Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-21T04:39:03.134Z Has data issue: false hasContentIssue false
  • English
  • Français

Population connectivity of hydrothermal-vent limpets along the northern Mid-Atlantic Ridge (Gastropoda: Neritimorpha: Phenacolepadidae)

Published online by Cambridge University Press:  07 December 2017

Takuya Yahagi ,
Hiroaki Fukumori ,
Anders Warén  and
Yasunori Kano
Takuya Yahagi
Affiliation:
Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan Graduate School of Frontier Sciences, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8561, Japan
Hiroaki Fukumori
Affiliation:
Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
Anders Warén
Affiliation:
Swedish Museum of Natural History, Box 50007, SE-10405 Stockholm, Sweden
Yasunori Kano*
Affiliation:
Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
*
Correspondence should be addressed to: Y. Kano, Department of Marine Ecosystems Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan email: kano@aori.u-tokyo.ac.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

The red-blooded limpet ‘Shinkailepas’ briandi (Neritimorpha: Phenacolepadidae) is one of the commonest gastropod species at deep-sea hydrothermal vents on the Mid-Atlantic Ridge (MAR). We investigated its population connectivity along MAR as the first such study for gastropods and explored the importance of larval migration for the distribution of vent-endemic animals. Our analyses, based on 1.3-kbp DNA sequences from the mitochondrial COI gene, showed a panmictic population throughout its geographic and bathymetric ranges that span from the northernmost and shallowest Menez Gwen vent field (38°N; 814–831 m depth) to the southernmost and deepest Ashadze field (13°N; 4090 m). Early development of this species is presumed to have a long pelagic duration as a planktotrophic larva; the hatchling with a shell diameter of 170–180 μm attains a constant settlement size of 706 ± 8 μm (mean ± SD). Retention of eye pigmentation in newly settled juveniles, along with the genetic panmixia, suggests that the hatched larva of ‘S.’ briandi migrates vertically to the surface water, presumably to take advantage of richer food supplies and stronger currents for dispersal, as has been shown for confamilial species at hydrothermal vents and cold methane seeps.

Keywords

biogeographychemosynthetic environmentdeep sealarval ecologylimpetpanmixiapopulation geneticsprotoconchShinkailepas briandivertical migration
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 1 , February 2019 , pp. 179 - 185
Copyright
Copyright © Marine Biological Association of the United Kingdom 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adams, D.K., Arellano, S.M. and Govenar, B. (2012) Larval dispersal: vent life in the water column. Oceanography 25, 256–268.Google Scholar
Arellano, S.M., Van Gaest, A.L., Johnson, S.B., Vrijenhoek, R.C. and Young, C.M. (2014) Larvae from deep-sea methane seeps disperse in surface waters. Proceedings of the Royal Society B 281, 20133276.Google Scholar
Beaulieu, S.E., Baker, E.T., German, C.R. and Maffei, A. (2013) An authoritative global database for active submarine hydrothermal vent fields. Geochemistry, Geophysics, Geosystems 14, 4892–4905.Google Scholar
Beck, L.A. (1992) Two new neritacean limpets (Gastropoda: Prosobranchia: Neritacea: Phenacolepadidae) from active hydrothermal vents at hydrothermal field 1 “Wienerwald” in the Manus Back-Arc Basin (Bismarck Sea, Papua-New Guinea). Annalen des Naturhistorischen Museums in Wien, Serie B 93, 259–275.Google Scholar
Beedessee, G., Watanabe, H., Ogura, T., Nemoto, S., Yahagi, T., Nakagawa, S., Nakamura, K., Takai, K., Koonjul, M. and Marie, D.E.P. (2013) High connectivity of animal populations in deep-sea hydrothermal vent fields in the Central Indian Ridge relevant to its geological setting. PLoS ONE 8, e81570.Google Scholar
Bouchet, P. and Warén, A. (1994) Ontogenetic migration and dispersal of deep-sea gastropod larvae. In Young, C.M. and Eckelbarger, K.J. (eds) Reproduction, larval biology, and recruitment of the deep-sea benthos. New York, NY: Columbia University Press, pp. 98–117.Google Scholar
Breusing, C., Biastoch, A., Drews, A., Metaxas, A., Jollivet, D., Vrijenhoek, R.C., Bayer, T., Melzner, F., Sayavedra, L., Petersen, J.M., Dubilier, N., Schihabel, M.B., Rosentiel, P. and Reusch, T.B.H. (2016) Biophysical and population genetic models predict the presence of “phantom” stepping stones connecting Mid-Atlantic Ridge vent ecosystems. Current Biology 26, 2257–2267.Google Scholar
Clement, M., Posada, D. and Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1659.Google Scholar
Cuvelier, D., Sarradin, P.M., Sarrazin, J., Colaço, A., Copley, J.T., Desbruyères, D., Glover, A.G., Serrão Santos, R. and Tyler, P.A. (2011) Hydrothermal faunal assemblages and habitat characterisation at the Eiffel Tower edifice (Lucky Strike, Mid-Atlantic Ridge). Marine Ecology 32, 243–255.Google Scholar
Daguin, C. and Jollivet, D. (2005) Development and cross-amplification of nine polymorphic microsatellite markers in the deep-sea hydrothermal vent polychaete Branchipolynoe seepensis. Molecular Ecology Notes 5, 780–783.Google Scholar
Desbruyères, D., Almeida, A., Comtet, T., Khripounoff, A., Le Bris, N., Sarradin, P.M. and Segonzac, M. (2000) A review of the distribution of hydrothermal vent communities along the northern Mid-Atlantic Ridge: dispersal vs. environmental controls. Hydrobiologia 440, 201–216.Google Scholar
Desbruyères, D., Segonzac, M. and Bright, M. (2006) Handbook of deep-sea hydrothermal vent fauna, 2nd edition. Linz: Biologiezentrum der Oberösterreichische Landesmuseen.Google Scholar
Excoffier, L. and Lischer, H.E.L. (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.Google Scholar
Fabri, M.C., Bargain, A., Briand, P., Gebruk, A., Fouquet, Y., Morineaux, M. and Desbruyeres, D. (2011) The hydrothermal vent community of a new deep-sea field, Ashadze-1, 12 58′N on the Mid-Atlantic Ridge. Journal of the Marine Biological Association of the United Kingdom 91, 1–13.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R.A. and Vrijenhoek, R.C. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Fretter, V. (1984) The functional anatomy of the neritacean limpet Phenacolepas omanensis Biggs and some comparison with Septaira. Journal of Molluscan Studies 50, 8–18.Google Scholar
Fu, Y.X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background section. Genetics 147, 915–925.Google Scholar
Fukumori, H. and Kano, Y. (2014) Evolutionary ecology of settlement size in planktotrophic neritimorph gastropods. Marine Biology 161, 213–227.Google Scholar
Herring, P.J. (2006) Presence of postlarval alvinocaridid shrimps over south-west Indian Ocean hydrothermal vents, with comparisons of the pelagic biomass at different vent sites. Journal of the Marine Biological Association of the United Kingdom 86, 125–128.Google Scholar
Holm, N.G. and Hennet, R.J.C. (1992) Hydrothermal systems: their varieties, dynamics, and suitability for prebiotic chemistry. In Holm, N.G., ed. Marine hydrothermal systems and the origin of life. Dordrecht: Kluwer Academic Publishers, pp. 15–31.Google Scholar
Hudson, R.R., Slatkin, M. and Maddison, W.P. (1992) Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589.Google Scholar
Jollivet, D., Empis, A., Baker, M.C., Hourdez, S., Comtet, T., Jouin-Toulmond, C., Desbruyères, D. and Tyler, P.A. (2000) Reproductive biology, sexual dimorphism, and population structure of the deep sea hydrothermal vent scale-worm, Branchipolynoe seepensis (Polychaeta: Polynoidae). Journal of the Marine Biological Association of the United Kingdom 80, 55–68.Google Scholar
Kano, Y. (2006) Usefulness of the opercular nucleus for inferring early development in neritimorph gastropods. Journal of Morphology 267, 1120–1136.Google Scholar
Kano, Y., Chiba, S. and Kase, T. (2002) Major adaptive radiation in neritopsine gastropods estimated from 28S rRNA sequences and fossil records. Proceedings of the Royal Society B 269, 2457–2465.Google Scholar
Kano, Y. and Kase, T. (2004) Genetic exchange between anchialine cave populations by means of larval dispersal: the case of a new gastropod species Neritiia cavernicola. Zoologica Scripta 33, 423–437.Google Scholar
Kelley, D.S. and Shank, T.M. (2010) Hydrothermal systems: a decade of discovery in slow spreading environments. In Rona, P.A., Devey, C.W., Dyment, J. and Murton, B.J., eds. Diversity of hydrothermal systems on slow spreading ocean ridges. Washington, DC: American Geophysical Union, pp. 369–407.Google Scholar
Lesoway, M.P. and Page, L.R. (2008) Growth and differentiation during delayed metamorphosis of feeding gastropod larvae: signatures of ancestry and innovation. Marine Biology 153, 723–734.Google Scholar
Moalic, Y., Desbruyères, D., Duarte, C.M., Rozenfeld, A.F., Bachraty, C. and Arnaud-Haond, S. (2012) Biogeography revisited with network theory: retracing the history of hydrothermal vent communities. Systematic Biology 61, 127–137.Google Scholar
Mullineaux, L.S. (2014) Deep-sea hydrothermal vent communities. In Bertness, M.D., Bruno, J.F., Silliman, B.R. and Stachowicz, J.J., eds. Marine community ecology and conservation. Sunderland, MA: Sinauer Associates Inc., pp. 383–400.Google Scholar
Nei, M. (1987) Molecular evolutionary genetics. New York, NY: Columbia University Press.Google Scholar
O'Mullan, G.D., Maas, P.A.Y., Lutz, R.A. and Vrijenhoek, R.C. (2001) A hybrid zone between hydrothermal vent mussels (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Molecular Ecology 10, 2819–2831.Google Scholar
Ramirez Llodra, E., Tyler, P.A. and Copley, J.T.P. (2000) Reproductive biology of three caridean shrimp, Rimicaris exoculata, Chorocaris chacei and Mirocaris fortunata (Caridea: Decapoda), from hydrothermal vents. Journal of the Marine Biological Association of the United Kingdom 80, 473–484.Google Scholar
Raymond, M. and Rousset, F. (1995) An exact test for population differentiation. Evolution 49, 1280–1283.Google Scholar
Rogers, A.R. and Harpending, H. (1992) Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552–569.Google Scholar
Scheltema, R.S. (1971) Larval dispersal as a means of genetic exchange between geographically separated populations of shallow-water benthic marine gastropods. Biological Bulletin 140, 284–322.Google Scholar
Stevens, C.J., Limén, H., Pond, D.W., Gélinas, Y. and Juniper, S.K. (2008) Ontogenetic shifts in the trophic ecology of two alvinocaridid shrimp species at hydrothermal vents on the Mariana Arc, western Pacific Ocean. Marine Ecology Progress Series 356, 225–237.Google Scholar
Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460.Google Scholar
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Teixeira, S., Cambon-Bonavita, M.A., Serrão, E.A., Desbruyéres, D. and Arnaud-Haond, S. (2011) Recent population expansion and connectivity in the hydrothermal shrimp Rimicaris exoculata along the Mid-Atlantic Ridge. Journal of Biogeography 38, 564–574.Google Scholar
Teixeira, S., Olu, K., Decker, C., Cunha, R.L., Fuchs, S., Hourdez, S., Serrão, E.A. and Arnaud-Haond, S. (2013) High connectivity across the fragmented chemosynthetic ecosystems of the deep Atlantic Equatorial Belt: efficient dispersal mechanisms or questionable endemism? Molecular Ecology 22, 4663–4680.Google Scholar
Teixeira, S., Serrão, E.A. and Arnaud-Haond, S. (2012) Panmixia in a fragmented and unstable environment: the hydrothermal shrimp Rimicaris exoculata disperses extensively along the Mid-Atlantic Ridge. PLoS ONE 7, e38521.Google Scholar
Van Dover, C.L. (1995) Ecology of mid-Atlantic ridge hydrothermal vents. Geological Society, London, Special Publications 87, 257–294.Google Scholar
Van Dover, C.L. (2000) The ecology of deep-sea hydrothermal vents. Princeton, NJ: Princeton University Press.Google Scholar
Warén, A. and Bouchet, P. (2001) Gastropoda and monoplacophora from hydrothermal vents and seeps; new taxa and records. The Veliger 44, 116–231.Google Scholar
Wheeler, A.J., Murton, B., Copley, J., Lim, A., Carlsson, J., Collins, P., Dorschel, B., Green, D., Judge, M., Nye, V., Benzie, J., Antoniacomi, A., Coughlan, M. and Morris, K. (2013) Moytirra: discovery of the first known deep-sea hydrothermal vent field on the slow-spreading Mid-Atlantic Ridge north of the Azores. Geochemistry, Geophysics, Geosystems 14, 4170–4184.Google Scholar
Wilke, T. (2003) Salenthydrobia gen. nov. (Rissooidea: Hydrobiidae): a potential relict of the Messinian salinity crisis. Zoological Journal of the Linnean Society 137, 319–336.Google Scholar
Yahagi, T., Kayama Watanabe, H., Kojima, S. and Kano, Y. (2017) Do larvae from deep-sea hydrothermal vents disperse in surface waters? Ecology 98, 1524–1534.Google Scholar
Young, C.M. (2003) Reproduction, development and life-history traits. In Tyler, P.A., ed. Ecosystems of the deep oceans. Amsterdam: Elsevier, pp. 381–426.Google Scholar