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.
Similar content being viewed by others
References
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 18:1887–1903
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 59:249–270
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 4:105–159
Bird CE, Holland BS, Bowen BW, Toonen RJ (2007) Contrasting phylogeography in three endemic Hawaiian limpets (Cellana spp.) with similar life histories. Mol Ecol 16:3173–3186
Bird CE, Holland BS, Bowen BW, Toonen RJ (2011) Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago. Mol Ecol 20:2128–2141
Bostock HC, Opdyke BN, Gagan MK, Kiss AE, Fifield LK (2006) Glacial/interglacial changes in the East Australian current. Clim Dynamics 26:645–659
Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Colgan DJ, da Costa P (2009) DNA haplotypes cross species and biogeographic boundaries in estuarine hydrobiid snails of the genus Tatea. Mar Freshw Res 60:861–872
Colgan DJ, Schreiter S (2011) Extrinsic and intrinsic influences on the phylogeography of the Austrocochlea constricta species group. J Exp Mar Biol Ecol 397:44–51
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/0071
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 29:707–719
Creese RG (1980) Reproductive cycles and fecundities of two species of Siphonaria (Mollusca: Pulmonata) in south-eastern Australia. Aust J Mar Freshw Res 31:37–47
Dawson MN (2001) Phylogeography in coastal marine animals: a solution from California? J Biogeog 28:723–736
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, 2012
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 3:294–299
Fraser CI, Spencer HG, Waters JM (2009) Glacial oceanographic contrasts explain phylogeography of Australian bull kelp. Mol Ecol 18:2287–2296
Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570
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 158:1259–1269
Goldstien SJ, Schiel DR, Gemmell NJ (2006) Comparative phylogeography of coastal limpets across a marine disjunction in New Zealand. Mol Ecol 15:3259–3268
Grande C, Templado J, Cervera JL, Zardoya R (2004) Molecular phylogeny of Euthyneura (Mollusca: Gastropoda). Mol Biol Evol 21:303–313
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, Launceston
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98
Hellberg ME, Vacquier VD (1999) Rapid evolution of fertilization selectivity and lysine cDNA sequences in teguline gastropods. Mol Biol Evol 16:839–848
Hellberg ME, Balch DP, Roy K (2001) Climate-driven range expansion and morphological evolution in a marine gastropod. Science 192:1707–1710
Hodgson AN (1999) The biology of siphonariid limpets (Gastropoda: Pulmonata). Oceanogr Mar Biol 37:245–314
Hubendick B (1946) Systematic monograph of the Patelliformia. Kungliga Sven Vetenskap Handl 23:1–93
Huelsenbeck JP, Ronquist F (2001).MrBayes: Bayesian inference of phylogeny. Bioinformatics 17:754–755
Jenkins BW (1981) Siphonaria funiculata Reeve (Siphonariidae, Pulmonata): a redescription making S. virgulata Hedley a geographical variant of S. funiculate. J Malacol Soc Australas 5:1–15
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 6:1–35
Jenkins BW (1984) A new siphonariid (Mollusca: Pulmonata) from south-western Australia. J Malacol Soc Australas 6:113–123
Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genetics 6:13. v.3.23
Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 426:4015–4026
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 45:519–533
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Knox GA (1980) Plate tectonics and the evolution of intertidal and shallow-water benthic biotic distribution patterns of the southwest Pacific. Palaeogeogr Palaeoclimatol Palaeoecol 31:267–297
Lambeck K, Chappell J (2001) Sea level change through the last glacial cycle. Science 292:679–686
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 59:2139–2358
Lisiecki LE, Raymo ME (2005) A Pliocene–Pleistocene stack of 57 globally distributed benthic d18O records. Paleoceanography 20:PA1003
Macpherson JH, Gabriel CJ (1962) Marine molluscs of Victoria. Melbourne University Press, Melbourne
McAlpine D (1952) Notes on some Siphonariidae. Proc R Zool Soc NSW 1952:36–42
McArthur AG, Koop BF (1999) Partial 28S rDNA sequences and the antiquity of the hydrothermal vent endemic gastropods. Mol Phylogenet Evol 13:255–274
Murray-Wallace CV (2002) Pleistocene coastal stratigraphy, sea-level highstands and neotectonism of the southern Australian passive continental margin - a review. J Quat Sci 17:469–489
Nei M (1973) Analysis of gene diversity in subdivided populations. Proc Natl Acad Sci USA 70:3321–3323
Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818
Quinn GP (1983) Spawning and egg masses of Siphonaria tasmanica Tenison Woods, 1876 from Victoria. J Malacol Soc Australas 6:81–82
Rambaut A, Drummond AJ (2004) Tracer v.1.3. Available at http://tree.bio.ed.ac.uk/software/tracer/
Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19:2092–2100
Ridgway KR (2007) Seasonal circulation around Tasmania: An interface between eastern and western boundary dynamics. J Geophys Res 112:C10016
Ridgway KR, Condie SA (2004) The 5500-km-long boundary flow off western and southern Australia. J Geophys Res 109:C04017
Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497
Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771
Swofford DL (2003) PAUP: Phylogenetic Analysis Using Parsimony, Version 4.0. Laboratory of Molecular Systematics. Smithsonian Institution, Washington
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 10:512–526
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
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 53:679–693
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 25:4876–4882
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 31:2917–2943
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 37:132–143
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 17:4812–4826
Waters JM (2008) Marine biogeographical disjunction in temperate Australia: historical landbridge, contemporary currents, or both? Div Dist 14:692–700
Waters JM, Roy MS (2003) Marine biogeography of southern Australia: phylogeographical structure in a temperate sea-star. J Biogeogr 30:1787–1796
Waters JM, King TM, O’Loughlin PM, Spencer HG (2005)Phylogeographic disjunction in an abundant high-dispersal littoral gastropod. Mol Ecol 14:2789–2802
Waters JM, McCulloch GA, Eason JA (2007) Marine biogeographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. J Biogeogr 34:678–687
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 35:988–992
Whitley G (1932) Marine zoogeographical regions of Australia. Aust Natural 8:166–167
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 3:68
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 17:1948–1961
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 394:165–177
Acknowledgements
We thank the Australian Museum and the NSW Environmental Trust (Grant 2008/RD/0071) for supporting this research financially. We thank Dr Peter Teske for discussions on Siphonaria taxonomy and gene flow and two anonymous reviewers for advice on an earlier version of this manuscript. Collections for this project were undertaken under Permits F86/2163(A) (New South Wales Fisheries Research Permit), 7118 (Tasmania DPIW permit) and RP972 (Victoria General Research Permit).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Colgan, D.J., da Costa, P. Possible drivers of biodiversity generation in the Siphonaria of southeastern Australia. Mar Biodiv 43, 73–85 (2013). https://doi.org/10.1007/s12526-012-0127-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12526-012-0127-2