Marine Biodiversity

, Volume 43, Issue 2, pp 73–85 | Cite as

Possible drivers of biodiversity generation in the Siphonaria of southeastern Australia

Original Article

Abstract

An inter-species approach may reveal insights into biodiversity that are not available by studying single-species phylogeography. Here, we have used this approach to investigate biodiversity generation in Siphonaria, a prominent component of the intertidal fauna of a biogeographically complex region of southeastern Australia. We collected DNA sequences of cytochrome c oxidase (COI) and internal transcribed spacer 2 (ITS-2) from the five species of Siphonaria in the region to study factors such as contemporary hydrology and historical geographic barriers that are known to be important in intra-species phylogeography. Except for the closely-related Siphonaria funiculata and S. tasmanica, the genetic divergences between studied species were deep and could not be related directly to intra-regional factors. In particular, isolation induced by the Bassian Isthmus landbridge at glacial maxima, which is the principal known historical barrier within southeastern Australia, has few detectable effects. Hydrological currents have apparently played only minor roles in determining the contemporary ranges of species or clades within them. Notably, species’ range limits in southern NSW are maintained despite the long-term flow of the East Australian Current. ITS-2 sequences were difficult to interpret phylogeographically as genetic divergence within species was absent for most taxa. All species had considerable numbers of low frequency COI haplotypes between which genetic divergence was shallow. Recently derived disequilibrium was revealed as an important driver of intra-species diversity for this gene. Inter-species comparisons favour demographic expansion over selective sweeps as explanations of the disequilibrium.

Keywords

Siphonariidae Biogeography Bassian Isthmus genetic disequilibrium 

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 18:1887–1903PubMedCrossRefGoogle Scholar
  2. Baird ME, Timko PG, Suthers IM, Middleton JH (2006) Coupled physical-biological modelling study of the East Australian Current with idealised wind forcing. Part I: Biological model intercomparison. J Mar Syst 59:249–270CrossRefGoogle Scholar
  3. Bennett I, Pope E (1953) Intertidal zonation of the exposed rocky shores of Victoria, together with a rearrangement of the biogeographical provinces of temperate Australian shores. Aust J Mar Freshw Res 4:105–159CrossRefGoogle Scholar
  4. Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186PubMedCrossRefGoogle Scholar
  5. Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141PubMedCrossRefGoogle Scholar
  6. Bostock HC, Opdyke BN, Gagan MK, Kiss AE, Fifield LK (2006) Glacial/interglacial changes in the East Australian current. Clim Dynamics 26:645–659CrossRefGoogle Scholar
  7. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedCrossRefGoogle Scholar
  8. Colgan DJ, da Costa P (2009) DNA haplotypes cross species and biogeographic boundaries in estuarine hydrobiid snails of the genus Tatea. Mar Freshw Res 60:861–872CrossRefGoogle Scholar
  9. Colgan DJ, Schreiter S (2011) Extrinsic and intrinsic influences on the phylogeography of the Austrocochlea constricta species group. J Exp Mar Biol Ecol 397:44–51CrossRefGoogle Scholar
  10. Colgan DJ, Middelfart P, Golding R, Criscione F (2009) Monitoring the response of NSW bivalves to climate change. Final report by the Australian Museum to the Environmental Trust for Grant 2008/RD/0071Google Scholar
  11. Crandall ED, Sbrocco EJ, DeBoer TS, Barber PH, Carpenter KE (2012) Expansion dating: calibrating molecular clocks in marine species from expansions onto the Sunda Shelf following the last glacial maximum. Mol Biol Evol 29:707–719PubMedCrossRefGoogle Scholar
  12. Creese RG (1980) Reproductive cycles and fecundities of two species of Siphonaria (Mollusca: Pulmonata) in south-eastern Australia. Aust J Mar Freshw Res 31:37–47CrossRefGoogle Scholar
  13. Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeog 28:723–736CrossRefGoogle Scholar
  14. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. Advance Access published February 25, 2012Google Scholar
  15. 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 Biotech 3:294–299Google Scholar
  16. Fraser CI, Spencer HG, Waters JM (2009) Glacial oceanographic contrasts explain phylogeography of Australian bull kelp. Mol Ecol 18:2287–2296PubMedCrossRefGoogle Scholar
  17. Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570PubMedGoogle Scholar
  18. Golding RE, Colgan DJ, Nelmes G, Reutelshöfer T (2011) Sympatry and allopatry in the deeply divergent mitochondrial DNA clades of the estuarine pulmonate gastropod genus Phallomedusa (Mollusca, Gastropoda). Mar Biol 158:1259–1269CrossRefGoogle Scholar
  19. Goldstien SJ, Schiel DR, Gemmell NJ (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268PubMedCrossRefGoogle Scholar
  20. Grande C, Templado J, Cervera JL, Zardoya R (2004) Molecular phylogeny of Euthyneura (Mollusca: Gastropoda). Mol Biol Evol 21:303–313PubMedCrossRefGoogle Scholar
  21. Grove SJ, Kershaw RC, Smith BJ, Turner E (2006) A systematic list of the marine molluscs of Tasmania. Queen Victoria Museum and Art Gallery, Occasional Paper 8, LauncestonGoogle Scholar
  22. 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
  23. Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysine cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848PubMedCrossRefGoogle Scholar
  24. Hellberg ME, Balch DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 192:1707–1710CrossRefGoogle Scholar
  25. Hodgson AN (1999) The biology of siphonariid limpets (Gastropoda: Pulmonata). Oceanogr Mar Biol 37:245–314Google Scholar
  26. Hubendick B (1946) Systematic monograph of the Patelliformia. Kungliga Sven Vetenskap Handl 23:1–93Google Scholar
  27. Huelsenbeck JP, Ronquist F (2001).MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755Google Scholar
  28. Jenkins BW (1981) Siphonaria funiculata Reeve (Siphonariidae, Pulmonata): a redescription making S. virgulata Hedley a geographical variant of S. funiculate. J Malacol Soc Australas 5:1–15Google Scholar
  29. Jenkins BW (1982) Redescriptions and relationship of Siphonaria zelandica Quoy and Gaimard to S. australis Quoy and Gaimard with a description of S. propria sp. nov. (Mollusca: Pulmonata: Siphonariidae). J Malacol Soc Australas 6:1–35Google Scholar
  30. Jenkins BW (1984) A new siphonariid (Mollusca: Pulmonata) from south-western Australia. J Malacol Soc Australas 6:113–123Google Scholar
  31. Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13. v.3.23Google Scholar
  32. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 426:4015–4026CrossRefGoogle Scholar
  33. Kameda Y, Kawakita A, Kato M (2007) Cryptic genetic divergence and associated morphological differentiation in the arboreal land snail Satsuma (Luchuhadra) largillierti (Camaenidae) endemic to the Ryukyu Archipelago, Japan. Mol Phylogenet Evol 45:519–533PubMedCrossRefGoogle Scholar
  34. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120PubMedCrossRefGoogle Scholar
  35. Knox GA (1980) Plate tectonics and the evolution of intertidal and shallow-water benthic biotic distribution patterns of the southwest Pacific. Palaeogeogr Palaeoclimatol Palaeoecol 31:267–297CrossRefGoogle Scholar
  36. Lambeck K, Chappell J (2001) Sea level change through the last glacial cycle. Science 292:679–686PubMedCrossRefGoogle Scholar
  37. Lee T, Ó’Foighil D (2005) Placing the Floridian marine genetic disjunction into a regional evolutionary context using the “scorched mussel” Brachidontes exustus species complex. Evolution 59:2139–2358PubMedGoogle Scholar
  38. Lisiecki LE, Raymo ME (2005) A Pliocene–Pleistocene stack of 57 globally distributed benthic d18O records. Paleoceanography 20:PA1003Google Scholar
  39. Macpherson JH, Gabriel CJ (1962) Marine molluscs of Victoria. Melbourne University Press, MelbourneGoogle Scholar
  40. McAlpine D (1952) Notes on some Siphonariidae. Proc R Zool Soc NSW 1952:36–42Google Scholar
  41. McArthur AG, Koop BF (1999) Partial 28S rDNA sequences and the antiquity of the hydrothermal vent endemic gastropods. Mol Phylogenet Evol 13:255–274PubMedCrossRefGoogle Scholar
  42. Murray-Wallace CV (2002) Pleistocene coastal stratigraphy, sea-level highstands and neotectonism of the southern Australian passive continental margin - a review. J Quat Sci 17:469–489CrossRefGoogle Scholar
  43. Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323PubMedCrossRefGoogle Scholar
  44. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818PubMedCrossRefGoogle Scholar
  45. Quinn GP (1983) Spawning and egg masses of Siphonaria tasmanica Tenison Woods, 1876 from Victoria. J Malacol Soc Australas 6:81–82Google Scholar
  46. Rambaut A, Drummond AJ (2004) Tracer v.1.3. Available at http://tree.bio.ed.ac.uk/software/tracer/
  47. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100PubMedCrossRefGoogle Scholar
  48. Ridgway KR (2007) Seasonal circulation around Tasmania: An interface between eastern and western boundary dynamics. J Geophys Res 112:C10016CrossRefGoogle Scholar
  49. Ridgway KR, Condie SA (2004) The 5500-km-long boundary flow off western and southern Australia. J Geophys Res 109:C04017CrossRefGoogle Scholar
  50. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  51. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771PubMedCrossRefGoogle Scholar
  52. Swofford DL (2003) PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0. Laboratory of Molecular Systematics. Smithsonian Institution, WashingtonGoogle Scholar
  53. 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
  54. 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
  55. Tellier F, Maynard AP, Correa JA, Faugeron S, Valero M (2009) Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens. Mol Phylogenet Evol 53:679–693PubMedCrossRefGoogle Scholar
  56. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  57. Tilburg CE, Hurlburt HE, O’Brien JJ, Shriver JF (2001) The dynamics of the East Australian Current system: the Tasman Front, the East Auckland Current and the East Cape Current. J Phys Oceanogr 31:2917–2943CrossRefGoogle Scholar
  58. Van Riel P, Jordaens K, Van Houtte N, Frias Martins AM, Verhagen R, Backeljau T (2005) Molecular systematics of the endemic Leptaxini (Gastropoda:Pulmonata) on the Azores islands. Mol Phylogenet Evol 37:132–143Google Scholar
  59. von der Heyden S, Prochazka K, Bowie RCK (2008) Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): application of molecular data to marine conservation planning in South Africa. Mol Ecol 17:4812–4826PubMedCrossRefGoogle Scholar
  60. Waters JM (2008) Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Div Dist 14:692–700CrossRefGoogle Scholar
  61. Waters JM, Roy MS (2003) Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J Biogeogr 30:1787–1796CrossRefGoogle Scholar
  62. Waters JM, King TM, O’Loughlin PM, Spencer HG (2005)Phylogeographic disjunction in an abundant high-dispersal littoral gastropod. Mol Ecol 14:2789–2802Google Scholar
  63. Waters JM, McCulloch GA, Eason JA (2007) Marine biogeographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. J Biogeogr 34:678–687CrossRefGoogle Scholar
  64. Waters JM, Wernberg T, Connell SD, Thomsen MS, Zuccarello GC, Kraft GT, Sanderson JC, West JA, Gurgel CFD (2010) Australia’s marine biogeography revisited: Back to the future? Austral Ecol 35:988–992CrossRefGoogle Scholar
  65. Whitley G (1932) Marine zoogeographical regions of Australia. Aust Natural 8:166–167Google Scholar
  66. Wood AR, Gardner JPA (2010) Evolutionary relationships and biogeography of the New Zealand Siphonariidae. Abstract for the 17th International Conference for UNITAS MALACOLOGICA. Trop Nat Hist Suppl 3:68Google Scholar
  67. York KL, Blacket MJ, Appleton BR (2008) The Bassian Isthmus and the major ocean currents of southeast Australia influence the phylogeography and population structure of a southern Australian barnacle Catomerus polymerus (Darwin). Mol Ecol 17:1948–1961PubMedCrossRefGoogle Scholar
  68. Zakas C, Binford J, Navarrete SA, Wares JP (2009) Restricted gene flow in Chilean barnacles reflects an oceanographic and biogeographic transition zone. Mar Ecol Prog Ser 394:165–177CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.The Australian MuseumSydneyAustralia

Personalised recommendations