Polar Biology

, Volume 34, Issue 4, pp 575–586 | Cite as

Evolutionary history of Southern Ocean Odontaster sea star species (Odontasteridae; Asteroidea)

  • Alexis M. Janosik
  • Andrew R. Mahon
  • Kenneth M. Halanych
Original Paper

Abstract

We investigated the recent evolutionary history of demersal sea stars in the genus Odontaster throughout the Western Antarctic waters and on the South American shelf. The mitochondrial 16S ribosomal and cytochrome c oxidase subunit I (COI) genes were sequenced from adult and larval specimens. TCS parsimony network analysis and Bayesian inference were used to examine evolutionary history. Hierarchical AMOVA and mitochondrial DNA diversity statistics were also computed. Additionally, morphological characters were used. In assessing O. validus, we discovered morphological and range descriptions of Odontaster species to be inaccurate and include other Odontaster species in the Southern Ocean. We found O. meridionalis on both sides of the Antarctic circumpolar current (ACC) and Antarctic polar front (APF), whereas O. validus and O. penicillatus do not appear to have permeated these oceanographic features. Additionally, we discovered previously unrecognized species of Odontaster. Subsequent examination revealed diagnostic morphological differences in the number of spinelets on the abactinal and actinal plates. Mitochondrial characterization of Odontaster species suggests their recent history has been influenced by the APF and ACC in different ways. With the exception of O. meridionalis, Odontaster species are restricted to either side of the Drake Passage. O. validus shows genetic connectivity throughout sampled Antarctic waters.

Keywords

16S rDNA COI mtDNA Antarctic circumpolar current Antarctic polar front Odontaster Phylogeography 

Supplementary material

300_2010_916_MOESM1_ESM.doc (628 kb)
Supplementary material 1 (DOC 628 kb)

References

  1. Arntz W, Gutt J, Klages M (1997) Antarctic marine biodiversity. In: Battaglia B, Valencia J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 3–14Google Scholar
  2. Bargelloni L, Zane L, Derome N, Lecointre G, Patarnello T (2000) Molecular zoogeography of Antarctic euphausiids and notothenioids: from species phylogenies to intraspecific patterns of genetic variation. Ant Sci 12:259–268CrossRefGoogle Scholar
  3. Blake DB (1987) Classification and phylogeny of post-Palaeozoic sea stars (Asteroidea: Echinodermata). J Nat Hist 21:481–528CrossRefGoogle Scholar
  4. Clark AM (1962) B.A.N.Z. Asteroidea. Brit Mus Antarct Exped Rep Ser B 9:1–143Google Scholar
  5. Clarke A (1988) Seasonality in the Antarctic marine environment. Comp Bio Phys B 90:461–473CrossRefGoogle Scholar
  6. Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3CrossRefPubMedGoogle Scholar
  7. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefPubMedGoogle Scholar
  8. Crame JA (1999) An evolutionary perspective on marine faunal connections between southernmost South America and Antarctica. Sci Mar 63:1–14CrossRefGoogle Scholar
  9. Dayton PK, Robilliar GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 44:105–128CrossRefGoogle Scholar
  10. Dell RK (1972) Antarctic benthos. Adv Mar Biol 10:1–216CrossRefGoogle Scholar
  11. Edmands S, Moberg PE, Burton RS (1996) Allozyme and mitochondrial DNA evidence of population subdivision in the purple sea urchin Strongylocentrotus purpuratus. Mar Biol 126:443–450CrossRefGoogle Scholar
  12. Ekman S (1953) Zoogeography of the sea. Sidgwick and Jackson, LondonGoogle Scholar
  13. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinfor 1:47–50Google Scholar
  14. Fisher WK (1940) Asteroidea. Discov Rep 20:69–306Google Scholar
  15. Foltz DW (1997) Hybridization frequency is negatively correlated with divergence time of mitochondrial DNA haplotypes in a sea star (Leptasterias spp.) species complex. Evolution 51:283–288CrossRefGoogle Scholar
  16. Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  17. 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 silicieous microfossil records. Quat Sci Rev 24:869–896CrossRefGoogle Scholar
  18. Hall TA (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid S 41:95–98Google Scholar
  19. Hart MW, Byrne M, Smith MJ (1997) Molecular phylogenetic analysis of life history evolution in Asterinid starfish. Evolution 51:1848–1861CrossRefGoogle Scholar
  20. Hayes KA, Karl SA (2009) Phylogenetic relationships of crown conchs (Melongena spp.): the corona complex simplified. J Biogeogr 36:28–38CrossRefGoogle Scholar
  21. Hedgepeth JW (1969) Introduction to Antarctic zoogeography. Antarct Map Folio Ser 11:l–44Google Scholar
  22. Held C (2000) Phylogeny and biogeography of serolid isopods (Crustacea, Isopoda, Serolidae) and the use of ribosomal expansion segments in molecular systematics. Mol Phylogenet Evol 15:165–178CrossRefPubMedGoogle Scholar
  23. Held C, Leese F (2007) The utility of fast evolving molecular markers for studying speciation in Antarctic benthos. Polar Biol 30:513–521CrossRefGoogle Scholar
  24. Helmuth B, Veit R, Holderton R (1994) Dispersal of benthic invertebrates in the Scotia Arc by kelp rafting. Antarct J US 29:145–147Google Scholar
  25. Hunter RL, Halanych KM (2008) Evaluating connectivity of the brooding brittle star Astrotoma agassizii across the Drake Passage in the Southern Ocean. J Hered 99:137–148CrossRefPubMedGoogle Scholar
  26. Janosik AM, Halanych KM (2010) Unrecognized Antarctic biodiversity: a case study of the genus Odontaster (Odontasteridae; Asteroidea). Integr Comp Biol 50:981–992Google Scholar
  27. Janosik AM, Mahon AR, Scheltema RA, Halanych KM (2008) Life history of the Antarctic sea star Labidiaster annulatus (Asteroidea: Labidiasteridae) revealed by DNA barcoding. Ant Sci 20:563–564CrossRefGoogle Scholar
  28. Krabbe K, Leese F, Mayer C, Tollrian R, Held C (2010) Cryptic mitochondrial lineages in the widespread pycnogonid Colossendeis megalonyx Hoek, 1881 from Antarctic and Subantarctic waters. Polar Biol 33:281–292CrossRefGoogle Scholar
  29. 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 53:806–817CrossRefGoogle Scholar
  30. Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975CrossRefPubMedGoogle Scholar
  31. Linse K, Cope T, Lorz A-N, Sands C (2007) Is the Scotia Sea a centre of Antarctic marine diversification? Some evidence of cryptic speciation in the circum-Antarctic bivalve Lissarca notocadensis (Arcoidea: Philobryidae). Polar Biol 30:1059–1068CrossRefGoogle Scholar
  32. Mahon AR, Arango CL, Halanych KM (2008) Genetic diversity of Nymphon Arthropoda: Pycnogonida: Nymphonidae) along the Antarctic Peninsula with a focus on Nymphon australe. Mar Biol 155:315–323CrossRefGoogle Scholar
  33. Mahon AR, Thornhill DJ, Norenburg JL, Halanych KM (2009) DNA discovers missing Antarctic nemerteans and exposes a decades-old cold case of asymmetric inventory. Polar Biol 33:193–202CrossRefGoogle Scholar
  34. McCartney MA, Keller G, Lessios HA (2000) Dispersal barriers in tropical oceans and speciation of Atlantic and eastern Pacific Echinometra sea urchins. Mol Ecol 9:391–1400CrossRefGoogle Scholar
  35. McClintock JB, Pearse JS, Bosch I (1988) Population structure and energetics of the shallow-water Antarctic sea star Odontaster validus in contrasting habitats. Mar Biol 99:235–246CrossRefGoogle Scholar
  36. McClintock JB, Angus RA, Ho C, Amsler CD, Baker BJ (2008) A laboratory study of behavioral interactions of the Antarctic keystone sea star Odontaster validus with three sympatric predatory sea stars. Mar Biol 154:1077–1084CrossRefGoogle Scholar
  37. Mileikovsky SA (1971) Types of larval development in marine bottom invertebrates, their distribution and ecological significance: a re-evaluation. Mar Biol 10:193–213CrossRefGoogle Scholar
  38. Moore JK, Abbott MR, Richman JG, Nelson DM (2000) The Southern Ocean at the last glacial maximum: a strong sink for atmospheric carbon dioxide. Global Biogeochem Cy 14:445–475CrossRefGoogle Scholar
  39. Nylander JAA (2004) MRMODELTEST. Version 2. Distributed by the author. Evolutionary Biology Centre, Uppsala University, SwedenGoogle Scholar
  40. Orsi AH, Whitworth T III, Nowlin WD Jr (1995) On the meridional extent and fronts of the Antarctic circumpolar current. Deep-Sea Res I 42:641–673CrossRefGoogle Scholar
  41. Page TJ, Linse K (2002) More evidence of speciation and dispersal across the Antarctic Polar Front through molecular systematics of Southern Ocean Limatula (Bivalvia: Limidae). Polar Biol 25:818–826Google Scholar
  42. Palumbi SR, Martin AP, Romano S, McMillan WO, Stice L, Grabowski G (1991) The simple fool’s guide to PCR. Special publication of the Department of Zoology, University of Hawaii, Honolulu, HawaiiGoogle Scholar
  43. Patarnello T, Bargelloni L, Varotto V, Battaglia B (1996) Krill evolution and the Antarctic ocean currents: evidence of vicariant speciation as inferred by molecular data. Mar Biol 126:1432–1793CrossRefGoogle Scholar
  44. Pearse JS (1965) Reproductive periodicities in several contrasting populations of Odontaster validus Koehler, a common Antarctic asteroid. Ant Res Ser 5:39–85Google Scholar
  45. Pearse JS, Bosch I (1986) Are the feeding larvae of the commonest Antarctic asteroid really demersal? Bull Mar Sci 39:477–484Google Scholar
  46. Pearse JS, Bosch I (1994) Brooding in the Antarctic: Ostergren had it nearly right. In: David B, Guille A, Féral J-P, Roux M (eds) Echinoderms through time. Balkema, Rotterdam, pp 111–120Google Scholar
  47. Pfuhl HA, McCave N (2005) Evidence for late Oligocene establishment of the Antarctic circumpolar current. Earth Planet Sci Lett 235:715–728CrossRefGoogle Scholar
  48. Phillpot HR (1985) Physical geography—climate. In: Bonner WN, Walton DWH (eds) Key environments: Antarctica. Pergamon Press, Oxford, pp 23–38Google Scholar
  49. Raupach MJ, 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
  50. Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefPubMedGoogle Scholar
  51. Rozas J, Sànchesz-DelBarrio JC, Messeguer X, Rozas R (2003) Dnasp, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497CrossRefPubMedGoogle Scholar
  52. Scher HD, Martin EE (2006) Timing and climatic consequences of the opening of Drake Passage. Science 213:428–430CrossRefGoogle Scholar
  53. Smith AB (1997) Echinoderm larvae and phylogeny. Annu Rev Ecol Syst 28:219–241CrossRefGoogle Scholar
  54. Stanwell-Smith D, Peck LS (1998) Temperature and embryonic development in relation to spawning and field occurrence of larvae of three Antarctic Echinoderms. Biol Bull 194:44–52CrossRefGoogle Scholar
  55. Stevens DP, Ivchenko VO (1997) The zonal momentum balance in an eddy-resolving general-circulation model of the Southern Ocean. Q J Roy Meteor Soc 123:929–951CrossRefGoogle Scholar
  56. Strugnell JM, Rogers AD, Prodohl PA, Collins MA, Allcock AL (2008) The thermohaline expressway: the Southern Ocean as a centre of origin for deep-sea Octopuses. Cladistics 24:853–860CrossRefGoogle Scholar
  57. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 125:585–593Google Scholar
  58. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  59. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  60. Thatje S, Hillenbrand CD, Larter R (2005) On the origin of Antarctic marine benthic community structure. Trends Ecol Evol 20:534–540CrossRefPubMedGoogle Scholar
  61. 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 17:5104–5117CrossRefPubMedGoogle Scholar
  62. Tyler PA, Reeves S, Peck LS, Clarke A, Powell D (2003) Seasonal variation in the gametogenic ecology of the Antarctic scallop Adamussium colbecki. Polar Biol 26:727–733CrossRefGoogle Scholar
  63. Wares JP (2009) Natural distributions of mitochondrial sequence diversity support new hull hypotheses. Evolution 64:1136–1142CrossRefPubMedGoogle Scholar
  64. Waters JM, Roy MS (2003) Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J Biogeogr 30:1787–1796CrossRefGoogle Scholar
  65. Whitworth T III, Nowlin WD Jr, Worley SJ (1982) The net transport of the Antarctic circumpolar current through Drake Passage. J Phys Oceanogr 12:960–971CrossRefGoogle Scholar
  66. Wilson NG, Hunter RL, Lockhart SJ, Halanych KM (2007) Multiple lineages and absence of panmixia in the “circumpolar” crinoid Promachocrinus kerguelensis in the Atlantic sector of Antarctica. Mar Biol 152:895–904CrossRefGoogle Scholar
  67. 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 18:965–984CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Alexis M. Janosik
    • 1
  • Andrew R. Mahon
    • 1
    • 2
  • Kenneth M. Halanych
    • 1
  1. 1.Department of Biological SciencesAuburn UniversityAuburnUSA
  2. 2.Centre for Aquatic Conservation, Department of Biological SciencesUniversity of Notre DameNotre DameUSA

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