Polar Biology

, Volume 39, Issue 1, pp 77–89 | Cite as

Out of Antarctica: quaternary colonization of sub-Antarctic Marion Island by the limpet genus Nacella (Patellogastropoda: Nacellidae)

  • Claudio A. González-WevarEmail author
  • Steven L. Chown
  • Simon Morley
  • Nestor Coria
  • Thomas Saucéde
  • Elie Poulin
Original Paper


The distribution of the Southern Ocean nearshore marine benthic fauna is the consequence of major geologic, oceanographic, and climatic changes during the last 50 Ma. As a result, a main biogeographic principle in the Southern Ocean is the clear distinction of the Antarctic biota. The Antarctic Polar Front (APF) represents an important barrier between Antarctica and other sub-Antarctic provinces. However, the high degree of genetic affinity between populations of the Antarctic limpet Nacella concinna and its sub-Antarctic relative Nacella delesserti from Marion Island stands against this tenet. Here, we performed new phylogenetic reconstructions in Nacella with special emphasis on the relationship between N. concinna and N. delesserti. Similarly, we performed population-based analyses in N. concinna and N. delesserti to further understand the genetic legacy of the Quaternary glacial cycles. Phylogenetic reconstructions recognized N. concinna and N. delesserti as two closely but distinct monophyletic entities and therefore as valid evolutionary units. The cladogenetic process separating them occurred ~0.35 Ma and is consistent with the origin of Marion Island (~0.45 Ma). Exceptional long-distance dispersal between provinces located inside and outside the APF, rather than revealing the permeability of the Antarctic Polar Front, seems to be related to latitudinal shift in the position of the APF during coldest periods of the Quaternary. Diversity indices, neutrality tests, haplotype networks, and demographic inference analysis showed that the demography of both species exhibits a clear signal of postglacial expansion.


Biogeography Southern Ocean Antarctic Polar Front Long-distance dispersal Marion Island Bayesian skyline plot 



INACH Office project G_04_11, PhD thesis projects INACH B_01-07, Conicyt 24090009 and postdoctorate fellowship 3120075 (C.G-W), projects INACH 02-02 & 13-05 and Ecos C06B02 (E.P). Institute of Ecology and Biodiversity (IEB, Universidad de Chile) ICM-P05-002 & PFB-023- CONICYT. Census of Antarctic Marine Life (CAML), EBA-SCAR and PROSUL-Brazil for encouraging and supporting Antarctic research in Evolution. Simon Morley was funded by the British Antarctic Survey (BAS). Program JR230 of the British Antarctic Survey (T.S). This work was supported by South African National Research Foundation Grant SNA2011110700005. Collections on Marion Island were made with the assistance of Aleks Terauds, Jennifer Lee, and Susana Clusella-Trullas.


  1. Aljanabi S, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res 25:4692–4693PubMedCrossRefPubMedCentralGoogle Scholar
  2. Allcock A, Strugnell J (2012) Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol Evol 27:520–528PubMedCrossRefGoogle Scholar
  3. Antezana T (1999) Plankton of Southern Chilean fjords: trends and linkages. Sci Mar 63 (Supll 1):69–80Google Scholar
  4. Aronson R, Thatje S, Clarke A, Peck L, Blake D, Wilga C, Seibel B (2007) Climate change and invasibility of the Antarctic benthos. Annu Rev Ecol Evol Syst 38:129–154CrossRefGoogle Scholar
  5. Bargelloni L, Marcato S, Zane L, Patarnello T (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst Biol 49:114–129PubMedCrossRefGoogle Scholar
  6. Barker P, Filippelli G, Florindo F, Martin E, Scher H (2007) Onset and role of the Antarctic circumpolar current. Deep-Sea Res Pt II 54:2388–2398CrossRefGoogle Scholar
  7. Barnes D, Hodgson D, Convey P, Allen C, Clarke A (2006) Incursion and excursion of Antarctic biota: past, present and future. Global Ecol Biogeogr 15:121–142CrossRefGoogle Scholar
  8. Bird C, Holland B, Bowen B, Toonen R (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186PubMedCrossRefGoogle Scholar
  9. Blankley W, Branch G (1985) Ecology of the limpet Nacella delesserti (Phillipi) at Marion Island in the Sub-Antarctic Southern Ocean. J Exp Mar Biol Ecol 92:259–281CrossRefGoogle Scholar
  10. Bölter M, Beyer L, Stonehouse B (2002) Antarctic Coastal landscapes: characteristics, ecology and research. In: Beyer L, Bölter M (eds) Ecological studies geoecology of antarctic ice-free coastal landscapes. Springer, Berlin, pp 5–9CrossRefGoogle Scholar
  11. Bowden D, Clarke A, Peck L, Barnes D (2006) Antarctic sessile marine benthos: colonisation and growth on artificial substrata over three years. Mar Ecol Prog Ser 316:1–16CrossRefGoogle Scholar
  12. Chown SL, Froneman PW (2008) The Prince Edward Islands. Land-Sea interactions in a changing ecosystem. Sunderland Press, Stellenbosch 470 ppGoogle Scholar
  13. Chown S, Gremmen N, Gaston K (1998) Biogeography of Southern Ocean Islands: species-areas relationships, human impacts, and conservation. Am Nat 152:562–575PubMedCrossRefGoogle Scholar
  14. Clarke A, Crame J (1989) The origin of the Southern Ocean marine fauna. Geol Soc Lond Spec Publ 47:253–268Google Scholar
  15. Clarke A, Crame J (2010) Evolutionary dynamics at high latitudes: speciation and extinction in polar marine faunas. Phil Trans R Soc B 365:3655–3666PubMedCrossRefPubMedCentralGoogle Scholar
  16. Clarke A, Barnes D, Hodgson D (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3Google Scholar
  17. Clarke A, Crame J, Stromberg J, Barker P (1992) The Southern Ocean benthic fauna and climate change: a historical perspective [and discussion]. Philos Trans R Soc Lond Ser B Biol Sci 338:299–309Google Scholar
  18. Convey P, Stevens M, Hodgson D, Smellie J, Hillenbrand C, Barnes D, Clarke A, Pugh P, Linse K, Cary S (2009) Exploring biological constraints on the glacial history of Antarctica. Quat Sci Rev 28:3035–3048CrossRefGoogle Scholar
  19. Crame J (1999) An evolutionary perspective on marine faunal connection between southernmost South America and Antarctica. Sci Mar (Supl. 1) 63:1–14Google Scholar
  20. Cumming RA, Nikula R, Spencer HG, Waters JM (2014) Transoceanic genetic similarities of kelp-associated sea slug populations: long-distance dispersal via rafting? J Biogeogr. doi: 10.1111/jbi.12376 Google Scholar
  21. Dalziel I, Lawver L, Pearce J, Barker P, Hastie A, Barfod D, Schenke H, Davis M (2013) A potential barrier to deep Antarctic circumpolar flow until the late Miocene? Geology 41:947–950CrossRefGoogle Scholar
  22. Darriba D, Taboada G, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772PubMedCrossRefPubMedCentralGoogle Scholar
  23. de Aranzamendi M, Gardenal C, Martin J, Bastida R (2009) Limpets of the genus Nacella (Patellogastropoda) from the Southwestern Atlantic: species identification based on molecular data. J Mollus Stud 75:241–251CrossRefGoogle Scholar
  24. de Aranzamendi M, Bastidas R, Gardenal C (2011) Different evolutionary histories in two sympatric limpets of the genus Nacella (Patellogastropoda) in the South-western Atlantic coast. Mar Biol 158:2405–2418CrossRefGoogle Scholar
  25. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886PubMedCrossRefGoogle Scholar
  26. Dell R (1972) Antarctic Benthos. Adv Mar Biol 10:1–216CrossRefGoogle Scholar
  27. DeVries T (2009) Cenozoic Nacella (Patellogastropoda: Nacellidae) from Peru and Chile: filling in the gaps. Veliger 50:274–291Google Scholar
  28. Díaz A, Féral J, 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 II 58:205–211CrossRefGoogle Scholar
  29. Drummond A, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214PubMedCrossRefPubMedCentralGoogle Scholar
  30. Drummond A, Ho S, Phillips M, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88PubMedCrossRefPubMedCentralGoogle Scholar
  31. Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2010) Geneious v5.5
  32. Drummond A, Suchard M, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973PubMedCrossRefPubMedCentralGoogle Scholar
  33. Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of population. Mol Ecol 11:2571–2581PubMedCrossRefGoogle Scholar
  34. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedCentralGoogle Scholar
  35. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376PubMedCrossRefGoogle Scholar
  36. Filatov D (2009) Processing and population genetic analysis of multigenic datasets with ProSeq3 software. Bioinformatics 25:3189–3190PubMedCrossRefPubMedCentralGoogle Scholar
  37. Flower B, Kennett J (1994) The middle Miocene climatic transition: East Antarctic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeogr Palaeocl 108:537–555CrossRefGoogle Scholar
  38. Fraser C, Nikula R, Spencer H, Waters J (2009) Kelp genes reveal effects of subantarctic sea during the last glacial maximum. Proc Nat Acad Sci USA 106:3249–3253PubMedCrossRefPubMedCentralGoogle Scholar
  39. Froneman P, Perissinotto R, Pakhomov E (1997) Biogeographical structure of the microphytoplankton assemblages in the region of the subtropical convergence and across a warmcore eddy during austral winter. J Plankton Res 19:519–521CrossRefGoogle Scholar
  40. Gersonde R, Crosta X, Abelmann A, Armand L (2005) Sea-surface temperature and sea ice distribution of the Southern Ocean at the EPILOG last glacial maximum: a circum-Antarctic view based on siliceous microfossil records. Quat Sci Rev 24:869–896CrossRefGoogle Scholar
  41. Goldstien S, Schiel D, Gemmel N (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268PubMedCrossRefGoogle Scholar
  42. González-Wevar C, Nakano T, Cañete J, Poulin E (2010) Molecular phylogeny and historical biogeography of Nacella (Patellogastropoda: Nacellidae) in the Southern Ocean. Mol Phylogenet Evol 56:115–124PubMedCrossRefGoogle Scholar
  43. González-Wevar C, Nakano T, Cañete J, Poulin E (2011a) Concerted genetic, morphological and ecological diversification in Nacella limpets in the Magellanic Province. Mol Ecol 20:1936–1951PubMedCrossRefGoogle Scholar
  44. González-Wevar C, David B, Poulin E (2011b) Phylogeography and demographic inference in Nacella (Patinigera) concinna (Strebel, 1908) in the western Antarctic Peninsula. Deep-Sea Res II 58:220–229CrossRefGoogle Scholar
  45. González-Wevar C, Díaz A, Gérard K, Cañete J, Poulin E (2012a) Divergence time estimations and contrasting patterns of genetic diversity between Antarctic and southern South America benthic invertebrates. Rev Chil Hist Nat 85:445–456CrossRefGoogle Scholar
  46. González-Wevar C, Hüne M, Cañete J, Mansilla A, Nakano T, Poulin E (2012b) Towards a model of postglacial biogeography in shallow marine species along the Patagonian Province: lessons from the limpet Nacella magellanica (Gmelin, 1791). BMC Evol Biol 12:139PubMedCrossRefPubMedCentralGoogle Scholar
  47. González-Wevar C, Saucède T, Morley SA, Chown S, Poulin E (2013) Extinction and recolonization of maritime Antarctica in the limpet Nacella concinna (Strebel, 1908) during the last glacial cycle: toward a model of Quaternary biogeography in shallow Antarctic invertebrates. Mol Ecol 22:5221–5236PubMedCrossRefGoogle Scholar
  48. Greve M, Gremmen NJM, Gaston KJ, Chown SL (2005) Nestedness of Southern Ocean island biotas: ecological perspectives on a biogeographical conundrum. J Biogeogr 32:155–168CrossRefGoogle Scholar
  49. Griffiths H, Barnes D, Linse K (2009) Towards a generalized biogeography of the Southern Ocean benthos. J Biogeogr 36:162–177CrossRefGoogle Scholar
  50. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  51. Hall K (1982) Rapid deglaciation as an initiator of volcanic activity: an hypothesis. Palaegeogr Palaeocl 29:243–259CrossRefGoogle Scholar
  52. Hall B (2009) Holocene glacial history of Antarctica and the sub-Antarctic islands. Quat Sci Rev 28:2213–2230CrossRefGoogle Scholar
  53. Hall K, Meiklejohn I (2011) Glaciation in Southern Africa and in the sub-Antarctic. In: Ehlers J, Gibbard PL, Hughes PD (eds) Quaternary glaciations: extent and chronology: a closer look 15, pp 1081–1087Google Scholar
  54. Hall K, Meiklejohn I, Bumby A (2011) Marion Island volcanism and glaciation. Antarct Sci 23:155–163CrossRefGoogle Scholar
  55. Ho S, Phillips M, Cooper A, Drummond A (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568PubMedCrossRefGoogle Scholar
  56. Ho S, Shapiro B, Phillips M, Cooper A, Drummond A (2007) Evidence for time dependency of molecular rates. Syst Biol 56:515–522PubMedCrossRefGoogle Scholar
  57. Ho S, Lanfear R, Bromham L, Phillips M, Soubrier J, Rodrigo A, Cooper A (2011) Time-dependent rates of molecular evolution. Mol Ecol 20:3087–3101PubMedCrossRefGoogle Scholar
  58. Hudson R, Coyne J (2002) Mathematical consequences of the genealogical species concept. Evolution 56:1557–1565PubMedCrossRefGoogle Scholar
  59. Huelsenbeck J, Ronquist F (2001) MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17:754–755PubMedCrossRefGoogle Scholar
  60. Hunter R, Halanych K (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the Drake Passage in the Southern Ocean. J Hered 99:137–148PubMedCrossRefGoogle Scholar
  61. Janosik A, Mahon A, Halanych K (2010) Evolutionary history of Southern Ocean Odontaster sea star species (Odontasteridae: Asteroidea). Polar Biol 34:575–586CrossRefGoogle Scholar
  62. Jonkers H, Kelley S (1998) A reassessment of the age of the Cockburn Island Formation, northern Antarctic Peninsula, and its palaeoclimatic implications. J Geol Soc 155:737–740CrossRefGoogle Scholar
  63. Kemp A, Grigorov I, Pearce R, Naveira Garabato A (2010) Migration of the Antarctic Polar Front through the mid-Pleistocene transition: evidence and climatic implications. Quat Sci Rev 29:1993–2009CrossRefGoogle Scholar
  64. Koufopanou V, Reid D, Ridgway S, Thomas R (1999) A molecular phylogeny of Patellid limpet (Gastropoda: Patellidae) and its implications for their antitropical distribution. Mol Phylogenet Evol 11:138–156PubMedCrossRefGoogle Scholar
  65. Krabbe K, Leese F, Mayer C, Tollrian R, Held C (2009) Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biol 33:281–292CrossRefGoogle Scholar
  66. Lawver L, Gahagan L (2003) Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeogr Palaeocl 198:1–27CrossRefGoogle Scholar
  67. Lear C, Elderfield H, Wilson P (2000) Cenozoic deep-sea temperatures and global ice volumes from Mg/Ca in Benthic Foraminiferal Calcite. Science 287:269–272PubMedCrossRefGoogle Scholar
  68. Lewis A, Marchant D, Ashworth A, Hedenäs L, Hemming S, Johnsong J, Leng M, Newton A, Raine J, Willenbring J, Williams W, Wolfe A (2008) Mid-Miocene cooling and the extinction of tundra in continental Antarctica. Proc Natl Acad Sci USA 105:1–5CrossRefGoogle Scholar
  69. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  70. Lindberg DR, Hickman CS (1986) A new anomalous giant limpet from the Oregon Eocene (Mollusca: Patellida). J Paleontol 60:661–668Google Scholar
  71. Linse K, Griffiths H, Barnes D, Clarke A (2006) Biodiversity and biogeography of Antarctic and sub-Antarctic mollusca. Deep-Sea Res II 53:985–1008CrossRefGoogle Scholar
  72. Littlewood D, Curini-Galletti M, Herniou E (2000) The Interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466PubMedCrossRefGoogle Scholar
  73. Macaya E, Zuccarello G (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol-Prog Ser 420:103–112CrossRefGoogle Scholar
  74. Mackensen A (2004) Changing Southern Ocean palaeocirculation and effects on global climate. Antarct Sci 16:369–386CrossRefGoogle Scholar
  75. Mortimer E, Jansen van Vuuren B, Lee JE, Marshall DJ, Convey P, Chown SL (2011) Mite dispersal among the Southern Ocean Islands and Antarctica before the last glacial maximum. Proc R Soc B 278:1247–1255PubMedCrossRefPubMedCentralGoogle Scholar
  76. Nakano T, Ozawa T (2005) Systematic revision of Patelloida pygmaea (Dunker, 1860) (Gastropoda: Lottiidae), with a description of a new species. J Mollus Stud 71:357–370CrossRefGoogle Scholar
  77. Nakano T, Ozawa T (2007) Worldwide phylogeography of limpets of the order Patellogastropoda: molecular, morphological and palaeontological evidence. J Mollus Stud 73:79–99CrossRefGoogle Scholar
  78. Nikula R, Fraser C, Spencer H, Waters J (2010) Circumpolar dispersal by rafting in two subantarctic kelp-dwelling crustaceans. Mar Ecol-Prog Ser 405:221–230CrossRefGoogle Scholar
  79. Page T, Linse K (2002) More evidence of speciation and dispersal across Antarctic Polar Front through molecular systematics of Southern Ocean Limatula (Bivalvia: Limidae). Polar Biol 25:818–826Google Scholar
  80. Pfuhl H, McCave I (2005) Evidence for late Oligocene establishment of the Antarctic circumpolar current. Earth Planet Sc Lett 235:715–728CrossRefGoogle Scholar
  81. Pierrat B, Saucède T, Brayard A, David B (2013) Comparative biogeography of echinoids, bivalves and gastropods from the Southern Ocean. J Biogeogr 40:1374–1385CrossRefGoogle Scholar
  82. Pons O, Petit R (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245PubMedPubMedCentralGoogle Scholar
  83. Poulin E, González-Wevar C, Díaz A, Gérard K, Hüne M (2014) Divergence between Antarctic and South American marine invertebrates: what molecules tell us about Scotia Arc geodynamics and the intensification of the Antarctic circumpolar current. Global Planet Change. doi: 10.1016/j.gloplacha.2014.07.017 Google Scholar
  84. Powell A (1973) The Patellid limpets of the World (Patellidae). Auckland Institute and Museum Auckland, New ZealandGoogle Scholar
  85. Raupach M, Thatje S, Dambach J, Rehm P, Misof B, Leese F (2010) Genetic homogeneity and circum-Antarctic distribution of two benthic shrimp species of the Southern Ocean, Chorismus antarcticus and Nematocarcinus lanceopes. Mar Biol 157:1783–1797CrossRefGoogle Scholar
  86. Rintoul S (2011) The southern ocean in the earth system. In: Berkman P, Lang M, Walton D, Young O (eds) Science diplomacy: Antarctica, science and the governance of international spaces. Smithsonian Institution Scholarly Press, Washington, pp 1–13Google Scholar
  87. Rintoul S, Hughes C, Olbers D (2001) The Antarctic circumpolar current system. In: Siedler G, Church J, Gould J (eds) Ocean circulation and climate. Academic Press, pp 1–32Google Scholar
  88. Roe A, Sperling F (2007) Patterns of evolution of mitochondrial cytochrome c oxidase I and II DNA and implications for DNA barcoding. Mol Phylogenet Evol 44:325–345PubMedCrossRefGoogle Scholar
  89. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574Google Scholar
  90. Scher H, Martin E (2006) Timing and climatic consequences of the opening of Drake Passage. Science 312:428–430Google Scholar
  91. Shaw P, Arkhipkin A, Al-Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13:3293–3303PubMedCrossRefGoogle Scholar
  92. Shevenell A, Kennett J, Lea D (2004) Middle Miocene Southern Ocean cooling and Antarctic cryosphere expansion. Science 305:1766–1770PubMedCrossRefGoogle Scholar
  93. Slatkin M, Hudson R (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562PubMedPubMedCentralGoogle Scholar
  94. Stankovic A, Spalik K, Kamler E, Borsuk P, Weglenski P (2002) Recent origin of sub-Antarctic notothenioids. Polar Biol 25:203–205Google Scholar
  95. Strugnell J, Watts P, Smith P, Allcock A (2012) Persistent genetic signatures of historic climatic events in an Antarctic octopus. Mol Ecol 21:2775–2787PubMedCrossRefGoogle Scholar
  96. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (* and Other Methods), Version 4. Sinauer Associations, Sunderland, MAGoogle Scholar
  97. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  98. Terauds A, Chown S, Morgan F, Peat H, Watts D, Keys H, Convey P, Bergstrom DM (2012) Conservation biogeography of the Antarctic. Divers Distrib 18:726–741CrossRefGoogle Scholar
  99. Thatje S, Arntz W (2004) Antarctic reptant decapods: more than a myth? Polar Biol 27:195–201CrossRefGoogle Scholar
  100. Thatje S, Fuentes V (2003) First record of anomuran and brachyuran larvae (Crustacea: Decapoda) from Antarctic waters. Polar Biol 26:279–282Google Scholar
  101. Thatje S, Anger K, Calcagno J, Lovrich G, Pörtner H, Arntz W (2005) Challenging the cold: crabs reconquer the Antarctic. Ecology 86:619–625CrossRefGoogle Scholar
  102. Thornhill D, Mahon A, Norenburg J, Halanych K (2008) Open-ocean barriers to dispersal: a test case with the Antarctic Polar Front and the ribbon worm Parborlasia corrugatus (Nemertea: Lineidae). Mol Ecol 17:5104–5117PubMedCrossRefGoogle Scholar
  103. Valdovinos C, Rüth M (2005) Nacellidae limpets of southern South America: taxonomy and distribution. Rev Chil Hist Nat 78:497–517CrossRefGoogle Scholar
  104. Verducci M, Foresi L, Scott G, Sprovieri M, Lirer F, Pelosi N (2009) The Middle Miocene climatic transition in the Southern Ocean: evidence of paleoclimatic and hydrographic changes at Kerguelen plateau from planktonic foraminifers and stable isotopes. Palaeogeogr Palaeocl 280:371–386CrossRefGoogle Scholar
  105. Williams S, Reid D, Littlewood D (2003) A molecular phylogeny of the Littorininae (Gastropoda: Littorinidae): unequal evolutionary rates, morphological parallelism, and biogeography of the Southern Ocean. Mol Phylogenet Evol 28:60–86PubMedCrossRefGoogle Scholar
  106. Wilson N, Schrödl M, Halanych K (2009) Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia). Mol Ecol 18:965–984PubMedCrossRefGoogle Scholar
  107. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Claudio A. González-Wevar
    • 1
    • 2
    Email author
  • Steven L. Chown
    • 3
  • Simon Morley
    • 4
  • Nestor Coria
    • 5
  • Thomas Saucéde
    • 6
  • Elie Poulin
    • 2
  1. 1.GAIA-AntárticaUniversidad de MagallanesPunta ArenasChile
  2. 2.Laboratorio de Ecología Molecular (LEM)Instituto de Ecología y Biodiversidad (IEB)SantiagoChile
  3. 3.School of Biological SciencesMonash UniversityMelbourneAustralia
  4. 4.British Antarctic SurveyCambridgeUK
  5. 5.Departamento de Aves MarinasInstituto Antártico ArgentinoBuenos AiresArgentina
  6. 6.Biogéosciences, UMR CNRS 6282Université de BourgogneDijonFrance

Personalised recommendations