisamytha (Ampharetidae, Annelida), with descriptions of three new species. Systematics and Biodiversity 11, 35–65.
| Phylogeny, biogeography and systematics of hydrothermal vent and methane seep Amphisamytha (Ampharetidae, Annelida), with descriptions of three new species.Crossref | GoogleScholarGoogle Scholar |
Swofford, D. (2002). ‘PAUP 4.0 B10: Phylogenetic Analysis using Parsimony.’ (Sinauer: Sunderland, MA.)
Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
| Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=6b4d3dc663a87d2ea977fd9ba4830982CAS | 17654362PubMed | 17654362PubMed |
Uebelacker, J. M. (1984). Hesionidae. In ‘Taxonomic Guide to the Polychaetes of the Northern Gulf of Mexico’. Vol. IV, Ch. 28, pp. 1–39. (Eds J. M. Uebelacker and P. G. Johnson.) (US Department of the Interior Minerals Management Service.)
Vrijenhoek, R. C., Johnson, S. B., and Rouse, G. W. (2009). A remarkable diversity of bone-eating worms (Osedax:Siboglinidae:Annelida). BMC Biology 7, 74.
| A remarkable diversity of bone-eating worms (Osedax:Siboglinidae:Annelida).Crossref | GoogleScholarGoogle Scholar | 19903327PubMed | 19903327PubMed |
Xia, X., and Xie, Z. (2001). DAMBE: software package for data analysis in molecular biology and evolution. The Journal of Heredity 92, 371–373.
| DAMBE: software package for data analysis in molecular biology and evolution.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvptlagtA%3D%3D&md5=bebc9ecc43e1e64e767bfc28ca7a3f3bCAS | 1:STN:280:DC%2BD3MvptlagtA%3D%3D&md5=bebc9ecc43e1e64e767bfc28ca7a3f3bCAS | 11535656PubMed | 11535656PubMed |
Xia, X., Xie, Z., Salemi, M., Chen, L., and Wang, Y. (2003). An index of substitution saturation and its application. Molecular Phylogenetics and Evolution 26, 1–7.
| An index of substitution saturation and its application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1WhtrY%3D&md5=516db0b5c930891faa088dcc6651d0e6CAS | 1:CAS:528:DC%2BD38Xps1WhtrY%3D&md5=516db0b5c930891faa088dcc6651d0e6CAS | 12470932PubMed | 12470932PubMed |