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Marine Biology

, Volume 156, Issue 4, pp 597–610 | Cite as

Genetic structure of the high dispersal Atlanto-Mediterreanean sea star Astropecten aranciacus revealed by mitochondrial DNA sequences and microsatellite loci

  • Deborah E. ZulligerEmail author
  • S. Tanner
  • M. Ruch
  • G. Ribi
Original Paper

Abstract

To investigate the impact of potential marine barriers on gene-flow in high dispersal marine invertebrates, we assessed the population genetic structure of the sea star Astropecten aranciacus. Samples were obtained from nine locations within the Atlantic and the Mediterranean Sea including populations east of the Siculo-Tunisian Strait. We obtained both DNA sequence data of the mitochondrial control region and genotype data at four microsatellite loci. Both markers were highly polymorphic and showed a great level of genetic diversity. Genetic differentiation between populations (FST) was in general low, particularly for nuclear data, as is often the case in high dispersal marine invertebrates. Nevertheless, both marker sets indicated a significant genetic differentiation of the population from the island of Madeira to most other populations. Our results also demonstrate a clear pattern of isolation-by-distance supported by both mitochondrial and nuclear markers. Therefore, we conclude that larval dispersal of A. aranciacus is somewhat limited even within the basins of the Atlantic, the west Mediterranean and the east Mediterranean. Microsatellite loci further revealed genetic differentiation between the three basins; however, it is not clear whether this is truly caused by marine barriers. Genetic differentiation between basins might also be a result of isolation-by-distance allowing for any grouping to be significant as long as geographical neighbors are clustered together. Although levels of genetic differentiation were less pronounced in microsatellite data, both datasets were coherent and revealed similar patterns of genetic structure in A. aranciacus.

Keywords

Genetic Differentiation Microsatellite Locus Allelic Richness Microsatellite Data Significant Genetic Differentiation 

Notes

Acknowledgments

We thank Luigia Santella, Teresa Cerveira Borges and the BIOPESCAS team (CCMAR, University of Algarve), Paulo Morais, Martin von Arx, Heinz Maag and Till Danckwart for providing specimens from Gaeta, Naples, Faro, Banyuls, Muravera and Cres. Santi Diliberto and Susanna Tassis enabled further sampling in Greece. Thomas Bucher, Andy Pemberton, Heinz Maag and Marco Bernasconi all provided lab and technical support. We are grateful for the assistance with data analyses that we received from Peter Wandeler, Tony Wilson and Rob Toonen and for helpful suggestions from anonymous reviewers. This project was funded in part by the Swiss National Science Foundation.

Supplementary material

227_2008_1111_MOESM1_ESM.doc (452 kb)
Electronic supplementary material (DOC 452 kb)

References

  1. Addison JA, Hart MW (2002) Characterization of microsatellite loci in sea urchins (Strongylocentrotus spp.). Mol Ecol Notes 493–494. doi: https://doi.org/10.1046/j.1471-8286.2002.00295.x Google Scholar
  2. Aquadro CF, Greenberg BD (1983) Human mitochondrial-DNA variation and evolution—analysis of nucleotide-sequences from 7 individuals. Genetics 103:287–312PubMedPubMedCentralGoogle Scholar
  3. Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial-DNA lineage survivorship in animal populations. J Mol Evol 20:99–105. doi: https://doi.org/10.1007/BF02257369 PubMedGoogle Scholar
  4. Baus E, Darrock DJ, Bruford MW (2005) Gene-flow patterns in Atlantic and Mediterranean populations of the Lusitanian sea star Asterina gibbosa. Mol Ecol 14:3373–3382. doi: https://doi.org/10.1111/j.1365-294X.2005.02681.x PubMedGoogle Scholar
  5. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate—a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 57:289–300Google Scholar
  6. Birky CW, Maruyama T, Fuerst P (1983) An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103:513–527PubMedPubMedCentralGoogle Scholar
  7. Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154. doi: https://doi.org/10.1093/jhered/93.2.153 CrossRefGoogle Scholar
  8. Borsa P, Blanquer A, Berrebi P (1997) Zoogéographie intraspécifique de la mer Méditerranée. Analyse des données génétiques populationnelles sur seize espèces atlanto-méditerranéennes (Poissons et Invertèbres). Vie Milieu 47:95–305Google Scholar
  9. Burla H, Pabst B, Stahel W (1976) Environmental-conditions affecting occurrence of Astropecten-Aranciacus (Asteroidea, Echinodermata). Helgol Wiss Meeresunters 28:167–182. doi: https://doi.org/10.1007/BF01610351 Google Scholar
  10. Burla H, Ribi G, Ferlin V, Pabst B (1972) Notes on ecology of Astropecten-Aranciacus. Mar Biol (Berl) 14:235Google Scholar
  11. 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 (Berl) 154:137–151. doi: https://doi.org/10.1007/s00227-008-0908-0 Google Scholar
  12. Carlon DB, Lippe C (2007) Eleven new microsatellite markers for the tropical sea urchin Tripneustes gratilla and cross-amplification in Tripneustes ventricosa. Mol Ecol Notes 7:1002–1004. doi: https://doi.org/10.1111/j.1471-8286.2007.01755.x Google Scholar
  13. Chenuil A, Le Gac M, Thierry M (2003) Fast isolation of microsatellite loci of very diverse repeat motifs by library enrichment in echinoderm species, Amphipholis squamata and Echinocardium cordatum. Mol Ecol Notes 3:324–327. doi: https://doi.org/10.1046/j.1471-8286.2003.00434.x Google Scholar
  14. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659. doi: https://doi.org/10.1046/j.1365-294x.2000.01020.x PubMedGoogle Scholar
  15. Colgan DJ, Byrne M, Rickard E, Castro LR (2005) Limited nucleotide divergence over large spatial scales in the asterinid sea star Patiriella exigua. Mar Biol (Berl) 146:263–270. doi: https://doi.org/10.1007/s00227-004-1415-6 Google Scholar
  16. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedPubMedCentralGoogle Scholar
  17. Costantini F, Fauvelot C, Abbiati M (2007) Genetic structuring of the temperate gorgonian coral (Corallium rubrum) across the western Mediterranean Sea revealed by microsatellites and nuclear sequences. Mol Ecol 16:5168–5182PubMedGoogle Scholar
  18. Diaz-Almela E, Boudry P, Launey S, Bonhomme F, Lapegue S (2004) Reduced female gene flow in the European flat oyster Ostrea edulis. J Hered 95:510–516. doi: https://doi.org/10.1093/jhered/esh073 PubMedGoogle Scholar
  19. Duran S, Palacin C, Becerro MA, Turon X, Giribet G (2004a) Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea). Mol Ecol 13:3317–3328. doi: https://doi.org/10.1111/j.1365-294X.2004.02338.x PubMedGoogle Scholar
  20. Duran S, Pascual M, Estoup A, Turon X (2004b) Strong population structure in the marine sponge Crambe crambe (Poecilosclerida) as revealed by microsatellite markers. Mol Ecol 13:511–522. doi: https://doi.org/10.1046/j.1365-294X.2004.2080.x PubMedGoogle Scholar
  21. ElMousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree Argania spinosa (L) Skeels endemic to Morocco. Theor Appl Genet 92:832–839. doi: https://doi.org/10.1007/BF00221895 Google Scholar
  22. Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Mol Ecol 11:1591–1604. doi: https://doi.org/10.1046/j.1365-294X.2002.01576.x PubMedPubMedCentralGoogle Scholar
  23. Excoffier L, Laval G, Schneider S (2005) ARLEQUIN (version 3.0): an integrated software package for population genetic data analysis. Bioinformatics Online 1:47–50Google Scholar
  24. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes—application to human mitochondrial-DNA restriction data. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  25. Féral J-P, Poulin E, Derelle E, Gallardo S, Chmbon C (1995) Genetic differentiation of Echinocardium chordatum as revealed by allozymes and RNA sequencing. In: Emson R, Smith A, Campbell A (eds) Echinoderm research 1995. Balkema, Rotterdam, pp 41–42Google Scholar
  26. Geldmacher J, Hoernle K (2000) The 72 Ma geochemical evolution of the Madeira hotspot (eastern North Atlantic): recycling of Paleozoic (≤500 Ma) oceanic lithosphere. Earth Planet Sci Lett 183:73–92. doi: https://doi.org/10.1016/S0012-821X(00)00266-1 Google Scholar
  27. Gerard K, Roby C, Chevalier N, Thomassin B, Chenuil A, Feral JP (2008) Assessment of three mitochondrial loci variability for the crown-of-thorns starfish: a first insight into Acanthaster phylogeography. C R Biol 331:137–143. doi: https://doi.org/10.1016/j.crvi.2007.11.005 PubMedGoogle Scholar
  28. Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486Google Scholar
  29. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372. doi: https://doi.org/10.2307/2532296 PubMedGoogle Scholar
  30. Hansen MM, Mensberg KLD, Berg S (1999) Postglacial recolonization patterns and genetic relationships among whitefish (Coregonus sp.) populations in Denmark, inferred from mitochondrial DNA and microsatellite markers. Mol Ecol 8:239–252. doi: https://doi.org/10.1046/j.1365-294X.1999.00557.x Google Scholar
  31. Harley CDG, Pankey MS, Wares JP, Grosberg RK, Wonham MJ (2006) Color polymorphism and genetic structure in the sea star Pisaster ochraceus. Biol Bull 211:248–262. doi: https://doi.org/10.2307/4134547 PubMedGoogle Scholar
  32. Harper FM, Addison JA, Hart MW (2007) Introgression versus immigration in hybridizing high-dispersal echinoderms. Evolution 61:2410–2418. doi: https://doi.org/10.1111/j.1558-5646.2007.00200.x PubMedGoogle Scholar
  33. Harper FM, Hart MW (2005) Gamete compatibility and sperm competition affect paternity and hybridization between sympatric Asterias sea stars. Biol Bull 209:113–126. doi: https://doi.org/10.2307/3593129 PubMedGoogle Scholar
  34. Hedrick PW (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318. doi: https://doi.org/10.2307/2640768 PubMedGoogle Scholar
  35. Hedrick PW (2005) A standardized genetic differentiation measure. Evolution 59:1633–1638PubMedGoogle Scholar
  36. Hörstadius S (1938) Über die Entwicklung von Astropecten aranciacus L. Pubbl Stn Zool Napoli 17:221–312Google Scholar
  37. 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. Mar Ecol Prog Ser 92:179–186. doi: https://doi.org/10.3354/meps092179 Google Scholar
  38. Koehler R (1921) Echinodermes. Faune de France, Lechevalier, Paris, pp 1–210Google Scholar
  39. Krafsur ES (2002) Population structure of the tsetse fly Glossina pallidipes estimated by allozyme, microsatellite and mitochondrial gene diversities. Insect Mol Biol 11:37–45. doi: https://doi.org/10.1046/j.0962-1075.2001.00307.x PubMedPubMedCentralGoogle Scholar
  40. 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. doi: https://doi.org/10.1093/jhered/93.5.331 PubMedGoogle Scholar
  41. Lemaire C, Versini JJ, Bonhomme F (2005) Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. J Evol Biol 18:70–80. doi: https://doi.org/10.1111/j.1420-9101.2004.00828.x PubMedGoogle Scholar
  42. Mariani S, Ketmaier V, de Matthaeis E (2002) Genetic structuring and gene flow in Cerastoderma glaucum (Bivalvia : Cardiidae): evidence from allozyme variation at different geographic scales. Mar Biol (Berl) 140:687–697. doi: https://doi.org/10.1007/s00227-001-0753-x Google Scholar
  43. Matsuoka N, Asano H (2003) Genetic variation in northern Japanese populations of the starfish Asterina pectinifera. Zool Sci 20:985–988. doi: https://doi.org/10.2108/zsj.20.985 PubMedGoogle Scholar
  44. McCartney MA, 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. doi: https://doi.org/10.1046/j.1365-294x.2000.01022.x PubMedGoogle Scholar
  45. McGoldrick DJ, Hedgecock D, English LJ, Baoprasertkul P, Ward RD (2000) The transmission of microsatellite alleles in Australian and North American stocks of the Pacific oyster (Crassostrea gigas): selection and null alleles. J Shellfish Res 19:779–788Google Scholar
  46. Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402PubMedGoogle Scholar
  47. Michalakis Y, Excoffier L (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics 142:1061–1064PubMedPubMedCentralGoogle Scholar
  48. Mougenot D, Vanney J-R (1982) The Plio-Quarternary sediment drifts of the south Portuguese continental slope. Bull Inst Geologie Bassin Aquitaine 31:131–139Google Scholar
  49. Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi: https://doi.org/10.1007/s10592-005-9056-y Google Scholar
  50. Nei M (1987) Molecular evolutionary genetics. Colombia University Press, New YorkGoogle Scholar
  51. Nelson RJ, Cooper G, Garner T, Schnupf P (2002) Polymorphic markers for the sea cucumber Parastichopus californicus. Mol Ecol Notes 2:233–235. doi: https://doi.org/10.1046/j.1471-8286.2002.00205.x Google Scholar
  52. Pabst B (1986) Eigenschaften der Dislokation bei drei Seesternarten der Gattung Astropecten. Inaugural-Dissertation, Universität ZürichGoogle Scholar
  53. Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific Sea urchins. Evolution 51:1506–1517. doi: https://doi.org/10.2307/2411203 PubMedGoogle Scholar
  54. Palumbi SR, Wilson AC (1990) Mitochondrial-DNA diversity in the Sea-Urchins Strongylocentrotus-Purpuratus and Strongylocentrotus-Droebachie. Evolution 44:403–415. doi: https://doi.org/10.2307/2409417 PubMedGoogle Scholar
  55. Parsons TJ, Muniec DS, Sullivan K, Woodyatt N, AllistonGreiner R, Wilson MR, Berry DL, Holland KA, Weedn VW, Gill P, Holland MM (1997) A high observed substitution rate in the human mitochondrial DNA control region. Nat Genet 15:363–368. doi: https://doi.org/10.1038/ng0497-363 PubMedGoogle Scholar
  56. Patarnello T, Volckaert F, Castilho R (2007) Pillars of Hercules: is the Atlantic–Mediterranean transition a phylogeographical break? Mol Ecol 16:4426–4444. doi: https://doi.org/10.1111/j.1365-294X.2007.03477.x PubMedGoogle Scholar
  57. Peijnenburg K, Fauvelot C, Breeuwer AJ, Menken SBJ (2006) Spatial and temporal genetic structure of the planktonic Sagitta setosa (Chaetognatha) in European seas as revealed by mitochondrial and nuclear DNA markers. Mol Ecol 15:3319–3338. doi: https://doi.org/10.1111/j.1365-294X.2006.03002.x PubMedGoogle Scholar
  58. Perez-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. doi: https://doi.org/10.1038/sj.hdy.6800160 PubMedGoogle Scholar
  59. Perez-Losada M, Nolte MJ, Crandall KA, Shaw PW (2007) Testing hypotheses of population structuring in the Northeast Atlantic ocean and Mediterranean sea using the common cuttlefish Sepia officinalis. Mol Ecol 16:2667–2679. doi: https://doi.org/10.1111/j.1365-294X.2007.03333.x PubMedGoogle Scholar
  60. Perrin C, Roy MS (2000) Rapid and efficient identification of microsatellite loci from the sea urchin, Evechinus chloroticus. Mol Ecol 9:2221–2223. doi: https://doi.org/10.1046/j.1365-294X.2000.105335.x PubMedGoogle Scholar
  61. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedPubMedCentralGoogle Scholar
  62. Quesada H, Zapata C, Alvarez G (1995) A multilocus Allozyme discontinuity in the Mussel Mytilus-Galloprovincialis—the interaction of ecological and life-history factors. Mar Ecol Prog Ser 116:99–115. doi: https://doi.org/10.3354/meps116099 Google Scholar
  63. Rogers AR, Harpending H (1992) Population-growth makes waves in the distribution of pairwise genetic-differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  64. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898. doi: https://doi.org/10.1111/j.1365-294X.2004.02255.x PubMedGoogle Scholar
  65. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedPubMedCentralGoogle Scholar
  66. Saavedra C, Pena JB (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. J Exp Mar Biol Ecol 323:138–150. doi: https://doi.org/10.1016/j.jembe.2005.03.006 Google Scholar
  67. Shanks AL, Grantham BA, Carr MH (2003) Propagule dispersal distance and the size and spacing of marine reserves. Ecol Appl 13:S159–S169. doi: https://doi.org/10.1890/1051-0761(2003)013[0159:PDDATS]2.0.CO;2 Google Scholar
  68. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417. doi: https://doi.org/10.1046/j.1365-294X.1999.00588.x Google Scholar
  69. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:1463 (vol 139, p 457, 1995)Google Scholar
  70. Slatkin M, Excoffier L (1996) Testing for linkage disequilibrium in genotypic data using the expectation–maximization algorithm. Heredity 76:377–383. doi: https://doi.org/10.1038/hdy.1996.55 PubMedGoogle Scholar
  71. Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36:545–554. doi: https://doi.org/10.1007/BF00556359 PubMedGoogle Scholar
  72. Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2004) Mitochondrial DNA variation in northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mol Ecol 13:1377–1390. doi: https://doi.org/10.1111/j.1365-294X.2004.02165.x PubMedGoogle Scholar
  73. Stamatis C, Triantafyllidis A, Moutou KA, Mamuris Z (2006) Allozymic variation in Northeast Atlantic and Mediterranean populations of Norway lobster, Nephrops norvegicus. Mark Sci 63:875–882. doi: https://doi.org/10.1016/j.icesjms.2006.01.006 Google Scholar
  74. Tajima F (1983) Evolutionary relationship of DNA-sequences in finite populations. Genetics 105:437–460PubMedPubMedCentralGoogle Scholar
  75. Tajima F (1989) The effect of change in population-size on DNA polymorphism. Genetics 123:597–601PubMedPubMedCentralGoogle Scholar
  76. Templeton AR, Crandall KA, Sing CF (1992) A cladistic-analysis of phenotypic Associations with Haplotypes Inferred from Restriction Endonuclease Mapping and DNA-Sequence Data. 3. Cladogram Estimation. Genetics 132:619–633PubMedPubMedCentralGoogle Scholar
  77. 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 140:767–782PubMedPubMedCentralGoogle Scholar
  78. Tintore J, Laviolette PE, Blade I, Cruzado A (1988) A study of an intense density front in the Eastern Alboran-Sea–the Almeria-Oran Front. J Phys Oceanogr 18:1384–1397. doi :10.1175/1520-0485(1988)018<1384:ASOAID>2.0.CO;2Google Scholar
  79. Tortonese E (1980) Apérçu sommaire sur les asteroidea de la Méditerrannée (histoire, distribution, systematique). Journées d’études sur la systématique évolutive et la biogéographie en Méditerranée, Cagliari, pp 11–19Google Scholar
  80. Triantafyllidis A, Apostolidis AP, Katsares V, Kelly E, Mercer J, Hughes M, Jorstad K, Tsolou A, Hynes R, Triantaphyllidis C (2005) Mitochondrial DNA variation in the European lobster (Homarus gammarus) throughout the range. Mar Biol (Berl) 146:223–235. doi: https://doi.org/10.1007/s00227-004-1435-2 Google Scholar
  81. Turan C, Carvalho GR, Mork J (1998) Molecular genetic analysis of Atlanto-Scandian herring (Clupea harengus) populations using allozymes and mitochondrial DNA markers. J Mar Biol Assoc UK 78:269–283Google Scholar
  82. 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. doi: https://doi.org/10.1046/j.1365-294X.2003.01954.x PubMedGoogle Scholar
  83. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. doi: https://doi.org/10.1111/j.1471-8286.2004.00684.x Google Scholar
  84. 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. doi: https://doi.org/10.1016/j.ympev.2003.11.014 PubMedGoogle Scholar
  85. Waters JM, Roy MS (2004) Phylogeography of a high-dispersal New Zealand sea-star: does upwelling block gene-flow? Mol Ecol 13:2797–2806. doi: https://doi.org/10.1111/j.1365-294X.2004.02282.x PubMedGoogle Scholar
  86. Watterson GA (1984) Allele frequencies after a Bottleneck. Theor Popul Biol 26:387–407. doi: https://doi.org/10.1016/0040-5809(84)90042-X Google Scholar
  87. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution Int J Org Evolution 38:1358–1370. doi: https://doi.org/10.2307/2408641 Google Scholar
  88. Williams ST (2000) Species boundaries in the starfish genus Linckia. Mar Biol (Berl) 136:137–148. doi: https://doi.org/10.1007/s002270050016 Google Scholar
  89. Williams ST, Benzie JAH (1997) Indo-West Pacific patterns of genetic differentiation in the high-dispersal starfish Linckia laevigata. Mol Ecol 6:559–573. doi: https://doi.org/10.1046/j.1365-294X.1997.00221.x Google Scholar
  90. Williams ST, Benzie JAH (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. doi: https://doi.org/10.2307/2410923 PubMedGoogle Scholar
  91. Williams ST, Jara J, Gomez E, Knowlton N (2002) The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr Comp Biol 42:941–952. doi: https://doi.org/10.1093/icb/42.5.941 PubMedGoogle Scholar
  92. Xia X, Xie Z (2001) DAMBE: Software package for data analysis in molecular biology and evolution. J Hered 92:371–373. doi: https://doi.org/10.1093/jhered/92.4.371 PubMedGoogle Scholar
  93. Yasuda N, Nagai S, Hamaguchi M, Lian CL, Nadaoka K (2006) Development of microsatellite markers for the crown-of-thorns starfish Acanthaster planci. Mol Ecol Notes 6:141–143. doi: https://doi.org/10.1111/j.1471-8286.2005.01168.x Google Scholar
  94. 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 (Berl) 136:191–199. doi: https://doi.org/10.1007/s002270050676 Google Scholar
  95. Zavodnik D (1960) Echinodermata der Insel Krk. Acta Adriat 9:3–19Google Scholar
  96. Zhan AB, Bao ZM, Lu W, Hu XL, Peng W, Wang ML, Hu JJ (2007) Development and characterization of 45 novel microsatellite markers for sea cucumber (Apostichopus japonicus). Mol Ecol Notes 7:1345–1348. doi: https://doi.org/10.1111/j.1471-8286.2007.01876.x Google Scholar
  97. Zulliger D, Ruch M, Tanner S, Ribi G (2008) Characterization of nine microsatellite loci in the sea star Astropecten aranciacus and cross-species amplification for related taxa. Mol Ecol Res 8:634–636. doi: https://doi.org/10.1111/j.1471-8286.2007.02027.x Google Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Deborah E. Zulliger
    • 1
    Email author
  • S. Tanner
    • 1
  • M. Ruch
    • 1
  • G. Ribi
    • 1
  1. 1.Zoological Museum of the University of ZurichZurichSwitzerland

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