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Depth-dependent gene flow in Gulf of Mexico cold seep Lamellibrachia tubeworms (Annelida, Siboglinidae)

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Abstract

Lamellibrachia vestimentiferan tubeworms form aggregations at hydrocarbon cold seeps in the deep Gulf of Mexico (GoM), creating structures that provide living space for other fauna. In the GoM, three Lamellibrachia taxa vary in morphology and depth ranges: Lamellibrachia luymesi (300–950 m), Lamellibrachia sp. 1 (950–2,604 m), and Lamellibrachia sp. 2 (1,175–3,304 m). While Lamellibrachia sp. 2 is consistently identified as a separate species, L. luymesi and sp. 1 cannot be discriminated using barcoding markers cytochrome oxidase subunit 1 (COI) and large ribosomal subunit rDNA (16S). To determine if limited gene flow was a factor in the formation of these taxa, we employed more quickly evolving markers, including mitochondrial cytochrome B (CYTB), hemoglobin subunit B2 intron (HbB2i), and six polymorphic microsatellites; microsatellites were amplified across 45 L. luymesi and sp. 1 individuals. Additionally, we used microsatellites to ask whether populations of Lamellibrachia sp. 1 and sp. 2 show evidence of significant structure. Despite a lack of resolution seen with CYTB and HbB2i, L. luymesi and sp. 1 form genetically differentiated clusters at the cross-amplified microsatellites. Furthermore, we find no evidence for population structure for either Lamellibrachia sp. 1 or sp. 2 across the GoM.

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References

  • Andersen, A. C., S. Hourdez, B. Marie, D. Jollivet, F. H. Lallier & M. Sibuet, 2004. Escarpia southwardae sp. nov., a new species of vestimentiferan tubeworm (Annelida, Siboglinidae) from West African cold seeps. Canadian Journal of Zoology 82: 980–999.

    Article  Google Scholar 

  • Aquino-Souza, R., S. J. Hawkins & P. A. Tyler, 2008. Early development and larval survival of Psammechinus miliaris under deep-sea temperature and pressure conditions. Journal of the Marine Biological Association of the United Kingdom 88: 453–461.

    Article  Google Scholar 

  • Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.

    Article  CAS  PubMed  Google Scholar 

  • Bazin, E., S. Glémin & N. Galtier, 2006. Population size does not influence mitochondrial genetic diversity in animals. Science 312: 570–571.

    Article  CAS  PubMed  Google Scholar 

  • Becker, E. L., S. A. Macko, R. W. Lee & C. R. Fisher, 2011. Stable isotopes provide new insights into vestimentiferan physiological ecology at Gulf of Mexico cold seeps. Naturwissenschaften 98: 169–174.

    Article  CAS  PubMed  Google Scholar 

  • Benjamini, Y. & D. Yekutieli, 2001. The control of the false discovery rate in multiple testing under dependency. Annals of Statistics 29: 1165–1188.

    Article  Google Scholar 

  • Bergquist, D. C., I. A. Urcuyo & C. R. Fisher, 2002. Establishment and persistence of seep vestimentiferan aggregations on the upper Louisiana slope of the Gulf of Mexico. Marine Ecology Progress Series 241: 89–98.

    Article  Google Scholar 

  • Bergquist, D. C., T. Ward, E. E. Cordes, T. McNelis, S. Howlett, R. Kosoff, S. Hourdez, R. Carney & C. R. Fisher, 2003a. Community structure of vestimentiferan-generated habitat islands from Gulf of Mexico cold seeps. Journal of Experimental Marine Biology and Ecology 289: 197–222.

    Article  Google Scholar 

  • Bergquist, D. C., J. P. Andras, T. McNelis, S. Howlett, M. J. Van Horn & C. R. Fisher, 2003b. Succession in Gulf of Mexico cold seep vestimentiferan aggregations: the importance of spatial variability. Marine Ecology 24: 31–44.

    Article  Google Scholar 

  • Black, M. B., K. M. Halanych, P. A. Y. Maas, W. R. Hoeh, J. Hashimoto, D. Desbruyeres, R. A. Lutz & R. C. Vrijenhoek, 1997. Molecular systematics of vestimentiferan tubeworms from hydrothermal vents and cold-water seeps. Marine Biology 130: 141–149.

    Article  CAS  Google Scholar 

  • Brooks, J. M., M. C. Kennicutt, C. R. Fisher, S. A. Macko, K. Cole, J. J. Childress, R. R. Bidigare & R. D. Vetter, 1987. Deep-sea hydrocarbon seep communities – evidence for energy and nutritional carbon sources. Science 238: 1138–1142.

    Article  CAS  PubMed  Google Scholar 

  • Broughton, R. E. & R. G. Harrison, 2003. Nuclear gene genealogies reveal historical, demographic and selective factors associated with speciation in field crickets. Genetics 163: 1389–1401.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brown, J. H., 1984. On the relationships between abundance and distribution of species. American Naturalist 124: 255–279.

    Article  Google Scholar 

  • Bruun, A., 1957. Deep sea and abyssal depths. Treatise on Marine Ecology and Paleoecology 1: 641–672.

    Google Scholar 

  • Cairns, S. D., D. M. Opresko, T. S. Hopkins & W. W. Schroeder, 1993. New records of deep-water Cnidaria (Scleractinia & Antipatharia) from the Gulf of Mexico. Northeast Gulf Science 13: 1–11.

    Google Scholar 

  • Calabrese, J. M. & W. F. Fagan, 2004. Lost in Time: lonely and single: productive asynchrony and the Allee Effect. American Naturalist 164: 25–37.

    Article  PubMed  Google Scholar 

  • Carney, R., 1994. Consideration of the oasis analogy for chemosynthetic communities at Gulf of Mexico hydrocarbon vents. Geo-Marine Letters 14: 149–159.

    Article  Google Scholar 

  • Carney, R. S., 2005. Zonation of deep biota on continental margins. Oceanography and Marine Biology: An Annual Review 43: 211–278.

    Article  Google Scholar 

  • Chelton, D. S. & M. G. Schlax, 1996. Global observations of oceanic Rossby waves. Science 272: 234–238.

    Article  CAS  Google Scholar 

  • Childress, J. J. & C. R. Fisher, 1992. The biology of hydrothermal vent animals – physiology, biochemistry and autotrophic symbioses. Oceanography and Marine Biology: An Annual Review 30: 337–441.

    Google Scholar 

  • Chybicki, I. & J. Burczyk, 2009. Simultaneous Estimation of Null Alleles and Inbreeding Coefficients. Journal of Heredity 100: 106–113.

    Article  CAS  PubMed  Google Scholar 

  • Cordes, E. E., D. C. Bergquist, B. L. Predmore, C. Jones, P. Deines, G. Telesnicki & C. R. Fisher, 2006. Alternate unstable states: convergent paths of succession in hydrocarbon-seep tubeworm-associated communities. Journal of Experimental Marine Biology and Ecology 339: 159–176.

    Article  CAS  Google Scholar 

  • Cordes, E. E., S. L. Carney, S. Hourdez, R. S. Carney, J. M. Brooks & C. R. Fisher, 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 54: 637–653.

    Article  Google Scholar 

  • Cordes, E. E., D. C. Bergquist & C. R. Fisher, 2009. Macro-ecology of Gulf of Mexico cold seeps. Annual Review of Marine Science 1: 143–168.

    Article  PubMed  Google Scholar 

  • Cordes, E. E., E. L. Becker, S. Hourdez & C. R. Fisher, 2010. Influence of foundation species, depth, and location on biodiversity and structure of cold seep macrofaunal communities on the lower slope of the Gulf of Mexico. Deep-Sea Research Part II 57: 1870–1881.

    Article  Google Scholar 

  • Cowart, D. A., C. Huang & S. W. Schaeffer, 2012. Identification and amplification of microsatellite loci in deep-sea tubeworms of the genus Escarpia (Polychaeta, Siboglinidae). Conservation Genetics Resources 5: 479–482.

    Article  Google Scholar 

  • Cowart, D. A., C. Huang, S. Arnaud-Haond, S. L. Carney, C. R. Fisher & S. W. Schaeffer, 2013. Restriction to large-scale gene flow versus regional panmixia among cold seep Escarpia spp. (Polychaeta, Siboglinidae). Molecular Ecology 22: 4147–4162.

    Article  CAS  PubMed  Google Scholar 

  • Edgar, R. C., 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792–1797.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Etter, R. J. & M. A. Rex, 1990. Population differentiation decreases with depth in deep-sea gastropods. Deep-Sea Research Part A. Oceanographic Research Papers 37: 1251–1261.

    Article  Google Scholar 

  • Etter, R., M. A. Rex, M. R. Chase & J. M. Quattro, 2005. Population differentiation decreases with depth in deep-sea bivalves. Evolution 59: 1479–1491.

    Article  PubMed  Google Scholar 

  • Excoffier, L., P. Smouse & J. Quattro, 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131: 479–491.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Freytag, J. K., P. R. Girguis, D. C. Bergquist, J. P. Andras, J. J. Childress & C. R. Fisher, 2001. A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proceedings of the National Academy of Science of the United States of America 98: 13408–13413.

    Article  CAS  Google Scholar 

  • Gage, J. D. & P. A. Tyler, 1991. Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Gage, J. D. & P. A. Tyler, 1992. Deep-Sea Biology: A Natural History of Organisms at the Deep-Sea Floor. Cambridge University Press, Cambridge.

    Google Scholar 

  • Galtier, N., B. Nabholz, S. Glémin & G. D. D. Hurst, 2009. Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18: 4541–4550.

    Article  CAS  PubMed  Google Scholar 

  • Gelfand, Y., A. Rodriguez & G. Benson, 2006. TRDB – The Tandem Repeat Database. Nucleic Acids Research 35: D80–D87.

    Article  PubMed Central  PubMed  Google Scholar 

  • Goudet, J., 1995. FSTAT (version 1.2): a computer program to calculate F-Statistics. Journal of Heredity 86: 485–486.

    Google Scholar 

  • Hartl, D. L. & A. G. Clark, 2007. Principles of Population Genetics, 4th ed. Sinauer Associates, Sunderland.

    Google Scholar 

  • Hamilton, P., 1990. Deep currents in the Gulf of Mexico. Journal of Physical Oceanography 20: 1180–1207.

    Article  Google Scholar 

  • Hamilton, P., 2007. Deep-current variability near the Sigsbee Escarpment in the Gulf of Mexico. Journal of Physical Oceanography 37: 708–726.

    Article  Google Scholar 

  • Hebert, P. D. N., S. Ratnasingham & J. R. de Waard, 2003. Barcoding animal of life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London Part B 270: S96–S99.

    Article  CAS  Google Scholar 

  • Howell, K., A. Rogers, P. Tyler & D. M. Billett, 2004. Reproductive isolation among morphotypes of the Atlantic seastar species Zoroaster fulgens (Asteroidea: Echinodermata). Marine Biology 144: 977–984.

    Article  Google Scholar 

  • Jennings, R. M., R. J. Etter & L. Ficarra, 2013. Population differentiation and species formation in the deep sea: the potential role of environmental gradients and depth. PLoS ONE 8: e77594.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Johns, G. C. & J. C. Avise, 1998. A comparative summary of genetic distances in the vertebrates from the mitochondrial cytochrome b gene. Molecular Biology and Evolution 15: 1481–1490.

    Article  CAS  PubMed  Google Scholar 

  • Jones, M., 1985. On the Vestimentifera, new phylum: six new species, and other taxa, from hydrothermal vents and elsewhere. Bulletin of the Biological Society of Washington 6: 117–158.

    Google Scholar 

  • Julian, D., F. Gaill, E. Wood, A. J. Arp & C. R. Fisher, 1999. Roots as a site of hydrogen sulfide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia sp. Journal of Experimental Biology 202: 2245–2257.

    CAS  PubMed  Google Scholar 

  • Kalinowski, S., 2005. HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Resources 5: 187–189.

    Article  CAS  Google Scholar 

  • Kennicutt, M. C., J. M. Brooks, R. R. Bidigare & G. J. Denoux, 1988. Gulf of Mexico hydrocarbon seep communities – I. Regional distribution of hydrocarbon seepage and associated fauna. Deep-Sea Research Part A. Oceanographic Research Papers 35: 1639–1651.

    Article  CAS  Google Scholar 

  • Kocot, K. M., J. T. Cannon, C. Todt, M. R. Citarella, A. B. Kohn, A. Meyer, S. R. Santos, C. Schander, L. L. Moroz, B. Lieb & K. M. Halanych, 2011. Phylogenomics reveals deep molluscan relationships. Nature 477: 452–456.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lalli, C. M. & T. R. Parsons, 1993. Biological Oceanography: An Introduction. Butterworth-Heinemann, Oxford.

    Google Scholar 

  • MacArthur, R. H., 1972. Geographical Ecology: Patterns in the Distribution of Species. Princeton University Press, Princeton.

    Google Scholar 

  • Maddison, W. P. & L. L. Knowles, 2006. Inferring phylogeny despite incomplete lineage sorting. Systematic Biology 55: 21–30.

    Article  PubMed  Google Scholar 

  • Mallet, J., 1995. A species definition for the modern synthesis. Trends in Ecology & Evolution 10: 294–299.

    Article  CAS  Google Scholar 

  • McMullin, E. R., S. Hourdez, S. W. Schaeffer & C. R. Fisher, 2003. Phylogeny and biogeography of deep sea vestimentiferan tubeworms and their bacterial symbionts. Symbiosis 34: 1–41.

    Google Scholar 

  • McMullin, E. R., J. Wood & S. Hamm, 2004. Twelve microsatellites for two deep sea polychaete tubeworm species, Lamellibrachia luymesi and Seepiophila jonesi, from the Gulf of Mexico. Molecular Ecology Notes 4: 1–4.

    Article  CAS  Google Scholar 

  • McMullin, E., K. Nelson, C. R. Fisher & S. W. Schaeffer, 2010. Population structure of two deep sea tubeworms, Lamellibrachia luymesi and Seepiophila jonesi, from the hydrocarbon seeps of the Gulf of Mexico. Deep-Sea Research Part I 57: 1499–1509.

    Article  CAS  Google Scholar 

  • Meirmans, P. & P. W. Hedrick, 2011. Assessing population structure: FST and related measures. Molecular Ecology Research 11: 5–18.

    Article  Google Scholar 

  • Miglietta, M. P., S. Hourdez, D. A. Cowart, S. W. Schaeffer & C. R. Fisher, 2010. Species boundaries of Gulf of Mexico vestimentiferans (Polychaeta, Siboglinidae) inferred from mitochondrial genes. Deep-Sea Research Part II 57: 1916–1925.

    Article  CAS  Google Scholar 

  • Minerals Management Service Gulf of Mexico, 2006. Gulf of Mexico OCS Oil and Gas Lease Sales: 2007–2012. Western Planning Area Sales 204, 207, 210, 215, and 218. Central Planning Area Sales 205, 206, 208, 213, 216, and 222. Draft Environmental Impact Statement. Volume II, pp. 1–170, Figure 173–179, page 115. U.S. Department of the Interior.

  • Miura, T. & S. Kojima, 2006. Two new species of vestimentiferan tubeworm (Polychaeta: Siboglinidae aka Pogonophora) from the Brothers Caldera, Kermadec Arc, South Pacific Ocean. Species Diversity 11: 209–224.

    Google Scholar 

  • Miura, T., J. Tsukahara & J. Hashimoto, 1997. Lamellibrachia satsuma, a new species of vestimentiferan worms bay, Japan. Proceedings of the Biological Society of Washington 110: 447–456.

    Google Scholar 

  • Moalic, Y., S. Arnaud-Haond, C. Perrin, G. A. Pearson & E. A. Serrao, 2011. Travelling in time with networks: revealing present day hybridization versus ancestral polymorphism between two species of brown algae, Fucus vesiculosus and F. spiralis. BMC Evolutionary Biology 11: 33–46.

    Article  PubMed Central  PubMed  Google Scholar 

  • Oliphant, A., S. Thatje, A. Brown, M. Morini, J. Ravaux & B. Shillito, 2011. Pressure tolerance of the shallow-water caridean shrimp Palaemonetes varians across its thermal tolerance window. Experimental Biology 214: 1109–1117.

    Article  Google Scholar 

  • Palumbi, S., 1994. Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology, Evolution and Systematics 25: 547–572.

    Article  Google Scholar 

  • Pradillon, F. & F. Gaill, 2007. Pressure and life: some biological strategies. Reviews in Environmental Science and Bio/Technology 6: 181–195.

    Article  Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed Central  PubMed  Google Scholar 

  • R Core Development Team, 2009. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

    Google Scholar 

  • Raymond, M. & F. Rousset, 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248–249.

    Google Scholar 

  • Rex, M. A. & R. J. Etter, 2010. Deep-Sea Biodiversity: Pattern and Scale. Harvard University Press, Cambridge.

    Google Scholar 

  • Roberts, H., R. Carney, M. Kupchik, C. R. Fisher, K. Nelson, E. Becker, L. Goehring, S. Lessard-Pilon, G. Telesnicki, B. Bernard, J. Brooks, M. Bright, E. Cordes, S. Hourdez, J. Hunt, W. Shedd, G. Boland, S. Joye, V. Samarkin, M. Bernier, M. Bowles, I. MacDonald, H. Niemann, C. Petersen, C. Morrison & J. Potter, 2007. ALVIN explores the deep northern Gulf of Mexico slope. EOS Transactions American Geophysical Union 88: 341–342.

    Article  Google Scholar 

  • Rocha, L. A., D. R. Robertson, J. Roman & B. W. Bowen, 2005. Ecological speciation in tropical reef fishes. Proceedings of the Royal Society B: Biological Sciences 272: 573–579.

    Article  PubMed Central  PubMed  Google Scholar 

  • Root, R. B., 1967. The niche exploitation pattern of the blue-gray gnatcatcher. Ecological Monographs 37: 317–350.

    Article  Google Scholar 

  • Rozen, S. & H. Skaletsky, 1999. Primer3 on the WWW for general users and for biologist programmers. Bioinformatics Methods and Protocols 132: 365–386.

    Article  Google Scholar 

  • Rozenfeld, A., S. Arnaud-Haond, E. Hernández-García, V. M. Eguíluz, M. A. Matías, E. Serrão & C. M. Duarte, 2007. Spectrum of genetic diversity and networks of clonal organisms. Journal of the Royal Society Interface 4: 1093–1102.

    Article  PubMed Central  Google Scholar 

  • Rozenfeld, A., S. Arnaud-Haond, E. Hernández-García, V. M. Eguíluz, E. A. Serrão & C. M. Duarte, 2008. Network analysis identifies weak and strong links in a metapopulation system. Proceedings of the National Academy of Sciences 105: 18824–18829.

    Article  Google Scholar 

  • Sammarco, P. W., D. A. Brazeau & J. Sinclair, 2012. Genetic connectivity in scleractinian corals across the northern Gulf of Mexico: oil/gas platforms, and relationship to the Flower Garden Banks. PLoS ONE 7: e30144.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sang, T., 2002. Utility of low-copy nuclear gene sequences in plant phylogenetics. Critical Reviews in Biochemistry and Molecular Biology 37: 121–147.

    Article  CAS  PubMed  Google Scholar 

  • Saunders, P. M. & N. P. Fofonoff, 1976. Conversion of pressure to depth in the ocean. Deep-Sea Research 23: 109–111.

    Google Scholar 

  • Schluter, D. N. & L. M. Nagel, 1995. Parallel speciation by natural selection. American Naturalist 146: 292–301.

    Article  Google Scholar 

  • Schneider, S. & H. Lischer, 2009. ARLEQUIN, Version 3.5. An Integrated Software Package for Population Genetics Data Analysis. University of Berne, Berne.

    Google Scholar 

  • Schuelke, M., 2000. An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233–234.

    Article  CAS  PubMed  Google Scholar 

  • Shilling, F. M. & D. T. Manahan, 1994. Energy metabolism and amino acid transport during early development of Antarctic and temperate echinoderms. Biological Bulletin 187: 398–407.

    Article  CAS  Google Scholar 

  • Sibuet, M. & K. Olu, 1998. Biogeography, biodiversity and fluid dependence of deep-sea cold-seep communities at active and passive margins. Deep-Sea Research Part II 45: 517–567.

    Article  Google Scholar 

  • Somero, G. N., 1992a. Biochemical ecology of deep-sea animals. Cellular and Molecular Life Sciences 48: 537–543.

    Article  CAS  Google Scholar 

  • Somero, G. N., 1992b. Adaptations to high hydrostatic pressure. Annual Review of Physiology 54: 557–577.

    Article  CAS  PubMed  Google Scholar 

  • Southward, E. C., 1991. Three new species of Pogonophora, including two vestimentiferans, from hydrothermal sites in the Lau Back-arc Basin (Southwest Pacific Ocean). Journal of Natural History 25: 859–881.

    Article  Google Scholar 

  • Southward, E. C., A. C. Andersen & S. Hourdez, 2011. Lamellibrachia anaximandri n. sp., a new vestimentiferan tubeworm (Annelida) from the Mediterranean, with notes on frenulate tubeworms from the same habitat. Zoosystema 33: 245–279.

    Article  Google Scholar 

  • Stauffer, D. & A. Aharony, 1994. Introduction to Percolation Theory. Taylor and Francis, London.

    Google Scholar 

  • Storey, J. & R. Tibshirani, 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences 100: 9440–9445.

    Article  CAS  Google Scholar 

  • Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    CAS  PubMed  Google Scholar 

  • Tamura, K., M. Nei & S. Kumar, 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences 101: 11030–11035.

    Article  CAS  Google Scholar 

  • Tamura, K., D. Peterson, N. Perterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Thompson, J. D., D. G. Higgins & T. J. Gibson, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4673–4680.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tyler, P. A. & C. M. Young, 1998. Temperature and pressure tolerances in dispersal stages of the genus Echinus (Echinodermata: Echinoidea): prerequisites for deep-sea invasion and speciation. Deep-Sea Research Part II 45: 253–277.

    Article  Google Scholar 

  • Tyler, P. A. & C. M. Young, 1999. Reproduction and dispersal at vents and cold seeps. Journal of the Marine Biological Association of the United Kingdom 79: 193–208.

    Article  Google Scholar 

  • Valentini, A., F. Pompanon & P. Taberlet, 2009. DNA barcoding for ecologists. Trends in Ecology and Evolution 24: 110–117.

    Article  PubMed  Google Scholar 

  • van der Land, J. & A. NØrrevang, 1975. The systematic position of Lamellibrachia [sic] (Annelida, Vestimentifera). Journal of Zoological Systematics and Evolutionary Research Forsch (Sonderheft) 1: 86–101.

    Google Scholar 

  • van Oosterhout, C. H., W. F. Hutchinson, D. P. Willis & P. Shipley, 2004. Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  CAS  Google Scholar 

  • Watts, D. J., 2004. The “new” science of networks. Annual Review of Sociology 30: 243–270.

    Article  Google Scholar 

  • Webb, M., 1969. Lamellibrachia barhami, gen. nov., sp. nov. (Pogonophora), from the northeast Pacific. Bulletin of Marine Science 19: 18–47.

    Google Scholar 

  • Wright, S., 1951. The genetic structure of populations. Annual Eugeneics 15: 323–354.

    Article  CAS  Google Scholar 

  • Young, C. M. & P. A. Tyler, 1993. Embryos of the deep-sea echinoid Echinus affinis require high pressure for development. Limnology and Oceanography 38: 178–181.

    Article  Google Scholar 

  • Young, C. M., E. Vazquez, A. Metaxas & P. A. Tyler, 1996. Embryology of vestimentiferan tube worms from deep-sea methane/sulphide seeps. Nature 381: 514–516.

    Article  CAS  Google Scholar 

  • Young, C., P. A. Tyler & L. Fenaux, 1997. Potential for deep sea invasion by Mediterranean shallow water echinoids: pressure and temperature as stage-specific dispersal barriers. Marine Ecology Progress Series 154: 197–209.

    Article  Google Scholar 

  • Young, C., R. He, R. B. Emlet, Y. Li, H. Qian, S. M. Arellano, A. V. Gaest, K. C. Bennett, M. Wolf, T. I. Smart & M. E. Rice, 2012. Dispersal of deep-sea larvae from the Intra-American seas: simulations of trajectories using ocean models. Integrative and Comparative Biology 52: 483–496.

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank the following people for their contribution to this project: captains, crews, and expedition leaders of the DSV Johnson Sea Link II, R/V Seward Johnson ROV Jason II, the US deep submergence facility, DSV Alvin, R/V Atlantis, the NOAA vessel Ronald Brown; Drew Wham, Sophie Arnaud-Haond, Kevin Kocot, Kimberlyn Nelson, Iliana Baums, Todd LaJeunesse, Chuyna Huang, Pen-Yuan Hsing, Miles Saunders, Andrew Mendelson, and Olivier Soubigou. This research was funded in part by the National Science Foundation (Award # 1209688 and IOS-0843473 to DAC and KMH), the National Oceanographic Partnership Program (NOPP) through support from the Bureau of Ocean Energy Management contracts #M05PC00018 and #M08PC20038 to CRF (TDI Brooks International Prime), the National Oceanic and Atmospheric Administration’s Office of Ocean Exploration and Research (NOAA OER), the Penn State Eberly College of Science, and an Alfred P. Sloan Scholarship to DAC. Any opinions, findings, conclusions, or recommendations expressed in this article are those of the authors and do not necessarily reflect the views of the National Science Foundation.

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  1. Dominique A. Cowart

    Present address: Unité Environnement Profond - DEEP du, Département des Ressources physiques et Ecosystèmes de Fond de mer (REM), IFREMER - Institut Français de Recherche pour l’Exploitation de la MER, B.P. 70, 29280, Plouzané, France

Authors and Affiliations

  1. Department of Biology, The Pennsylvania State University, 208 Erwin W. Mueller Laboratory, University Park, PA, 16801, USA

    Dominique A. Cowart, Stephen W. Schaeffer & Charles R. Fisher

  2. Department of Biological Sciences, Auburn University, 101 Rouse Life Sciences Building, Auburn, AL, 36849, USA

    Kenneth M. Halanych

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Cowart, D.A., Halanych, K.M., Schaeffer, S.W. et al. Depth-dependent gene flow in Gulf of Mexico cold seep Lamellibrachia tubeworms (Annelida, Siboglinidae). Hydrobiologia 736, 139–154 (2014). https://doi.org/10.1007/s10750-014-1900-y

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  • DOI: https://doi.org/10.1007/s10750-014-1900-y

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