Abstract
The Southern Ocean benthic communities are characterized by their levels of endemism and their diversity of invertebrate brooding species. Overall, biological processes acting within these species remain poorly understood despite their importance to understand impacts of ongoing global change. We take part in filling this gap by studying the genetic structure over different spatial scales (from centimeters to tens of kilometers) in Abatus cordatus, an endemic and brooding sea urchin from the Kerguelen Islands. We developed three microsatellites and two exon-primed intron crossing markers and conducted a two-scale sampling scheme (from individuals to patches) within two dense localities of Abatus cordatus. Between patches, all pairwise comparisons, covering distances from few meters (between patches within locality) to 25 km (between localities), revealed significant genetic differentiation, a higher proportion of the molecular variance being explained by the comparisons between localities than within localities, in agreement with an isolation by distance model. Within patches, we found no significant correlation between individual pairwise spatial and genetic distances, except for the most polymorphic locus in the patch where the largest range of geographical distances had been analyzed. This study provides an estimation of the dispersal capacities of Abatus cordatus and highlights its low recolonization ability. Similar low recolonization capacities are thus expected in other Antarctic and Subantarctic brooding invertebrate species and suggest a high vulnerability of these species facing global change.
Similar content being viewed by others
References
Addison J, Hart M (2005) Spawning, copulation and inbreeding coefficients in marine invertebrates. Biol Bull 1:450–453
Agustí S, Sejr MK, Duarte CM (2010) Impacts of climate warming on polar marine and freshwater ecosystems. Polar Biol 33:1595–1598
Arnaud JF, Madec L, Guiller A, Bellido A (2001) Spatial analysis of allozyme and microsatellite DNA polymorphisms in the land snail Helix aspersa (Gastropoda: Helicidae). Mol Ecol 10:1563–1576
Arndt A, Smith MJ (1998) Genetic diversity and population structure in two species of sea cucumber: differing patterns according to mode of development. Mol Ecol 7:1053–1064
Aronson RB, Thatje S, Clarke A, Peck LS, Blake DB, Wilga CD, Seibel BA (2008) Climate change and invasibility of the Antarctic benthos. Annu Rev Ecol Evol Syst 38:129–154
Aurelle D, Cattaneo-Berrebi G, Berrebi P (2002) Natural and artificial secondary contact in brown trout (Salmo trutta, L.) in the French Western Pyrenees assessed by allozymes and microsatellites. Heredity 89:171–183
Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, populations, interactions, CNRS UMR 5000. Université de Montpellier II, Montpellier, France
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B-Stat Methodol 57:289–300
Berrebi P, Boissin E, Fang F, Cattaneo-Berrebi G (2005) Intron polymorphism (EPIC-PCR) reveals phylogeographic structure of Zacco platypus in China: a possible target for aquaculture development. Heredity 94:589–598
Bhattacharya CG (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23:115–135
Bierne N, Lehnert SA, Bédier E, Bonhomme F, Moore SS (2000) Screening for intron-length polymorphisms in penaeid shrimps using exon-primed intron-crossing (EPIC)-PCR. Mol Ecol 9:233–235
Boissin E, Hoareau TB, Feral JP, Chenuil A (2008) Extreme selfing rates in the cosmopolitan brittle star species complex Amphipholis squamata: data from progeny-array and heterozygote deficiency. Mar Ecol Prog Ser 361:151–159
Born C, Hardy OJ, Chevallier MH, Ossari S, Attéké C, Wickings EJ, Hossaert-McKey M (2008) Small-scale spatial genetic structure in the Central African rainforest tree species Aucoumea klaineana: a stepwise approach to infer the impact of limited gene dispersal, population history and habitat fragmentation. Mol Ecol 17:2041–2050
Bradbury IR, Bentzen P (2007) Non-linear isolation by distance: implications for dispersal estimation in anadromous and marine fish populations. Mar Ecol Prog Ser 340:245–257
Broquet T, Petit EJ (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216
Calderón I, Palacin C, Turon X (2009) Microsatellite markers reveal shallow genetic differentiation between cohorts of the common sea urchin Paracentrotus lividus (Lamarck) in northwest Mediterranean. Mol Ecol 18:3036–3049
Carlon DB, Lippé 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
Castric V, Belkhir K, Bernatchez L, Bonhomme F (2002) Heterozygote deficiencies in small lacustrine populations of brook charr Salvelinus fontinalis Mitchill (Pisces, Salmonidae): a test of alternative hypotheses. Heredity 89:27–35
Chakraborty R, Andrade MD, Daiger SP, Budowle B (1992) Apparent heterozygote deficiencies observed in DNA typing data and their implications in forensic applications. Ann Hum Genet 56:45–57
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Chapuis MP, Lecoq M, Michalakis Y, Loiseau A, Sword GA, Piry S, Estoup A (2008) Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles. Mol Ecol 17:3640–3653
Chenuil A (2006) Choosing the right molecular genetic markers for studying biodiversity: from molecular evolution to practical aspects. Genetica 127:101–120
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
Chenuil A, Gault A, Feral JP (2004) Paternity analysis in the Antarctic brooding sea urchin Abatus nimrodi: a pilot study. Polar Biol 27:177–182
Chenuil A, Hoareau TB, Egea E, Penant G, Rocher C, Aurelle D, Mokhtar-Jamai K, Bishop JDD, Boissin E, Diaz A, Krakau M, Luttikhuizen PC, Patti FP, Blavet N, Mousset S (2010) An efficient method to find potentially universal population genetic markers, applied to metazoans. BMC Evol Biol 10:276
Cornuet JM, Piry S, Luikart G, Estoup A, Solignac M (1999) New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153:1989–2000
Costello MJ, Coll M, Danovaro R, Halpin P, Ojaveer H, Miloslavich P (2010) A census of marine biodiversity knowledge, resources, and future challenges. PLoS One 5:e12110
David P, Perdieu M, Pernot A, Jarne P (1997) Fine-grained spatial and temporal population genetic structure in the marine bivalve Spisula ovalis. Evolution 51:1318–1322
David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487
De Ridder C, David B, Larrain A (1993) Antarctic and subantarctic echinoids from ‘Marion Dufresne’ expeditions MD03, MD04, MD08 and from the ‘Polarstern’ expedition Epos III. Bull Mus Nat Hist Nat Paris 14:405–441
Dell RK (1972) Antarctic benthos. Adv Mar Biol 10:1–216
Dempster A, Laird N, Rubin D (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc Ser B Stat Methodol 39:1–38
Diaz A, Féral JP, David B, Saucède T, Poulin E (2011) Evolutionary pathways among shallow and deep sea echinoids of the genus Sterechinus in the Southern Ocean. Deep Sea Res Part II 58 SI:205–211
Dupont L, Bernas D, Viard F (2007) Sex and genetic structure across age groups in populations of the European marine invasive mollusc, Crepidula fornicata L. (Gastropoda). Biol J Linnean Soc 90:365–374
Dupont L, Viard F, Dowell MJ, Wood C, Bishop JDD (2009) Fine- and regional-scale genetic structure of the exotic ascidian Styela clava (Tunicata) in southwest England, 50 years after its introduction. Mol Ecol 18:442–453
Epperson B (1995) Fine-scale spatial structure: correlation for individual genotypes differ from those for local gene-frequencies. Evolution 49:1022–1026
Estoup A, Rousset F, Michalakis Y, Cornuet JM, Adriamanga M, Guyomard R (1998) Comparative analysis of microsatellite and allozyme markers: a case study investigating microgeographic differentiation in brown trout (Salmo trutta). Mol Ecol 7:339–353
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 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics 164:1567–1587
Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: Dominant markers and null alleles. Mol Ecol Notes 7:574–578
Fenster CB, Vekemans X, Hardy OJ (2003) Quantifying gene flow from spatial genetic structure data in a metapopulation of Chamaecrista fasciculata (Leguminosae). Evolution 57:995–1007
Féral JP (2002) How useful are the genetic markers in attempts to understand and manage biodiversity? J Exp Mar Biol Ecol 268:121–145
Féral JP, Poulin E (1994) Growth, recruitment and age structure of Abatus cordatus, a brood protecting schizasterid. SCAR sixth biology symposium. Antarctic communities: species, structure and survival, Venice, 30 May–3 June 1994. Univ. Padova, Padova, p 91
Féral JP, Poulin E (2011) Kerguelen Islands: a living laboratory to understand the benthic biodiversity of the Antarctic. In: Duhamel G, Welsford D (eds) The Kerguelen plateau, marine ecosystem and fisheries. Société Française d'Ichtyologie, Paris, pp 151–156
Féral JP, Villard AM, Barré N, Chenuil A (2003) What is the smallest distance of genetic differentiation in the brood protecting ophiuroid Amphipholis squamata from Western Mediterranean? In: Féral JP, David B (eds) Echinoderm research. Proceedings of 6th European conference on Echinoderm, Banyuls-sur-mer, France. Swets and Zeitlinger Publishers, Lisse, pp 23–27
Gérard K, Bierne N, Borsa P, Chenuil A, Féral JP (2008) Pleistocene separation of mitochondrial lineages of Mytilus spp. mussels from Northern and Southern Hemispheres and strong genetic differentiation among southern populations. Mol Phylogenet Evol 49:84–91
Gil DG, Zaixso HE, Tolosano JA (2009) Brooding of the sub-Antarctic heart urchin, Abatus cavernosus (Spatangoida: Schizasteridae), in Southern Patagonia. Mar Biol 156:1647–1657
González-Wevar CA, Nakano T, Cañete JI, Poulin E (2010) Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean. Mol Phylogenet Evol 56:115–124
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.html. Updated from Goudet (1995)
Griffiths HJ (2010) Antarctic marine biodiversity—what do we know about the distribution of life in the Southern Ocean? PLoS One 5:e11683
Guo S, Thompson E (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372
Gutt J, Sirenko BI, Smirnov IS, Arntz WE (2004) How many macrozoobenthic species might inhabit the Antarctic shelf? Antarct Sci 16:11–16
Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620
Held C, Leese F (2007) The utility of fast evolving molecular markers for studying speciation in the Antarctic benthos. Polar Biol 30:513–521
Held C, Wägele JW (2005) Cryptic speciation in the giant Antarctic isopod Glyptonotus antarcticus (Isopoda: Valvifera: Chaetiliidae). Sci Mar 69:175–181
Hendry AP, Lohmann LG, Conti E, Cracraft J, Crandall KA, Faith DP, Hauser C, Joly CA, Kogure K, Larigauderie A, Magallon S, Moritz C, Tillier S, Zardoya R, Prieur-Richard AH, Walther BA, Yahara T, Donoghue MJ (2010) Evolutionary biology in biodiversity science, conservation and policy: a call to action. Evolution 64:1517–1528
Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, Van der Veer HW, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc B Biol Sci 272:497–503
Hoffman JI, Clarke A, Linse K, Peck LS (2011) Effects of brooding and broadcasting reproductive modes on the population genetic structure of two Antarctic gastropod molluscs. Mar Biol 158:287–296
Hunt A (1993) Effects of contrasting patterns of larval dispersal on the genetic connectedness of local populations of two intertidal starfish, Patiriella calcar and P. exigua. Mar Ecol Prog Ser 92:179–186
Jarman SN, Elliott NG, Nicol S, McMinn A (2002) Genetic differentiation in the Antarctic coastal krill Euphausia crystallorophias. Heredity 88:280–287
Jarne P, Lagoda PJL (1996) Microsatellites, from molecules to populations and back. Trends Ecol Evol 11:424–429
Kalinowski ST (2002) How many alleles per locus should be used to estimate genetic distances? Heredity 88:62–65
Krug AZ, Jablonski D, Roy K (2010) Differential extinction and the contrasting structure of polar marine faunas. PLoS One 5:e15362
Lavergne S, Mouquet N, Thuiller W, Ronce O (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol Syst 41:321–350
Leblois R, Estoup A, Rousset F (2003) Influence of mutational and sampling factors on the estimation of demographic parameters in a “continuous” population under isolation by distance. Mol Biol Evol 20:491–502
Ledoux JB, Mokthar-Jamaï K, Roby C, Féral JP, Garrabou J, Aurelle D (2010a) Genetic survey of shallow populations of the Mediterranean red coral [Corallium rubrum (Linnaeus, 1758)]: new insights into evolutionary processes shaping nuclear diversity and implications for conservation. Mol Ecol 19:675–690
Ledoux JB, Garrabou J, Bianchimani O, Drap P, Féral JP, Aurelle D (2010b) Fine-scale genetic structure and inferences on population biology in the threatened Mediterranean red coral, Corallium rubrum. Mol Ecol 19:4204–4216
Lemer S, Rochel E, Planes S (2011) Correction method for null alleles in species with variable microsatellite flanking regions, a case study of the black-lipped pearl oyster Pinctada margaritifera. J Hered 102:243–246
Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Sychotria officinalis (Rubiaceae). Am J Bot 82:1420–1425
McCartney MA, Brayer K, Levitan DR (2004) Polymorphic microsatellite loci from the red urchin, Strongylocentrotus franciscanus, with comments on heterozygote deficit. Mol Ecol Notes 4:226–228
Murray J (1885) Notes on the reproduction of certain echinoderms from the Southern Ocean. Rep Sci Res ‘Challenger’ Expedition (Her Majesty’s Stationery Office) 1:379–396
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686
Palumbi SR (2003) Population genetics, demographic connectivity, and the design of marine reserves. Ecol Appl 13:S146–S148
Poulin E (1996) Signification adaptative et conséquences évolutives de l’incubation chez un invertébré marin benthique subantarctique, Abatus cordatus (Verrill, 1876). PhD thesis, Université Montpellier II
Poulin E, Féral JP (1994) The fiction and the facts of antarctic incubation—population genetics and phylogeny of schizasterid echinoids. In: David B, Guille A, Féral JP, Roux M (eds) Echinoderms through time. Proceedings of the 8th international echinoderm conference, Dijon, France. Balkema, Rotterdam, pp 837–843
Poulin E, Féral JP (1995) Pattern of spatial distribution of a brood-protecting schizasterid echinoid, Abatus cordatus, endemic to the Kerguelen Islands. Mar Ecol Prog Ser 118:179–186
Poulin E, Féral JP (1996) Why are there so many species of brooding Antarctic echinoids? Evolution 50:820–830
Poulin E, von Boletzky S, Feral JP (2001) Combined ecological factors permit classification of developmental patterns in benthic marine invertebrates: a discussion note. J Exp Mar Biol Ecol 257:109–115
Poulin E, Palma AT, Féral JP (2002) Evolutionary versus ecological success in Antarctic benthic invertebrates. Trends Ecol Evol 17:218–222
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Pritchard JK, Wen X, Falush D (2007) Documentation for the STRUCTURE software, Version 2. Chicago. Available at http://pritch.bds.uchicago.edu. Accessed March 2011
Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 144:383–387
Raymond M, Rousset F (1995) GENEPOP (ver. 1.2): a population genetics software for exact test and ecumenicism. J Hered 86:248–249
Reusch TBH, Stam WT, Olsen JL (2000) A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant. Mol Ecol 9:127–140
Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Philos Trans R Soc B Biol Sci 362:2191–2214
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253
Rousset F (1997) Genetic differentiation and estimation of gene flow from F statistics under isolation by distance. Genetics 145:1219–1228
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62
Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Resour 8:103–106
Ryman N, Palm S, André C, Carvalho GR, Dahlgren TG, Jorde PE, Laikre L, Larsson LC, Palmé A, Ruzzante DE (2006) Power for detecting genetic divergence: differences between statistical methods and marker loci. Mol Ecol 15:2031–2045
Schatt P, Feral JP (1991) The brooding cycle of Abatus cordatus (Echinodermata, Spatangoida) at Kerguelen Islands. Polar Biol 11:283–292
Selkoe KA, Toonen RJ (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
Slattery M, Bosch I (1993) Mating-behavior of a brooding antarctic Asteroid, Neosmilaster georgianus. Invertebr Reprod Dev 24:97–102
Smetacek V, Nicol S (2005) Polar ocean ecosystems in a changing world. Nature 437:362–368
Stevens MI, Hogg ID (2006) Contrasting levels of mitochondrial DNA variability between mites (Penthalodidae) and springtails (Hypogastruridae) from the Trans-Antarctic Mountains suggest long-term effects of glaciation and life history on substitution rates, and speciation processes. Soil Biol Biochem 38:3171–3180
Tarnowska K, Chenuil A, Nikula R, Féral JP, Wolowicz M (2010) Complex genetic population structure of the bivalve Cerastoderma glaucum in a highly fragmented lagoon habitat. Mar Ecol Prog Ser 406:173–184
Teixido N, Garrabou J, Arntz WE (2002) Spatial pattern quantification of Antarctic benthic communities using landscape indices. Mar Ecol Prog Ser 242:1–14
Teixido N, Garrabou J, Gutt J, Arntz WE (2007) Iceberg disturbance and successional spatial patterns: the case of the shelf Antarctic benthic communities. Ecosystems 10:142–157
Thatje S (2005) The future fate of the Antarctic marine biota? Trends Ecol Evol 20:418–419
Thatje S, Hillenbrand CD, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540
Thomson CW (1878) Notice of some peculiarities on the mode of propagation of certain echinoderms of the southern seas. Zool J Linn Soc 13:55–79
Thornhill DJ, Mahon AR, Norenburg JL, Halanych KM (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Mol Ecol 17:5104–5117
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 6:255–256
Vaughan DG, Marshall GJ, Connolley WM, Parkinson C, Mulvaney R, Hodgson DA, King JC, Pudsey CJ, Turner J (2003) Recent rapid regional climate warming on the Antarctic Peninsula. Clim Change 60:243–274
Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935
Verrill AE (1876) Contribution to the natural history of Kerguelen Island. Annelids and Echinoderms. Bull US Natl Mus 3:64–75
Waples RS, Gaggiotti O (2006) What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Mol Ecol 15:1419–1439
Waples RS, Punt AE, Cope JM (2008) Integrating genetic data into management of marine resources: how can we do it better? Fish Fish 9:423–429
Watts PC, Rousset F, Saccheri IJ, Leblois R, Kemp SJ, Thompson DJ (2007) Compatible genetic and ecological estimates of dispersal rates in insect (Coenagrion mercuriale: Odonata: Zygoptera) populations: analysis of ‘neighbourhood size’ using a more precise estimator. Mol Ecol 16:737–751
Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wilson NG, Hunter RL, Lockhart SJ, Halanych KM (2007) Multiple lineages and absence of panmixia in the “circumpolar” crinoid Promachocrinus kerguelensis from the Atlantic sector of Antarctica. Mar Biol 152:895–904
Wilson NG, Schrodl M, Halanych KM (2009) Ocean barriers and glaciation: Evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984
Yasuda N, Nagai S, Hamaguchi M, Okaji K, Gérard K, Nadaoka K (2009) Gene flow of Acanthaster planci (L.) in relation to ocean currents revealed by microsatellite analysis. Mol Ecol 18:1574–1590
Yund PO (2000) How severe is sperm limitation in natural populations of marine free-spawners? Trends Ecol Evol 15:10–13
Zane L, Ostellari L, Maccatrozzo L, Bargelloni L, Battaglia B, Patarnello T (1998) Molecular evidence for genetic subdivision of Antarctic krill populations. Proc R Soc B-Biol Sci 265:2387–2391
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 Resour 8:634–636
Acknowledgments
Development of EPIC markers, corresponding salaries, and genotyping was possible owing to two European networks of excellence, NoE MARBEF (GOCE-CT-2003-505446) and NoE Marine Genomics Europe (GOCE-CT-2004-505403) and a French ANR Antflock. Logistic and collection of Abatus cordatus were supported by the program Macrobenthos no 195 of the French Polar Institute (IPEV), and thanks to Thomas Abiven for help in samples collection and management in fieldwork.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ledoux, JB., Tarnowska, K., Gérard, K. et al. Fine-scale spatial genetic structure in the brooding sea urchin Abatus cordatus suggests vulnerability of the Southern Ocean marine invertebrates facing global change. Polar Biol 35, 611–623 (2012). https://doi.org/10.1007/s00300-011-1106-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-011-1106-y