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Phylogeography and genetic diversity of Ophidiaster ophidianus (Echinodermata: Asteroidea)—evidence for a recent range expansion in the Azores

Published online by Cambridge University Press:  16 May 2014

J. Micael ,
P. Rodrigues ,
A.C. Costa  and
M.J. Alves
J. Micael*
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Polo dos Açores, Universidade dos Açores, 9501-801 Ponta Delgada, Portugal
P. Rodrigues
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Polo dos Açores, Universidade dos Açores, 9501-801 Ponta Delgada, Portugal
A.C. Costa
Affiliation:
CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Polo dos Açores, Universidade dos Açores, 9501-801 Ponta Delgada, Portugal
M.J. Alves
Affiliation:
Centro de Biologia Ambiental and Museu Nacional de História Natural, Universidade de Lisboa, Rua da Escola Politécnica, 1250-102 Lisboa, Portugal
*
Correspondence should be addressed to: J. Micael, CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Polo dos Açores, Universidade dos Açores, 9501-801 Ponta Delgada, Sao Miguel, Azores, Portugal email: [email protected]
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Abstract

The seastar Ophidiaster ophidianus is a vulnerable and protected species in the Mediterranean Sea but is common on North Atlantic islands such as the Azores and Madeira archipelagos. This work presents new insights into the phylogeography and genetic diversity of O. ophidianus from the Azores, based on 67 sequences of the 16S mitochondrial gene and 46 sequences of the nuclear ATP intron 5 gene. Twenty-six samples from the Mediterranean and seven samples from Madeira were used as out-groups. The results revealed that there is a lack of genetic differentiation between O. ophidianus from the Azores and the out-groups. All, therefore, belong to the same lineage and argue for a fast and recent range expansion of this species into the Azores. Our results also suggest the existence of distinctive periods of strong gene flow followed by periods of either low or non-existent gene flow between the Mediterranean Sea and this archipelago, which could explain the presence of private haplotypes in all studied areas.

Keywords

purple seastarechinodermsexpansionphylogeographygenetic structureAzores
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 94 , Issue 7 , November 2014 , pp. 1475 - 1484
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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References

REFERENCES

Almada, V.C., Oliveira, R.F., Gonçalves, E.J., Almeida, A.J., Santos, R.S. and Wirtz, P. (2001) Patterns of diversity of the northeastern Atlantic blennid fish fauna (Pisces: Blenniidae). Global Ecology and Biogeography 10, 411–422.CrossRefGoogle Scholar
Aris-Brosou, S. and Excoffier, L. (1996) The impact of population expansion and mutation rate heterogeneity on DNA sequence polymorphism. Molecular Biology and Evolution 13, 494–504.CrossRefGoogle ScholarPubMed
Barker, M.F. and Nichols, D. (1983) Reproduction, recruitment and juvenile ecology of the starfish, Asterias rubens and Marthasterias glacialis. Journal of the Marine Biological Association of United Kingdom 63, 745–765.CrossRefGoogle Scholar
Baringer, M.O. and Price, J.F. (1997) Mixing and spreading of the Mediterranean outflow. Journal of Physical Oceanography 27, 1654–1677.2.0.CO;2>CrossRefGoogle Scholar
Baus, E., Darrock, D.J. and Bruford, M.W. (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Molecular Ecology 14, 3373–3382.CrossRefGoogle ScholarPubMed
Bellwood, D.R., Hughes, T.P., Folke, C. and Nystrom, M. (2004) Confronting the coral reef crisis. Nature 429, 827–833.CrossRefGoogle ScholarPubMed
Borrero-Pérez, G.H., González-Wangüemert, M., Marcos, C. and Pérez-Ruzafa, A. (2011) Phylogeography of the Atlanto-Mediterranean sea cucumber Holothuria (Holothuria) mammata: the combined effects of historical processes and current oceanographical pattern. Molecular Ecology 20, 1964–1975.CrossRefGoogle ScholarPubMed
Borsa, P., Blanquer, A. and Berrebi, P. (1997) Zoogéographie intraspécifique de la mer Méditerranée. Analyse des données génétiques populationnelles sur seize espèces atlanto-méditerranéennes (Poissons et Invertébrés). Vie et Milieu 47, 95–305.Google Scholar
Botsford, L.W., Micheli, F. and Hastings, A. (2003) Principles for the design of marine reserves. Journal of Applied Ecology 13, 25–31.CrossRefGoogle Scholar
Bouzat, J.L. (2010) Conservation genetics of population bottlenecks: the role of chance, selection, and history. Conservation Genetics 11, 463–478.CrossRefGoogle Scholar
Brown, W.M., George, M. Jr and Wilson, A.C. (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America 74, 1967–1971.CrossRefGoogle Scholar
Calderón, I., Giribet, G. and Turon, X. (2008) Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Marine Biology 154, 137–151.CrossRefGoogle Scholar
Cebrián, E. and Ballesteros, E. (2004) Zonation patterns of benthic communities in an upwelling area from the Western Mediterranean (La Herradura, Alboran Sea). Scientia Marina 68, 69–84.CrossRefGoogle Scholar
Chenuil, A. and Féral, J.P. (2003) Sequences of mitochondrial DNA suggest that Echinocardium cordatum is a complex of several sympatric or hybridizing species: a pilot study. In Féral, J.P. and David, B. (eds) Echinoderm Research 2001, Proceedings of the Sixth European Conference on Echinoderm, Banyuls-sur-Mer, France. Lisse: Swets & Zeitlinger, pp. 15–32.Google Scholar
Clark, A.M. and Downey, M.E. (1992) Starfishes of the Atlantic. London: Chapman & Hall, 794 pp.Google Scholar
Clement, M., Posada, D. and Crandall, K. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 1657–1660.CrossRefGoogle ScholarPubMed
Colgan, D.J., Byrne, M., Rickard, E. and Castro, L.R. (2005) Limited nucleotide divergence over large spatial scales in the asterinid sea star Patiriella exigua. Marine Biology 146, 263–270.CrossRefGoogle Scholar
Costantini, F., Fauvelot, C. and Abbiati, M. (2007) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Molecular Ecology 16, 5168–5182.CrossRefGoogle ScholarPubMed
Diaz-Almela, E., Boudry, P., Launey, S., Bonhomme, F. and Lapegue, S. (2004) Reduced female gene Xow in the European Xat oyster Ostrea edulis. Journal of Heredity 95, 510–516.CrossRefGoogle Scholar
Domingues, V.S., Santos, R.S., Brito, A. and Almada, V.C. (2006) Historical population dynamics and demography of the eastern Atlantic pomacentrid Chromis limbata (Valenciennes, 1833). Molecular Phylogenetics and Evolution 40, 139–147.CrossRefGoogle ScholarPubMed
Domingues, V.S., Santos, R.S., Brito, A., Alexandrou, M. and Almada, V.C. (2007) Mitochondrial and nuclear markers reveal isolation by distance and effects of Pleistocene glaciations in the northeastern Atlantic and Mediterranean populations of the white seabream (Diplodus sargus, L.). Journal of Experimental Marine Biology and Ecology 346, 102–113.CrossRefGoogle Scholar
Domínguez-Alonso, P., Remón, J.M., Villena, M. and Ramos, M.A. (1999) Echinoderms from Fauna oceanographic expedition Fauna (Fauna Ibérica Project and from Museo Nacional de Ciencias Naturales (MNCN) historical Collections. In Carnevali, M.D.C. and Bonosoro, F. (eds) Echinoderm research 1998. Rotterdam: A.A. Balkema, pp. 449–451.Google Scholar
Drummond, A.J., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. and Wilson, A. (2009) Geneious v.4.7. Available at: http://www.geneious.com (accessed 8 April 2014).Google Scholar
Drummond, A.J., Suchard, M.A., Xie, D. and Rambaut, A. (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29, 1969–1973.CrossRefGoogle ScholarPubMed
Duran, S., Palacin, C., Becerro, M.A., Turon, X. and Giribet, G. (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Molecular Ecology 13, 3317–3328.CrossRefGoogle ScholarPubMed
Excoffier, L.P., Smouse, E. and Quattro, J.M. (1992) Analysis of molecular variance inferred from metric distances among haplotypes: application to human mitochondrial DNA restriction data. Genetics 131, 479–491.CrossRefGoogle ScholarPubMed
Fratini, S., Ragionieri, L., Cutuli, G., Vannini, M. and Cannicci, S. (2013) Pattern of genetic isolation in the crab Pachygrapsus marmoratus within the Tuscan Archipelago Mediterranean Sea. Marine Ecology Progress Series 478, 173–183.CrossRefGoogle Scholar
Foltz, D.W., Nguyen, A.T., Nguyen, I. and Kiger, J.R. (2007) Primers for the amplification of nuclear introns in sea stars of the family Asteriidae. Molecular Ecology Notes 7, 874–876.CrossRefGoogle Scholar
Fu, Y.-X. (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.CrossRefGoogle ScholarPubMed
Gerard, K., Roby, C., Chevalier, N., Thomassin, B., Chenuil, A., and Feral, J.P. (2008) Assessment of three mitochondrial loci variability for the crown-of-thorns starfish: a first insight into Acanthaster phylogeography. Comptes Rendus Biologie 331, 137–143.CrossRefGoogle ScholarPubMed
Grippa, G. (1990) Note sui Crostacei Decapodi dell'isola del Giglio (Arcipelago Toscano). Atti della Società italiana di scienze naturali 131, 337–363.Google Scholar
Hansen, M.M., Mensberg, K.L.D. and Berg, S. (1999) Postglacial recolonization patterns and genetic relationships among whitefish (Coregonus sp.) populations in Denmark, inferred from mitochondrial DNA and microsatellite markers. Molecular Ecology 8, 239–252.CrossRefGoogle Scholar
Hansson, H.G. (1999) Echinodermata. In Costello, M.J., Emblow, C.S. and White, R. (eds) European Register of Marine Species. A check-list of the marine species in Europe and a bibliography of guides to their identification. Patrimoines naturels, Volume 50, 463 pp.Google Scholar
Harley, C.D.G., Pankey, M.S., Wares, J.P., Grosberg, R.K. and Wonham, M.J. (2006) Color polymorphism and genetic structure in the sea star Pisaster ochraceus. Biological Bulletin. Marine Biological Laboratory, Woods Hole 211, 248–262.CrossRefGoogle ScholarPubMed
Harper, F.M., Addison, J.A. and Hart, M.W. (2007) Introgression versus immigration in hybridizing high-dispersal echinoderms. Evolution 61, 2410–2418.CrossRefGoogle ScholarPubMed
Hudson, R.R. (1990) Gene genealogies and the coalescent process. In Futuyma, D. and Antonovics, J. (eds) Oxford surveys in evolutionary biology, volume 7. New York: Oxford University Press, pp. 1–44.Google Scholar
Hunt, A. (1993) Effects of contrasting patterns of larval dispersal on the Genetic connectedness of local-populations of 2 intertidal starfish, Patiriella calcar and P. exigua. Marine Ecology Progress Series 92, 179–186.CrossRefGoogle Scholar
Jarman, S.N., Ward, R.D. and Elliott, N.G. (2002) Oligonucleotide primers for PCR amplification of coelomate introns. Marine Biotechnology 4, 347–355.CrossRefGoogle ScholarPubMed
Johnson, J. and Stevens, I. (2000) A fine resolution model of the eastern North Atlantic between the Azores, the Canary Islands and the Gibraltar Strait. Deep-Sea Research 47, 875–899.CrossRefGoogle Scholar
Keever, C.C., Sunday, J., Puritz, J.B., Addison, J.A., Toonen, R.J., Grosberg, R.K. and Hart, M.W. (2009) Discordant distribution of populations and genetic variation in a sea star with high dispersal potential. Evolution 63, 3214–3227.CrossRefGoogle Scholar
Koehler, R. (1924) Les Échinodermes des Mers D' Europe. Tomo I. Paris: Librarie Octave Doin, 362 pp.Google Scholar
Launey, S., Ledu, C., Boudry, P., Bonhomme, F. and Naciri-Graven, Y. (2002) Geographic structure in the European Xat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. Journal of Heredity 93, 331–338.CrossRefGoogle Scholar
Lemaire, C., Versini, J.J. and Bonhomme, F. (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. Journal of Evolutionary Biology 18, 70–80.CrossRefGoogle ScholarPubMed
Librado, P. and Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 1451–1452.CrossRefGoogle ScholarPubMed
Maltagliati, F., Di Giuseppe, G., Barbieri, M., Castelli, A. and Dini, F. (2010) Phylogeography and genetic structure of the edible sea urchin Paracentrotus lividus (Echinodermata: Echinoidea) inferred from the mitochondrial cytochrome b gene. Biological Journal of the Linnean Society 100, 910–923.CrossRefGoogle Scholar
Marques, V.M. (1983) Peuplements benthiques des Açores; 1—Echinodermes. Arquivo do Museu Bocage AII(I), 1–7.Google Scholar
Matsuoka, N. and Asano, H. (2003) Genetic variation in northern Japanese populations of the starfish Asterina pectinifera. Zoological Science 20, 985–988.CrossRefGoogle ScholarPubMed
McEdward, L.R. and Janies, D.A. (1993) Life cycle evolution in asteroids, what is a larva? Biological Bulletin. Marine Biological Laboratory, Woods Hole 184, 255–268.CrossRefGoogle ScholarPubMed
Micael, J., Alves, M.J., Costa, A.C. and Jones, M.B. (2009) Exploitation and Conservation of Echinoderms. Oceanography and Marine Biology; an Annual Review 47, 191–208.Google Scholar
Micael, J., Rodrigues, A.S., Barreto, M.C., Alves, M.J., Jones, M.B. and Costa, A.C. (2011) Allocation of nutrients during the reproductive cycle of Ophidiaster ophidianus (Echinodermata: Asteroidea). Journal of Invertebrate Reproduction and Development 55, 205–216.CrossRefGoogle Scholar
Micael, J., Alves, M.J. and Costa, A.C. (2013) The population dynamics of Ophidiaster ophidianus (Echinodermata: Asteroidea) in the Azores, at the north-western periphery of its distribution. Journal of the Marine Biological Association of the United Kingdom 93, 1087–1095.CrossRefGoogle Scholar
Michalakis, Y. and Excoffier, L. (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142, 1061–1064.CrossRefGoogle ScholarPubMed
Mougenot, D. and Vanney, J.-R. (1982) The Plio-Quarternary sediment drifts of the south Portuguese continental slope. Bulletin de l'Institut de Géologie du Bassin d'Aquitaine 31, 131–139.Google Scholar
Nei, M. (1987) Molecular evolutionary genetics. New York: Colombia University Press.CrossRefGoogle Scholar
Nobre, A. (1938) Echinodermes de Portugal. 2.a edição. Porto: Instituto de Zoologia Dr. Augusto Nobre, 176 pp.Google Scholar
Palumbi, S.R. (2003) Population genetics, demographic connectivity, and the design of marine reserves. Journal of Applied Ecology 13, 146–158.CrossRefGoogle Scholar
Pawson, D.L. (2007) Phylum Echinodermata. In Zhang, Z.-Q. and Shear, W.A. (eds.) Linnaeus tercentenary: progress in invertebrate taxonomy. Zootaxa 1668, 1–766.CrossRefGoogle Scholar
Peck, D.R. and Congdon, B.C. (2004) Reconciling historical processes and population structure in the sooty tern Sterna fuscata. Journal of Avian Biology 35, 327–335.CrossRefGoogle Scholar
Pereira, R.M.O. (1997) Checklist of the littoral echinoderms of the Azores. Açoreana 8, 331–337.Google Scholar
Pérez-Portela, R., Villamor, A. and Almada, V. (2010) Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western Mediterranean. Marine Biology 157, 2015–2028.CrossRefGoogle Scholar
Pérez-Ruzafa, A., Entrambasaguas, L. and Bacallado, J.J. (1999) Fauna de equinodermos (Echinodermata) de los fondos rocosos infralitorales del archipiélago de Cabo Verde. Revista de la Academia Canaria de Ciencias 11, 43–62.Google Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Ramos-Onsins, S.E. and Rozas, J. (2002) Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution 19, 2092–2100.CrossRefGoogle ScholarPubMed
Rambaut, A. (2008) Figtree v.1.1.1: Tree figure drawing tool. Available at: http://tree.bio.ed.ac.uk/software/figtree (accessed 8 April 2014).Google Scholar
Rogers, A.R. (1995) Genetic evidence for a pleistocene population explosion. Evolution 49, 608–615.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Romano, S.L. and Palumbi, S.R. (1997) Molecular evolution of a portion of the mitochondrial 16S ribosomal gene region in scleractinian corals. Journal of Molecular Evolution 45, 397–411.CrossRefGoogle ScholarPubMed
Rossi, F., Forster, R.M., Montserrat, F., Ponti, M., Terlizzi, A., Ysebaert, T. and Middelburg, J.J. (2007) Human trampling as short-term disturbance on intertidal mudflats: effects on macrofauna biodiversity and population dynamics of bivalves. Marine Biology 151, 2077–2090.CrossRefGoogle ScholarPubMed
Saavedra, C. and Pena, J.B. (2005) Nucleotide diversity and Pleistocene population expansion in Atlantic and Mediterranean scallops (Pecten maximus and P. jacobaeus) as revealed by the mitochondrial 16S ribosomal RNA gene. Journal of Experimental Marine Biology and Ecology 323, 138–150.CrossRefGoogle Scholar
Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular cloning. A laboratory manual. 2nd edition.Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.Google Scholar
Smith, M.J., Arndt, A., Gorski, S. and Fajber, E. (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. Journal of Molecular Evolution 36, 545–554.CrossRefGoogle ScholarPubMed
Schiebel, R., Schmuker, B., Alves, M. and Hemleben, C. (2002) Tracking the recent and late Pleistocene Azores front by the distribution of planktic foraminifers. Journal of Marine Systems 37, 213–227.CrossRefGoogle Scholar
Schneider, S., Roessli, D. and Excoffier, L. (2000) ARLEQUIN, Version 2.000: A Software for Population Genetics Data Analysis. Geneva: University of Geneva.Google Scholar
Send, U., Font, J., Krahmann, G., Millot, C., Rhein, M. and Tintoré, J. (1999) Recent advances in observing the physical oceanography of the western Mediterranean Sea. Progress in Oceanography 44, 37–64.CrossRefGoogle Scholar
Stamatis, C., Triantafyllidis, A., Moutou, K.A. and Mamuris, Z. (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Molecular Ecology 13, 1377–1390.CrossRefGoogle ScholarPubMed
Stamatis, C., Triantafyllidis, A., Moutou, K.A. and Mamuris, Z. (2006) Allozymic variation in Northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Molecular Ecology 63, 875–882.Google Scholar
Strathmann, R.R. (1993) Hypotheses on the origins of marine larvae. Annual Review of Ecology and Systematics 24, 89–117.CrossRefGoogle Scholar
Tajima, F. (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105, 437–460.CrossRefGoogle ScholarPubMed
Tajima, F. (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.CrossRefGoogle ScholarPubMed
Tanti, C.M. and Schembri, P.J. (2006) A synthesis of the echinoderm fauna of the Maltese islands. Journal of the Marine Biological Association of the United Kingdom 86, 163–165.CrossRefGoogle Scholar
Tortonese, E. (1965) Echinodermata. Fauna d'Italia VI. Bologna: Calderini, 422 pp.Google Scholar
von, Haeseler A., Sajantila, A. and Paabo, S. (1996) The genetical archaeology of the human genome. Nature Genetics 14, 135–140.Google Scholar
Wangensteen, O.S., Turon, X., Pérez-Portela, R. and Palacín, C. (2012) Natural or naturalized? Phylogeography suggests that the abundant sea urchin Arbacia lixula is a recent colonizer of the Mediterranean. PLoS ONE 7, e45067. doi:10.1371/journal.pone.0045067.CrossRefGoogle Scholar
Waters, J.M., O'Loughlin, P.M. and Roy, M.S. (2004) Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Molecular Phylogenetics and Evolution 32, 236–245.CrossRefGoogle Scholar
Williams, S.T. and Benzie, J.A.H. (1998) Evidence of a biogeographic break between populations of a high dispersal starfish: congruent regions within the Indo-West Pacific defined by color morphs, mtDNA, and allozyme data. Evolution 52, 87–99.Google ScholarPubMed
Zulliger, D., Tanner, S., Ruch, M. and Ribi, G. (2009) Genetic structure of the high dispersal Atlanto-Mediterreanean sea star Astropecten aranciacus revealed by mitochondrial DNA sequences and microsatellite loci. Marine Biology 156, 597–610.CrossRefGoogle Scholar
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