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Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western mediterranean

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Abstract

We explore the phylogeography of the broadcast spawner Marthasterias glacialis along south Europe and Azores. Sequences of the cytochrome c oxidase gene from 225 specimens, belonging to 10 localities, were analysed. We found 73 haplotypes grouped within two lineages (divergence 2.9%). One lineage was Atlanto–Mediterranean, whereas another one was exclusively Mediterranean. Estimation of lineages split goes back to 830,000–580,000 (±120,000) years ago. This suggests that sea-level oscillations during the Pleistocene glaciations promoted gene flow interruption, lineage divergence between basins and cryptic speciation. Secondary contact between populations allowed a recolonization of the Mediterranean by the Atlantic lineage. When animals of the Atlanto–Mediterranean lineage were considered separately, F st index and AMOVA did not show significant differences between populations along either the Iberian Peninsula or basins. Isolation by distance between populations was not detected, and only populations of Plymouth and Azores showed significant differences to all the others. The remoteness of Azores islands might explain the structure of this population. Haphazard arrival of larvae and local extinctions rather than contemporary restricted gene flow might be responsible for the distinctive population structure of Plymouth.

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References

  • Addison JA, Hart MW (2004) Analysis of population genetic structure of the green sea urchin (Strongylocentrotus droebachiensis) using microsatellites. Mar Biol 144:243–251

    Article  Google Scholar 

  • Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evolution 59:532–543

    PubMed  CAS  Google Scholar 

  • Avise JC (1994) Molecular markers, natural history and evolutionl. Chapman and Hall, London

    Google Scholar 

  • Avise JC (2000) Phylogeography: the history and formation of species, Vol. Harvard University Press, Cambridge

    Google Scholar 

  • Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial DNA lineage survivorship in animal populations. J Mol Evol 20:99–105

    Article  PubMed  CAS  Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    PubMed  CAS  Google Scholar 

  • Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic-Mediterranean divide. J Evol Biol 16:1149–1158

    Article  PubMed  CAS  Google Scholar 

  • Baric S, Sturmbauer C (1999) Ecological parallelism and cryptic species in the genus Ophiothrix derived from mitochondrial DNA sequences. Mol Phylogenet Evol 11:157–162

    Article  PubMed  CAS  Google Scholar 

  • Barker MF, Nichols D (1983) Reproduction, recruitment and juvenile ecology of the starfish, Asterias-rubens and Marthasterias glacialis. J Mar Biol Ass UK 63:745–765

    Article  Google Scholar 

  • Barton NH, Hewitt GM (1985) Analysis of hybrid zones. Annu Rev Ecol Syst 16:113–148

    Article  Google Scholar 

  • Benzie JAH (1999) Major genetic differences between crown-of-thorns starfish (Acanthaster planci) populations in the Indian and Pacific Oceans. Evolution 53:1782–1795

    Article  CAS  Google Scholar 

  • Borsa P, Naciri M, Bahri L, Chikhi L, Garcia de León FJ, Kotoulas G, Bonhomme F (1997) Intraspecific zoogeography of the Mediterranean: population genetic analysis on sixteen atlanto-mediterranean species (fishes and invertebrates). Vie et Milieu 47:295–305

    Google Scholar 

  • Bos AR, Gumanao GS, Alipoyo JCE, Cardona LT (2008) Population dynamics, reproduction and growth of the Indo-Pacific horned sea star, Protoreaster nodosus (Echinodermata; Asteroidea). Mar Biol 156:55–63

    Article  Google Scholar 

  • Calderon I, Giribet G, Turon X (2008) Two markers and one history: phylogeography of the edible common sea urchin Paracentrotus lividus in the Lusitanian region. Mar Biol 154:137–151

    Article  Google Scholar 

  • Cimmaruta R, Bondanelli P, Nascetti G (2005) Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Mol Ecol 14:2577–2591

    Article  PubMed  CAS  Google Scholar 

  • Clarke KR, Warwick RM (2001) Change in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E, Plymouth

    Google Scholar 

  • Couceiro L, Barreiro R, Ruiz JM, Sotka EE (2007) Genetic isolation by distance among populations of the netted dog whelk Nassarius reticulatus (L.) along the European Atlantic coastline. J Hered 98:603–610

    Article  PubMed  CAS  Google Scholar 

  • Cunningham CW, Collins TM (1998) Beyond area relationships: extinction and recolonization in molecular marine biogeography. In: Schierwater B, Streit B, Wagner G, DeSalle R (eds) Molecular ecology and evolution: approaches and applications. Birkhauser Verlag, Basel, pp 297–321

    Google Scholar 

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  PubMed  CAS  Google Scholar 

  • Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328

    Article  PubMed  CAS  Google Scholar 

  • Ellis JR, Rogers SI (2000) The distribution, relative abundance and diversity of echinoderms in the eastern English Channel, Bristol Channel, and Irish Sea. J Mar Biol Ass UK 80:127–138

    Article  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    PubMed  CAS  Google Scholar 

  • Feral JP (2002) How useful are the genetic markers in attempts to understand and manage marine biodiversity? J Exp Mar Biol Ecol 268:121–145

    Article  CAS  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Frid CLJ (1992) Foraging behavior of the spiny starfish Marthasteria glacialis in Lough Ine, Co Cork. Mar Behav Physiol 19:227–239

    Article  Google Scholar 

  • Fu YX (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Guidetti P (2004) Consumers of sea urchins, Paracentrotus lividus and Arbacia lixula, in shallow Mediterranean rocky reefs. Helgoland Mar Res 58:110–116

    Article  Google Scholar 

  • Harmelin J, Bouchon C, Duval C, Hong J (1980) Les échinodermes des substrats durs de l’ile de Port-Cros, Parc National. Elément pour un inventaire quantitatif. Trav Sci Parc Nation Port-Cros 6:25–38

    Google Scholar 

  • Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life-history evolution in Asterinid starfish. Evolution 51:1848–1861

    Article  Google Scholar 

  • Hebert PDN, Ratnasingham S, de Waard JR (2003) Barcoding animal life: cytochrome c oxidase subunint 1 divergences among closely related species. Proc R Soc Lond 270:96–99

    Article  CAS  Google Scholar 

  • Hedgecock D, Barber PH, Edmands S (2007) Genetic approaches to measuring connectivity. Oceanography 20:70–79

    Google Scholar 

  • Hellberg ME (1996) Dependence of gene flow on geographic distance in two solitary corals with different larval dispersal capabilities. Evolution 50:1167–1175

    Article  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    Article  PubMed  CAS  Google Scholar 

  • Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the Drake passage in the Southern Ocean. J Hered. doi:10.1093/jhered/esm119

  • Knowlton N (2000) Molecular genetic analyses of species boundaries in the sea. Hydrobiologia 420:73–90

    Article  CAS  Google Scholar 

  • Launey S, Ledu C, Boudry P, Bonhomme F, Naciri-Graven Y (2002) Geographic structure in the European flat oyster (Ostrea edulis L.) as revealed by microsatellite polymorphism. J Hered 93:331–338

    Article  PubMed  CAS  Google Scholar 

  • Le Gac M, Feral JP, Poulin E, Veyret M, Chenuil A (2004) Identification of allopatric clades in the cosmopolitan ophiuroid species complex Amphipholis squamata (Echinodermata). The end of a paradox? Mar Ecol Prog Ser 278:171–178

    Article  Google Scholar 

  • Lee M (2004) The molecularisation of taxonomy. Invertebr Sys 18:1–6

    Article  CAS  Google Scholar 

  • Lessios HA, Kessing BD, Robertson DR, Paulay G (1999) Phylogeography of the pantropical sea urchin Eucidaris in relation to land barriers and ocean currents. Evolution 53:806–817

    Article  Google Scholar 

  • Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975

    Article  PubMed  CAS  Google Scholar 

  • Lessios HA, Kane J, Robertson DR, Wallis G (2003) Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans. Evolution 57:2026–2036

    PubMed  CAS  Google Scholar 

  • Maggs CA, Castilho R, Foltz D, Henzler C, Jolly MT, Kelly J, Olsen J, Perez KE, Stam W, Väinölä R, Viard F, Wares J (2008) Evaluating signatures of the glacial refugia for North Atlantic benthic marine taxa. Ecology 89:108–122

    Article  Google Scholar 

  • Mccartney M, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation in Atlantic and eastern Pacific sea urchins of the genus Echinometra. Mol Ecol 9:1391–1400

    Article  PubMed  CAS  Google Scholar 

  • Mortensen T (1927) Echinoderms of the British Isles. VIII. Oxford University Press, Oxford, p 471

    Google Scholar 

  • Muths D, Jollivet D, Gentil F, Davoult D (2009) Large-scale genetic patchiness among NE Atlantic populations of the brittle star Ophiothrix fragilis. Aquat Biol 5:117–132

    Article  Google Scholar 

  • Nichols D, Barker MF (1984) Reproductive and nutritional periodicities in the starfish, Marthasterias glacialis, from Plymouth Sound. J Mar Biol Ass UK 64:461–470

    Article  Google Scholar 

  • Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572

    Article  Google Scholar 

  • Palumbi SR (1995) Using genetics as an indirect estimator of larval dispersal. In: McEdward L (ed) Ecology of marine invertebrate larvae. CRC Press, Boca Raton, pp 369–387

    Google Scholar 

  • Patarnello T, Volckaert F, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444

    Article  PubMed  Google Scholar 

  • Pérez-Losada M, Guerra A, Carvalho GR, Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: Cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424

    Article  PubMed  CAS  Google Scholar 

  • Pérez-Portela R, Turon X (2008) Cryptic divergence and strong population structure in the colonial invertebrate Pycnoclavella communis (Ascidiacea) inferred from molecular data. Zoology 111:163–178

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

  • Quesada H, Beynon CM, Skibinski DOF (1995) A mitochondrial-DNA discontinuity in the mussel Mytilus galloprovincialis (Lmk): pleistocene vicariance biogeography and secondary intergradation. Mol Biol Evol 12:521–524

    PubMed  CAS  Google Scholar 

  • Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100

    PubMed  CAS  Google Scholar 

  • Rios C, Sanz S, Saavedra C, Pena JB (2002) Allozyme variation in populations of scallops, Pecten jacobaeus (L.) and P maximus (L.) (Bivalvia : Pectinidae), across the Almeria-Oran front. J Exp Mar Biol Ecol 267:223–244

    Article  CAS  Google Scholar 

  • Rogers AR (1995) Genetic-evidence for a pleistocene population explosion. Evolution 49:608–615

    Article  Google Scholar 

  • Rogers AR, Harpending H (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    PubMed  CAS  Google Scholar 

  • Rozas J, Rozas R (1999) DNAsp version 3.0: an integrated program for molecular population genetics and molecular evolution analyses. Bioinformatics 15:174–175

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Savy S (1987) Activity pattern of the sea-star, marthasterias-glacialis, in port-cros bay (France, Mediterranean Coast). PSZNI Mar Ecol 8:97–106

    Article  Google Scholar 

  • Solé-Cava AM, Thorpe JP (1991) High levels of genetic variation in natural populations of marine lower invertebrates. Biol J Linn Soc 44:65–80

    Article  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2001) Cryptic species of Clavelina (Ascidiacea) in two different habitats: harbours and rocky littoral zones in the northwestern Mediterranean. Mar Biol 139:455–462

    Article  Google Scholar 

  • Templeton AR, Sing CF (1993) A Cladistic-analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping 4. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669

    PubMed  CAS  Google Scholar 

  • Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343–351

    PubMed  CAS  Google Scholar 

  • Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the Tiger Salamander, Ambystoma tigrinum. Genetics 140:767–782

    PubMed  CAS  Google Scholar 

  • Uthicke S, Benzie JAH (2003) Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific. Mol Ecol 12:2635–2648

    Article  PubMed  CAS  Google Scholar 

  • Uthicke S, Byrne M, Conand C (2010) Genetic Barcoding of commercial Bêche-de-mer species (Echinodermata: Holothuroidea). Mol Ecol Resour

  • Ward R, Holmes B, O’hara T (2008) DNA barcoding discriminates echinoderm species. Mol Ecol Resour 8:1202–1211

    Article  CAS  Google Scholar 

  • Wares JP (2001) Biogeography of Asterias: North Atlantic climate change and speciation. Biol Bull 201:95–103

    Article  PubMed  CAS  Google Scholar 

  • Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469

    PubMed  CAS  Google Scholar 

  • Waters JM, Roy MS (2003) Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J Biogeog 30:1787–1796

    Article  Google Scholar 

  • Waters JM, O’Loughlin PM, Roy MS (2004) Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Mol Phylogenet Evol 32:236–245

    Article  PubMed  CAS  Google Scholar 

  • Yamaguchi M, Lucas JS (1984) Natural parthenogenesis, larval and juvenile development, and geographical distribution of the coral reef asteroid Ophidiaster granifer. Mar Biol 83:33–42

    Article  Google Scholar 

  • Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Cuzin-Roudy J, Buchholz F, Patarnello T (2000) Genetic differentiation in a pelagic crustacean (Meganyctiphanes norvegica: Euphausiacea) from the North East Atlantic and the Mediterranean Sea. Mar Biol 136:191–199

    Article  Google Scholar 

  • Zulliger D, Tanner S, Ruch M, Ribi G (2009) Genetic structure of the high dispersal Atlanto-Mediterreanean sea star Astropecten aranciacus revealed by mitochondrial DNA sequences and microsatellite loci. Mar Biol 156:597–610

    Article  CAS  Google Scholar 

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Acknowledgments

Samples of Marthasterias glacialis from south Portugal were collected during the oceanographic expedition “LUSOEXPEDIÇÃO Olympus 2008” to the “Gorringe Seamounts”. This research was supported by a postdoctoral fellowship from the FCT of Portugal (Ref. SFRH/BPD/41055/2007) funded by the Pluriannual Program (FCT, UI&D 331/94, partially FEDER funded) and the project CMT2007-66635 (MARMOL) from the Spanish Ministry of Science. We strongly thank Xavier Mina for collecting samples from Mutriku, Pablo López for samples from Santander, Gustavo Martins and Joana Micael for samples from Azores, Fernando Roneberg for his help and support during the collection work and Sonia Chenu for her technical assistance in the laboratory.

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Authors and Affiliations

  1. Eco-Ethology Research Unit, Instituto Superior de Psicologia Aplicada (ISPA), Rua Jardim do Tabaco, 34, 1149-041, Lisbon, Portugal

    R. Pérez-Portela & V. Almada

  2. Department of Animal Biology (Invertebrates), Faculty of Biology, University of Barcelona, 645, Diagonal Avenue, 08028, Barcelona, Spain

    R. Pérez-Portela

  3. Center for Advanced Studies of Blanes (CEAB, CSIC), Accés a la Cala St. Francesc 14, 17300, Blanes, Girona, Spain

    A. Villamor

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  1. R. Pérez-Portela
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  2. A. Villamor
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  3. V. Almada
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Correspondence to R. Pérez-Portela.

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Communicated by S. Uthicke.

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Table 6 Haplotype frequencies of Marthasterias glacialis per population. Numbers in bold are private haplotypes
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Pérez-Portela, R., Villamor, A. & Almada, V. Phylogeography of the sea star Marthasterias glacialis (Asteroidea, Echinodermata): deep genetic divergence between mitochondrial lineages in the north-western mediterranean. Mar Biol 157, 2015–2028 (2010). https://doi.org/10.1007/s00227-010-1470-0

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