Abstract
Galapagomystides is an exclusively deep-sea group of Phyllodocidae, originally erected for Galapagomystides aristata from hydrothermal vents of the Galapagos Rift. In this study, Phyllodocidae collected from hydrothermal vents and methane seeps from the Pacific Ocean, including specimens from vents of the East Pacific Rise identified as Galapagomystides were studied using morphology (light microscopy and scanning electron microscopy) and DNA sequence data. Phylogenetic analysis of the newly generated molecular data (cytochrome c oxidase subunit I, 16S rRNA, 18S rRNA, and 28S rRNA) combined with an already available extensive dataset for Phyllodocidae resulted in a monophyletic Galapagomystides comprising five species. Galapagomystides aristata was found to occur on the East Pacific Rise vents as well as the Galapagos Rift and is redescribed. Two new species were from hydrothermal vents in the West Pacific, G. bobpearsoni n. sp., and G. kathyae n. sp., as well as one new species from a cold seep in the eastern Pacific, G. patricki n. sp. These new species are formally described, and a previously known vent species, Protomystides verenae, is redescribed and transferred to Galapagomystides. Galapagomystides verenae n. comb. was found to occur in both vents and seeps in the eastern Pacific, from Oregon to Costa Rica. The diagnosis of Galapagomystides is amended and the biogeography and habitat evolution of the five species of Galapagomystides is discussed.
References
Bandelt, H.J., Forster, P. & Röhl, A. (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular biology and evolution, 16, 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
Becker, E.L., Cordes, E.E., Macko, S.A., Lee, R.W. & Fisher, C.R. (2013) Using stable isotope compositions of animal tissues to infer trophic interactions in Gulf of Mexico lower slope seep communities. PloS One 8, e74459. https://doi.org/10.1371/journal.pone.0074459
Bergquist, D.C., Eckner, J.T., Urcuyo, I.A., Cordes, E.E., Hourdez, S., Macko, S.A. & Fisher, C.R. (2007) Using stable isotopes and quantitative community characteristics to determine a local hydrothermal vent food web. Marine Ecology Progress Series, 330, 49–65. https://doi.org/10.3354/meps330049
Blake, J.A. (1985) Polychaeta from the vicinity of deep-sea geothermal vents in the eastern pacific. I. Euphrosinidae, Phyllodocidae, Hesionidae, Nereididae, Glyceridae, Dorvilleidae, Orbiniidae, and Maldanidae. Bulletin of the Biological Society of Washington, 6, 67–101.
Blake, J.A. (1994) Family Phyllodocidae Savigny, 1818. In: Blake, J.A. & Hilbig, B. (Ed.), Taxonomic Atlas of the Benthic Fauna of the Santa Maria Basin and Western Santa Barbara Channel. Vol. 4. The Annelida. Part 2. Science Applications International Corporation, Woods Hole, pp. 115–86.
Blake, J.A. & 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
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) Cryptic species of Archinome (Annelida: Amphinomida) from vents and seeps. Proceedings. Biological Sciences: The Royal Society, 280, 20131876. https://doi.org/10.1098/rspb.2013.1876
Carr, C.M., Hardy, S.M., Brown, T.M., Macdonald, T.A. & Hebert, P.D.N. (2011) A tri-oceanic perspective: DNA barcoding reveals geographic structure and cryptic diversity in Canadian polychaetes. PloS One 6, e22232. https://doi.org/10.1371/journal.pone.0022232
Chapman, A.S.A., Tunnicliffe, V. & Bates, A.E. (2018) Both rare and common species make unique contributions to functional diversity in an ecosystem unaffected by human activities. Diversity & Distributions, 24, 568–78. https://doi.org/10.1111/ddi.12712
Chevaldonné, P., Jollivet, D., Desbruyères, D., Lutz, R. & Vrijenhoek, R. (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.
Cordes, E.E., Carney, S.L., Hourdez, S., Carney, R.S., Brooks, J.M. & Fisher, C.R. (2007) Cold seeps of the deep Gulf of Mexico: Community structure and biogeographic comparisons to Atlantic equatorial belt seep communities. Deep Sea Research Part I: Oceanographic Research Papers, 54, 637–653. https://doi.org/10.1016/j.dsr.2007.01.001
Darriba, D., Posada, D., Kozlov, A.M., Stamatakis, A., Morel, B. & Flouri, T. (2020) ModelTest-NG: a new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37, 291–94. https://doi.org/10.1093/molbev/msz189
Desbruyères, D. & Segonzac, M. (1997) Handbook of deep-sea hydrothermal vent fauna. IFREMER, Brest, 279 pp.
Desbruyères, D., Segonzac, M. & Bright, M. (Eds.) (2006) Handbook of deep-sea hydrothermal vent fauna. Denisia, Linz, 5 pp.
Dreyer, J.C. (2004) Stability at hydrothermal-vent mussel beds: dynamics at hydrothermal vents: evidence for stable macrofaunal communities in mussel beds on the northern East Pacific Rise. MA from College of William and Mary. Available from: https://doi.org/10.21220/s2-e641-wn93 (accessed 5 April 2022)
Edler, D., Klein, J., Antonelli, A. & Silvestro, D. (2021) raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution, 12, 373–77. https://doi.org/10.1111/2041-210X.13512
Eklöf, J., Pleijel, F. & Sundberg, P. (2007) Phylogeny of benthic Phyllodocidae (Polychaeta) based on morphological and molecular data. Molecular Phylogenetics and Evolution, 45, 261–71. https://doi.org/10.1016/j.ympev.2007.04.015
Giribet, G., Carranza, S., Baguna, J., Riutort, M. & Ribera C. (1996) First molecular evidence for the existence of a Tardigrada Arthropoda clade. Molecular Biology and Evolution, 13, 76–84. https://doi.org/10.1093/oxfordjournals.molbev.a025573.
Gollner, S., Govenar, B., Fisher, C.R. & Bright, M. (2015) Size matters at deep-sea hydrothermal vents: different diversity and habitat fidelity patterns of meio- and macrofauna. Marine Ecology Progress Series, 520, 57–66. https://doi.org/10.3354/meps11078
Govenar, B.W., Bergquist, D.C., Urcuyo, I.A., Eckner, J.T. & Fisher, C.R. (2002) Three Ridgeia piscesae assemblages from a single Juan de Fuca Ridge sulphide edifice: structurally different and functionally similar. Cahiers de Biologie Marine, 43, 247–52.
Govenar, B.W., Freeman, M., Bergquist, D.C., Johnson, G.A. & Fisher, C.R. (2004) Composition of a one-year-old Riftia Pachyptila community following a clearance experiment: insight to succession patterns at deep-sea hydrothermal vents. The Biological Bulletin, 207, 177–82. https://doi.org/10.2307/1543204
Govenar, B.W., Le Bris, N., Gollner, S., Glanville, J., Aperghis, A.B., Hourdez, S. & Fisher, C.R. (2005) Epifaunal community structure associated with Riftia Pachyptila aggregations in chemically different hydrothermal vent habitats. Marine Ecology Progress Series, 305, 67–77. https://doi.org/10.3354/meps305067
Govenar, B.W. & Fisher, C.R. (2007) Experimental evidence of habitat provision by aggregations of Riftia Pachyptila at hydrothermal vents on the East Pacific Rise. Marine Ecology, 28, 3–14. https://doi.org/10.1111/j.1439-0485.2007.00148.x
Hartman, O. (1936) A review of the Phyllodocidae (Annelida, Polychaeta) of the coast of California, with descriptions of nine new species. University of California Publications in Zoology, 41, 117–132.
Hatch, A.S., Liew, H., Hourdez, S. & Rouse, G.W. (2020) Hungry scale worms: phylogenetics of Peinaleopolynoe (Polynoidae, Annelida), with four new species. ZooKeys, 932, 27–74. https://doi.org/10.3897/zookeys.932.48532
Imajima, M. (2001) Deep-sea benthic polychaetous annelids of Tosa Bay, southwestern Japan. National Science Museum Monographs, 20, 31–100.
Jenkins, C.D., Ward, M.E., Turnipseed, M., Osterberg, J. & Van Dover, C.L. (2002) The digestive system of the hydrothermal vent polychaete Galapagomystides aristata (Phyllodocidae): evidence for hematophagy? Invertebrate Biology, 121, 243–254. https://doi.org/10.1111/j.1744-7410.2002.tb00064.x
Jimi, N., Kimura, T., Ogawa, A. & Kajihara, H. (2020) Alien worm in worm: a new genus of endoparasitic polychaete (Phyllodocidae, Annelida) from scale worms (Aphroditidae and Polynoidae, Annelida). Systematics and Biodiversity, 19, 13–21. https://doi.org/10.1080/14772000.2020.1785038
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–80. https://doi.org/10.1093/molbev/mst010
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C. & Thierer, T. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28, 1647–49. https://doi.org/10.1093/bioinformatics/bts199
Kelly, N., Metaxas, A. & Butterfield, D. (2007) Spatial and temporal patterns of colonization by deep-sea hydrothermal vent invertebrates on the Juan de Fuca Ridge, NE Pacific. Aquatic Biology, 1, 1–16. https://doi.org/10.3354/ab00001
Kiel, S. (2016) A biogeographic network reveals evolutionary links between deep-sea hydrothermal vent and methane seep faunas. Proceedings of the Royal Society B: Biological Sciences, 283, 2016–2337. https://doi.org/10.1098/rspb.2016.2337
Kobayashi, G. & Kojima, S. (2017) First record of Protomystides hatsushimaensis (Annelida: Phyllodocidae) inhabiting vacant tubes of vestimentiferan tubeworms. Marine Biodiversity Records, 10, 25. https://doi.org/10.1186/s41200-017-0127-9
Kozlov, M.A., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. (2019) RAxML-NG: A fast, scalable, and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics, 35, 4453–4455. https://doi.org/10.1093/bioinformatics/btz305
Krylova, E.M. & Sahling, H. (2010) Vesicomyidae (Bivalvia): current taxonomy and distribution. PloS One, 5, e9957. https://doi.org/10.1371/journal.pone.0009957
Le, H.L., Lecointre, G. & 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. https://doi.org/10.1006/mpev.1993.1005
Leigh, J.W., Bryant, D. & Nakagawa, S. (2015) POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution, 6, 1110–1116. https://doi.org/10.1111/2041-210X.12410
Leiva, C., Riesgo, A., Avila, C., Rouse, G.W. & Taboada, S. (2018) Population structure and phylogenetic relationships of a new shallow-water Antarctic phyllodocid annelid. Zoologica Scripta, 47, 714–26. https://doi.org/10.1111/zsc.12313
Lelièvre, Y., Sarrazin, J., Marticorena, J., Schaal, G., Day, T., Legendre, P., Hourdez, S. & Matabos, M. (2017) Biodiversity and trophic ecology of hydrothermal vent fauna associated with tubeworm assemblages on the Juan de Fuca Ridge. Biogeosciences Discussions, 2017, 1–34. https://doi.org/10.5194/bg-2017-411
Levin, L., Baco, A., Bowden, D., Colaco, A., Cordes, E., Cunha, M., Demopoulos, A., Gobin, J., Grupe, B., Le, J., Metaxas, A., Netburn, A., Rouse, G., Thurber, A., Tunnicliffe, V., Dover, C.V., Vanreusel, A. & Watling, L. (2016) Hydrothermal vents and methane seeps: Rethinking the sphere of influence. Frontiers in Marine Science, 3, 72.
https://doi.org/10.3389/fmars.2016.00072
Lewis, P.O. (2001) A likelihood approach to estimating phylogeny from discrete morphological character data. Systematic Biology, 50, 913–25. https://doi.org/10.1080/106351501753462876
Lockyer, A.E., Olson, P.D. & Littlewood, D.T.J. (2003) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): Implications and a review of the cercomer theory. Biological Journal of the Linnean Society, 78, 155–71. https://doi.org/10.1046/j.1095-8312.2003.00141.x
Maddison, W.P. & Maddison, D.R. (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61. Available from: http://www.mesquiteproject.org (accessed 28 September 2021)
McCowin, M.F., Feehery, C. & Rouse, G.W. (2020) Spanning the depths or depth-restricted: three new species of Bathymodiolus (Bivalvia, Mytilidae) and a new record for the hydrothermal vent Bathymodiolus Thermophilus at methane seeps along the Costa Rica Margin. Deep Sea Research Part I: Oceanographic Research Papers, 164, 103–322. https://doi.org/10.1016/j.dsr.2020.103322
McCowin, M.F. & Rouse, G.W. (2018) A New Lamellibrachia species and confirmed range extension for Lamellibrachia Barhami (Siboglinidae, Annelida) from Costa Rica methane seeps. Zootaxa, 4504 (1), 1–22. https://doi.org/10.11646/zootaxa.4504.1.1
Milligan, B.N. & Tunnicliffe, V. (1994) Vent and nonvent faunas of Cleft Segment, Juan de Fuca Ridge, and their relations to lava age. Journal of Geophysical Research, 99, 4777–4786. https://doi.org/10.1029/93JB03210
Miura, T. (1988) A new species of the genus Protomystides (Annelida, Polychaeta) associated with a Vestimentiferan worm from the Hatsushima Cold-Seep site. Japanese Society of Systematic Zoology, 38, 10–14.
Muir, A. & Maruf Hossain, M.M. (2014) The intertidal polychaete (Annelida) fauna of the Sitakunda coast (Chittagong, Bangladesh), with notes on the Capitellidae, Glyceridae, Lumbrineridae, Nephtyidae, Nereididae and Phyllodocidae of the “Northern Bay of Bengal Ecoregion.” ZooKeys, 419, 1–27. https://doi.org/10.3897/zookeys.419.7557
Palumbi, S.R., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The simple fool’s guide to PCR. Version 2.0. University of Hawaii, Honolulu, 45 pp.
Peek, A.S., Gustafson, R.G., Lutz, R.A. & Vrijenhoek, R.C. (1997) Evolutionary relationships of deep-sea hydrothermal vent and cold-water seep clams (Bivalvia: Vesicomyidae): results from the mitochondrial cytochrome oxidase subunit I. Marine Biology, 130, 151–61. https://doi.org/10.1007/s002270050234
Pleijel, F. (1991) Phylogeny and classification of the Phyllodocidae (Polychaeta). Zoologica Scripta, 20, 225–261. https://doi.org/10.1111/j.1463-6409.1991.tb00289.x
Rodrigo, A.P., Costa, M.H., de Matos, A.P.A., Carrapiço, F. & Costa, P.M. (2015) A study on the digestive physiology of a marine polychaete (Eulalia viridis) through microanatomical changes of epithelia during the digestive cycle. Microscopy and Microanalysis, 21, 91–101. https://doi.org/10.1017/S143192761401352X
Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–42. https://doi.org/10.1093/sysbio/sys029
Rouse, G.W. & Kupriyanova, E.K. (2021) Laminatubus (Serpulidae, Annelida) from Eastern Pacific hydrothermal vents and methane seeps, with description of two new species. Zootaxa, 4915 (1), 1–27. https://doi.org/10.11646/zootaxa.4915.1.1
Rouse, G.W. & Pleijel, F. (2003) Problems in polychaete systematics. Hydrobiologia, 496, 175–89. https://doi.org/10.1023/A:1026188630116
Rouse, G.W., Pleijel, F. & Tilic, E. (2022) Annelida. Oxford University Press, London/New York, 418 pp.
San Martín, G., Álvarez-Campos, P., Kondo, Y., Núñez, J., Fernández-Álamo, M.A., Pleijel, F., Goetz, F.E., Nygren, A. & Osborn, K. (2021) New symbiotic association in marine annelids: Ectoparasites of comb jellies. Zoological Journal of the Linnean Society, 191, 672–694. https://doi.org/10.1093/zoolinnean/zlaa034
Sibuet, M. & Olu, K. (1998) Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Research. Part II, Topical Studies in Oceanography, 45, 517–67. https://doi.org/10.1016/S0967-0645(97)00074-X
Smith, C.R. & Baco, A.R. (1998) Phylogenetic and functional affinities between whale-fall, seep and vent chemoautotrophic communities. Cahiers de Biologie Marine, 39, 345–346.
Solís-Weiss, V. & Hernández-Alcántara, P. (1994) Amphisamytha fauchaldi: a new species of ampharetid (Annelida: Polychaeta) from the hydrothermal vents at Guaymas Basin, Mexico. Bulletin of the Southern California Academy of Sciences, 93, 127–134.
Stamatakis, A. (2014) RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30, 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Stiller, J., Rousset, V., Pleijel, F., Chevaldonné, P., Vrijenhoek, R.C. & 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. https://doi.org/10.1080/14772000.2013.772925
Tsurumi, M. & Tunnicliffe, V. (2003) Tubeworm-associated communities at hydrothermal vents on the Juan de Fuca Ridge, Northeast Pacific. Deep Sea Research Part I: Oceanographic Research Papers, 50, 611–29. https://doi.org/10.1016/S0967-0637(03)00039-6
Tunnicliffe, V. (1992) The nature and origin of the modern hydrothermal vent fauna. Palaios, 7, 338–2350. https://doi.org/10.2307/3514820
Tunnicliffe, V., Juniper, S.K. & Sibuet, M. (2003) Reducing environments of the deep-sea floor. In: Tyler, P.A. (Ed.), Ecosystems of the world. 28. Ecosystems of the Deep Oceans. Elsevier, Amsterdam, pp. 81–110.
Tunnicliffe, V., McArthur, A.G. & McHugh, D. (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Advances in Marine Biology, 34, 353–442. https://doi.org/10.1016/S0065-2881(08)60213-8
Tyler, P.A., German, C.R., Ramirez-Llodra, E. & Van Dover, C.L. (2002) Understanding the biogeography of chemosynthetic ecosystems. Oceanologica Acta, 25, 227–241. https://doi.org/10.1016/S0399-1784(02)01202-1
Vaidya, G., Lohman, D.J. & Meier, R. (2011) SequenceMatrix: concatenation software for the fast assembly of multi-gene datasets with character set and codon information. Cladistics, 27, 171–180. https://doi.org/10.1111/j.1096-0031.2010.00329.x
Van Dover, C. (2000) The Ecology of Deep-sea Hydrothermal Vents. Princeton University Press, Princeton, New Jersey, 424 pp.
Van Dover, C.L. (2002) Community structure of mussel beds at deep-sea hydrothermal vents. Marine Ecology Progress Series, 230, 137–158. https://doi.org/10.3354/meps230137
Warèn, A. & Bouchet, P. (1989) New gastropods from East Pacific hydrothermal vents. Zoologica Scripta, 18, 67–102. https://doi.org/10.1111/j.1463-6409.1989.tb00124.x
Watanabe, H., Fujikura, K., Kojima, S., Miyazaki, J.I. & Fujiwara, Y. (2010) Japan: vents and seeps in close proximity. In: Kiel, S. (Ed.), The Vent and Seep Biota. Vol. 33. Aspects from Microbes to Ecosystems. Springer, Dordrecht, pp. 379–401. https://doi.org/10.1007/978-90-481-9572-5_12
Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology, 46, 1–68. https://doi.org/10.1093/sysbio/46.1.1
Wolff, T. (2005) Composition and endemism of the deep-sea hydrothermal vent fauna. Cahiers de Biologie Marine, 46, 97–104.
Yen, N.K. & Rouse, G.W. (2020) Phylogeny, biogeography and systematics of Pacific vent, methane seep, and whale-fall Parougia (Dorvilleidae: Annelida), with eight new species. Invertebrate Systematics, 34, 200–233. https://doi.org/10.1071/IS19042.