Marine Biology

, Volume 158, Issue 6, pp 1259–1269 | Cite as

Sympatry and allopatry in the deeply divergent mitochondrial DNA clades of the estuarine pulmonate gastropod genus Phallomedusa (Mollusca, Gastropoda)

  • Rosemary E. Golding
  • Donald J. Colgan
  • Guy Nelmes
  • Tina Reutelshöfer
Original Paper

Abstract

DNA sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene were collected from estuarine snails in the genus Phallomedusa to examine the effects of estuarine isolation on population structure and gene flow. Three clades were recovered, one corresponding to Phallomedusa austrina and two others with the morphology of Phallomedusa solida. The haplotype diversity in all three clades indicated recent population expansion. Phallomedusa austrina was restricted to the west of a previous land bridge in the Bass Strait between mainland Australia and Tasmania, and P. solida to its east and to northern Tasmania. Phylogeographic analysis of P. austrina and P. solida shows strong geographic separation of species, but no local genetic structure indicative of regional or estuarine isolation. The clades of P. solida exhibit substantial genetic divergence and were sympatric across their entire distribution in eastern Tasmania and mainland Australia. Such a situation, which has not previously been observed in phylogeographic studies of southeast Australia, suggests that P. solida has had a complex refugial history during periods of environmental challenge.

References

  1. Ayre DJ, Minchinton TE, Perrin C (2009) Does life history predict past and current connectivity for rocky intertidal invertebrates across a marine biogeographic barrier? Mol Ecol 18:1887–1903CrossRefGoogle Scholar
  2. Bilton DT, Paula J, Bishop JDD (2002) Dispersal, genetic differentiation and speciation in estuarine organisms. Estuar Coast Shelf Sci 55:937–952CrossRefGoogle Scholar
  3. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1660CrossRefGoogle Scholar
  4. Colgan DJ, da Costa P (2009) The mitochondrial DNA haplotypes of snails of the estuarine hydrobiid genus Tatea cross species and geographic boundaries. Mar Freshw Res 60:861–872Google Scholar
  5. Colgan DJ, Schreiter S (2011) Extrinsic and intrinsic influences on the phylogeography of the Austrocochlea species group. J Exp Mar Biol Ecol 397:44–51Google Scholar
  6. Colgan DJ, Ponder WF, Beacham E, Macaranas JM (2003) Molecular phylogenetic studies of Gastropoda based on six gene segments representing coding or non-coding and mitochondrial or nuclear DNA. Moll Res 23:123–148CrossRefGoogle Scholar
  7. Collin R (1997) Hydrophobic larval shells: another character for higher level systematics of gastropods. J Moll Stud 63:425–430CrossRefGoogle Scholar
  8. Dawson MN (2005) Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south-east Australia. J Biogeogr 32:515–533CrossRefGoogle Scholar
  9. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50Google Scholar
  10. 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. Molec Mar Biol Biotech 3:294–299Google Scholar
  11. Fraser CI, Spencer HG, Waters JM (2009) Glacial oceanographic contrasts explain phylogeography of Australian bull kelp. Molec Ecol 18:2287–2296CrossRefGoogle Scholar
  12. Fu X-Y (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925Google Scholar
  13. Golding RE, Ponder WF, Byrne M (2007) Taxonomy and anatomy of Amphiboloidea (Gastropoda: Heterobranchia: Archaeopulmonata). Zootaxa 1476:1–50Google Scholar
  14. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98Google Scholar
  15. Huelsenbeck JP, Ronquist F (2001) MrBAYES; Bayesian inference for phylogeny. Bioinformatics 17:754–755CrossRefGoogle Scholar
  16. Kuroda T (1928) Two families new to Japan. Venus 1:11Google Scholar
  17. Lambeck K, Chappell J (2001) Sea level change through the last glacial cycle. Science 292:679–686CrossRefGoogle Scholar
  18. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  19. Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72 http://mesquiteproject.org
  20. Martens E, von in Schacko G (1878) Die Zungenbewaffnung der Gattung Amphibola. Jahrbüch. d. Deutsch. Malak Ges 5:1–9Google Scholar
  21. Martyn T (1786) Universal conchologist. LondonGoogle Scholar
  22. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala UniversityGoogle Scholar
  23. O’Loughlin PM, Waters JM, Roy MS (2003) A molecular and morphological review of the asterinid, Patiriella gunnii (Gray) (Echinodermata, Asteroidea). Mem Mus Vic 60:181–195Google Scholar
  24. Parmakelis A, Pfenninger M, Spanos L, Papagiannakis G, Louis C, Mylonas M, O’Foighil D (2005) Inference of a radiation in Mastus (Gastropoda, Pulmonata, Enidae) on the island of Crete. Evolution 59:991–1005CrossRefGoogle Scholar
  25. Pfenninger M, Staubach S, Albrecht C, Streit B, Schwenk K (2003) Ecological, morphological differentiation among cryptic evolutionary lineages in freshwater limpets of the nominal form-group Ancylus fluviatilis (O.F. Müller, 1774). Mol Ecol 12:2731–2745CrossRefGoogle Scholar
  26. Pilkington MC, Pilkington JB (1982) The planktonic veliger of Ammphibola crenata (Gmelin). J Moll Stud 48:24–29Google Scholar
  27. Posada D, Buckley TR (2004) Model selection and model averaging in phylogenetics: advantages of Akaike information criterian and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808CrossRefGoogle Scholar
  28. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100Google Scholar
  29. Roach AC (1998) Effects of predation on the size structure of the gastropod Salinator solida (Martens) populations at Towra Point, NSW, Australia. Mar Freshw Res 49:779–784CrossRefGoogle Scholar
  30. Rogers AR, Harpending HC (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569Google Scholar
  31. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  32. Saintalan N, Williams RJ (2001) Mangrove transgression into saltmarsh environments in south-east Australia. Glob Ecol Biogeogr 8:117–124CrossRefGoogle Scholar
  33. Thompson JD, Higgins DG, Gibson TJ (1994) ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acid Res 22:4673–4680CrossRefGoogle Scholar
  34. Waters JM (2008) Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Divers Distrib 14:692–700CrossRefGoogle Scholar
  35. Waters JM, O’Loughlin PM, Roy MS (2004) Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Mol Phyl Evol 32:236–245CrossRefGoogle Scholar
  36. Waters JM, King RM, O’Loughlin PM, Spencer HG (2005) Phylogeographic disjunction in abundant high-dispersal littoral gastropods. Mol Ecol 14:2789–2802CrossRefGoogle Scholar
  37. White LR, McPheron BA, Stauffer JR (1994) Identification of freshwater mussel glochidia on host fishes using restriction fragment length polymorphisms. Mol Ecol 3:183–185CrossRefGoogle Scholar
  38. Xia X, Xie Z (2001) Data analysis in molecular biology and evolution. J Hered 92:371–373CrossRefGoogle Scholar
  39. Xia X, Xie Z, Salemi M, Chen L, Wang Y (2003) An index of substitution saturation and its application. Mol Phyl Evol 26:1–7CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Rosemary E. Golding
    • 2
    • 1
  • Donald J. Colgan
    • 1
  • Guy Nelmes
    • 1
  • Tina Reutelshöfer
    • 1
  1. 1.Australian MuseumSydneyAustralia
  2. 2.Field Museum of Natural HistoryChicagoUSA

Personalised recommendations