Polar Biology

, Volume 36, Issue 6, pp 871–883 | Cite as

Genetic variability and differentiation among polymorphic populations of the genus Synoicum (Tunicata, Ascidiacea) from the South Shetland Islands

  • M. Paula Wiernes
  • Ricardo Sahade
  • Marcos Tatián
  • Marina B. Chiappero
Original Paper

Abstract

In Antarctica, ascidians are among the most conspicuous and abundant organisms in benthic ecosystems and many species present wide distribution patterns. Two similar forms of ascidians of the colonial genus Synoicum were sampled along the South Shetland Islands, one greenish-yellow with elongated colony stalks and the other yellow-orange with shorter stalks and more rounded colony bodies. The taxonomic analyses indicated that the greenish-yellow form corresponded to the description of the species S. ostentor and the yellow-orange form to that of S. adareanum. However, molecular analyses using the cytochrome oxidase I gene did not detect clear differences between both forms. The frequency and geographic distribution of haplotypes indicate that some degree of gene flow may be occurring, strongly suggesting that both morphotypes did not achieve a complete reproductive isolation yet, that they can still interbreed and should therefore be considered as a single species. Surprisingly, these results are not in line with recent studies of Antarctic fauna using a similar approach, which revealed several cases of morphologically indistinguishable but genetically distinct species.

Keywords

Synoicum COI Morphotypes Genetic differentiation 

Supplementary material

300_2013_1312_MOESM1_ESM.tif (7.3 mb)
Supplementary material 1 (TIFF 7508 kb)
300_2013_1312_MOESM2_ESM.doc (68 kb)
Supplementary material 2 (DOC 67 kb)
300_2013_1312_MOESM3_ESM.tif (422 kb)
Supplementary material 3 (TIFF 422 kb)
300_2013_1312_MOESM4_ESM.tif (6.2 mb)
Supplementary material 4 (TIFF 6312 kb)
300_2013_1312_MOESM5_ESM.doc (35 kb)
Supplementary material 5 (DOC 35 kb)

References

  1. Allcock AL, Strugnell JM (2012) Southern Ocean diversity: new paradigms from molecular ecology. Trends Ecol Evol 27:520–528PubMedCrossRefGoogle Scholar
  2. Allcock AL, Barratt I, Eléaume M, Linse K, Norman MD, Smith PJ, Steinke D, Stevens DW, Strugnell JM (2011) Cryptic speciation and the circumpolarity debate: a case study on endemic Southern Ocean octopuses using the COI barcode of life. Deep Sea Res II 58:242–249CrossRefGoogle Scholar
  3. Baird HP, Miller KJ, Stark JS (2011) Evidence of hidden biodiversity, ongoing speciation and diverse patterns of genetic structure in giant Antarctic amphipods. Mol Ecol 20:3439–3454PubMedCrossRefGoogle Scholar
  4. Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedCrossRefGoogle Scholar
  5. Barnes DKA, Hodgson DA, Convey P, Allen CS, Clarke A (2006) Incursion and excursion of Antarctic biota: past, present and future. Global Ecol Biogeogr 15:121–142CrossRefGoogle Scholar
  6. Bernardi G, Goswami U (1997) Molecular evidence for cryptic species among the Antarctic fish Trematomus bernacchii and Trematomus hansoni. Antarct Sci 9:381–385CrossRefGoogle Scholar
  7. Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155PubMedCrossRefGoogle Scholar
  8. Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Single-locus and multilocus DNA fingerprinting. In: Hoelzel AR (ed) Molecular genetic analysis of populations: a practical approach. Oxford University Press, Oxford, pp 225–269Google Scholar
  9. Clarke A (1996) The distribution of Antarctic marine benthic communities. In: Hofmann EE, Ross RM, Quetin LB (eds) Foundations for ecological research west of the Antarctic Peninsula. Antarct Res Ser, AGU, Washington, DC, pp 219–230CrossRefGoogle Scholar
  10. Clarke A, Crame JA (1989) The origin of the southern ocean marine fauna. In: Crame JA (ed) Origins and evolution of the Antarctic Biota. The Geological Society, London, pp 253–268Google Scholar
  11. Clarke A, Johnston NM (2003) Antarctic marine benthic diversity. Oceanogr Mar Biol 41:47–114Google Scholar
  12. Clarke A, Barnes DKA, Hodgson DA (2005) How isolated is Antarctica? Trends Ecol Evol 20:1–3PubMedCrossRefGoogle Scholar
  13. Dayton PK (1990) Polar benthos. In: Smith W (ed) Polar oceanography. Academic Press, New York, pp 631–685Google Scholar
  14. Demarchi M, Chiappero MB, Tatián M, Sahade R (2010) Population genetic structure of the Antarctic ascidian Aplidium falklandicum from Scotia Arc and South Shetland Islands. Polar Biol 33:1567–1576CrossRefGoogle Scholar
  15. Diyabalange T, Amsler CD, McClintock JB, Baker BJ (2006) Palmerolide A, a Cytotoxic Macrolide from the Antarctic Tunicate Synoicum adareanum. J Am Chem Soc 128:5630–5631CrossRefGoogle Scholar
  16. Dowdeswell JA, Bamber JL (2007) Keel depths of modern Antarctic icebergs and implications for sea-floor scouring in the geological record. Mar Geol 243:120–131CrossRefGoogle Scholar
  17. Excoffier L, Schneider S (1999) Why hunter-gatherer populations do not show signs of Pleistocene demographic expansions. Proc Natl Acad Sci USA 96:10597–10602PubMedCrossRefGoogle Scholar
  18. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  19. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50Google Scholar
  20. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  21. 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 Biotechnol 3:294–299PubMedGoogle Scholar
  22. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  23. Gili JM, Arntz WE, Palanques A, Orejas C, Clarke A, Dayton PK, Isla E, Teixidó N, Rossi S, López-González PJ (2006) A unique assemblage of epibenthic sessile suspension feeders with archaic features in the high-Antarctic. Deep-Sea Res II 53:1029–1052CrossRefGoogle Scholar
  24. Goldstien SJ, Schiel DR, Gemmell NJ (2010) Regional connectivity and coastal expansion: differentiating pre-border and post-border vectors for the invasive tunicate Styela clava. Mol Ecol 19:874–885PubMedCrossRefGoogle Scholar
  25. Goodall-Copestake WP, Tarling GA, Murphy EJ (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56PubMedCrossRefGoogle Scholar
  26. Grosberg RK, Cunningham CW (2001) Genetic structure in the sea from populations to communities. In: Bertness MD, Hay ME, Gaines SD (eds) Marine community ecology. Sinauer, Sunderland, MA, pp 61–84Google Scholar
  27. Gutt J (2000) Some “driving forces” structuring communities of the sublittoral Antarctic macrobenthos. Antarct Sci 12:297–313CrossRefGoogle Scholar
  28. Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600PubMedGoogle Scholar
  29. Haydar D, Hoarau G, Olsen JL, Stam WT, Wolff WJ (2011) Introduced or glacial relict? Phylogeography of the cryptogenic tunicate Molgula manhattensis (Ascidiacea, Pleurogona). Divers Distrib 17:68–80CrossRefGoogle Scholar
  30. Held C (2003) Molecular evidence for cryptic speciation within the widespread Antarctic crustacean Ceratoserolis trilobitoides (Crustacea, Isopoda). In: Huiskes AH, Gieskes WW, Rozema J, Schorno RM, van der Vies SM, Wolff WJ (eds) Antarctic biology in a global context. Backhuys, Leiden, pp 135–139Google Scholar
  31. Herdman WA (1902) Tunicata. In: Report on the collections of natural history made in the Antarctic regions during the voyage of the “Southern Cross”, London, pp 190–200Google Scholar
  32. Hirose E, Oka AT, Hirose M (2009) Two new species of photosymbiotic ascidians of the genus Diplosoma from the Ryukyu Archipelago, with partial sequences of the COI gene. Zool Sci 26:362–368PubMedCrossRefGoogle Scholar
  33. Hirose M, Nozawa Y, Hirose E (2010) Genetic isolation among Morphotypes in the Photosymbiotic Didemnid Didemnum molle (Ascidiacea, Tunicata) from the Ryukyus and Taiwan. Zool Sci 27:959–964PubMedCrossRefGoogle Scholar
  34. Hunter RL, Halanych KM (2008) Evaluating connectivity in the brooding brittle star Astrotoma agassizii across the Drake Passage in the Southern Ocean. J Hered 99:137–148PubMedCrossRefGoogle Scholar
  35. Jiang X, Liu B, Lebreton S, De Brabander JK (2007) Total synthesis and structure revision of the marine metabolite Palmerolide A. J Am Chem Soc 129:6386–6387PubMedCrossRefGoogle Scholar
  36. Koplovitz G, McClintock JB, Amsler CD, Baker BJ (2011) A comprehensive evaluation of the potential chemical defenses of Antarctic ascidians against sympatric fouling microorganisms. Mar Biol 158:2661–2671CrossRefGoogle Scholar
  37. Kott P (1969) Antarctic Ascidiacea. Antarctic Res Ser 13:1–239Google Scholar
  38. Lawver LA, Gahagan LM, Dalziel IWD (2011) A different look at gateways: Drake Passage and Australia/Antarctica. In: Anderson JB, Wellner JS (eds) Tectonic, climatic, and cryospheric evolution of the Antarctic Peninsula. AGU, Washington, DC, pp 5–33Google Scholar
  39. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  40. López-Legentil S, Turon X (2005) How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Polycitoridae). Zool Scr 34:3–14Google Scholar
  41. López-Legentil S, Turon X (2006) Population genetics, phylogeography and speciation of Cystodytes (Ascidiacea) in the western Mediterranean Sea. Biol J Linn Soc 88:203–214CrossRefGoogle Scholar
  42. López-Legentil S, Dieckmann R, Bontemps-Subielos N, Turon X, Banaigs B (2005) Qualitative variation of alkaloids in color morphs of Cystodytes (Ascidiacea). Biochem Syst Ecol 33:1107–1119CrossRefGoogle Scholar
  43. López-Legentil S, Turon X, Planes S (2006) Genetic structure of the star sea squirt, Botryllus schlosseri, introduced in southern European harbours. Mol Ecol 15:3957–3967PubMedCrossRefGoogle Scholar
  44. Lynch M, Crease TJ (1990) The analysis of population survey data on DNA sequence variation. Mol Biol Evol 7:377–394PubMedGoogle Scholar
  45. Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587PubMedCrossRefGoogle Scholar
  46. McCarthy C (1998) Chromas ver. 1.45. School of Health Science, Griffith University, Queensland, Australia. http://www.technelysium.com.au/chromas.html. Accessed 14 Dec 2012
  47. Millar RH (1960) Ascidiacea. Discov Rep 30:1–160Google Scholar
  48. Monniot C, Monniot F (1983) Ascidies antarctiques et sub-antarctiques: morphologie et biogéographie. Mem Mus Nat Hist Nat Nouv Ser A 125:1–168Google Scholar
  49. Monniot F, Dettai A, Eleaume M, Cruaud C, Ameziane N (2011) Antarctic Ascidians (Tunicata) of the French-Australian survey CEAMARC in Terre Adélie. Zootaxa 2817:1–54Google Scholar
  50. Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New YorkGoogle Scholar
  51. Nicolaou KC, Guduru R, Sun Y-P, Banerji B, Chen DY-K (2007) Total synthesis of the originally proposed and revised structures of Palmerolide A. Angew Chem Int Ed 46:5896–5900CrossRefGoogle Scholar
  52. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  53. Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572CrossRefGoogle Scholar
  54. Pérez-Portela R, Turon X (2008) Phylogenetic relationships of the Clavelinidae and Pycnoclavellidae (Ascidiacea) inferred from mtDNA data. Invertebr Biol 127:108–120CrossRefGoogle Scholar
  55. Pérez-Portela R, Duran S, Palacín C, Turon X (2007) The genus Pycnoclavella (Ascidiacea) in the Atlanto-Mediterranean region: a combined molecular and morphological approach. Invertebr Syst 21:187–205CrossRefGoogle Scholar
  56. Pineda MC, López-Legentil S, Turon X (2011) The Whereabouts of an Ancient Wanderer: global Phylogeography of the Solitary Ascidian Styela plicata. PlosONE 6:e25495Google Scholar
  57. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  58. Raupach MJ, Wägele JW (2006) Distinguishing cryptic species in Antarctic Asellota (Crustacea: Isopoda)—a preliminary study of mitochondrial DNA in Acanthaspidia drygalskii. Antarct Sci 18:191–198CrossRefGoogle Scholar
  59. Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86PubMedCrossRefGoogle Scholar
  60. Riesenfeld CS, Murray AE, Baker BJ (2008) Characterization of the microbial community and Polyketide biosynthetic potential in the Palmerolide-producing tunicate Synoicum adareanum. J Nat Prod 71:1812–1818PubMedCrossRefGoogle Scholar
  61. Rogers AD (2007) Evolution and biodiversity of Antarctic organisms: a molecular perspective. Phil Trans R Soc B 362:2191–2214PubMedCrossRefGoogle Scholar
  62. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  63. Ronquist F, Huelsenbeck J (2003) Mrbayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  64. Sabbadin A (1982) Formal genetics of ascidians. Am Zool 22:765–773Google Scholar
  65. Savidge DK, Amft JA (2009) Circulation on the West Antarctic Peninsula derived from 6 years of shipboard ADCP transects. Deep-Sea Res I 56:1633–1655CrossRefGoogle Scholar
  66. Stoner DS, Weissman IL (1996) Somatic and germ cell parasitism in a colonial ascidian: possible role for a highly polymorphic allorecognition system. Evolution 93:15254–15259Google Scholar
  67. Svane I, Young CM (1989) The ecology and behaviour of ascidian larvae. Oceanogr Mar Biol Annu Rev 27:45–90Google Scholar
  68. Swofford DL (2001) PAUP: phylogenetic analysis using parsimony (and other methods) Version 4. Sinauer Associates, Sunderland, MAGoogle Scholar
  69. 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 130:455–462Google Scholar
  70. Tarjuelo I, Posada D, Crandall KA, Pascual M, Turon X (2004) Phylogeography and speciation of colour morphs in the colonial ascidian Pseudodistoma crucigaster. Mol Ecol 13:3125–3136PubMedCrossRefGoogle Scholar
  71. Thatje S (2012) Effects of capability for dispersal on the evolution of diversity in antarctic benthos. Integr Comp Biol 52:470–482PubMedCrossRefGoogle Scholar
  72. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 24:4876–4882CrossRefGoogle Scholar
  73. Turon X, Tarjuelo I, Duran S, Pascual M (2003) Characterising invasion processes with genetic data: an Atlantic clade of Clavelina lepadiformis (Ascidiacea) introduced into Mediterranean harbours. Hydrobiologia 503:29–35CrossRefGoogle Scholar
  74. Van Name WG (1945) The North and South American ascidians. Bull Am Mus Nat Hist 84:1–476Google Scholar
  75. Wares JP, Gaines SD, Cunningham CW (2001) A comparative study of asymmetric migration events across a marine biogeographic boundary. Evolution 55:295–306PubMedGoogle Scholar
  76. Wright S (1969) Evolution and the genetics of populations. The theory of gene frequencies, vol 2. University of Chicago Press, Chicago, ILGoogle Scholar
  77. Yund PO, O’Neil PG (2000) Microgeographic genetic differentiation in a colonial ascidian (Botryllus schlosseri) population. Mar Biol 137:583–588CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • M. Paula Wiernes
    • 1
    • 2
  • Ricardo Sahade
    • 1
    • 2
  • Marcos Tatián
    • 1
    • 2
  • Marina B. Chiappero
    • 1
    • 3
  1. 1.Instituto de Diversidad y Ecología Animal (CONICET/UNC)CórdobaArgentina
  2. 2.Ecología Marina, Facultad de Ciencias Exactas, Físicas y NaturalesUniversidad Nacional de CórdobaCórdobaArgentina
  3. 3.Genética de Poblaciones y Evolución, Facultad de Ciencias Exactas, Físicas y NaturalesUniversidad Nacional de CórdobaCórdobaArgentina

Personalised recommendations