Abstract
Biogeographic barriers, some transitory in duration, are likely to have been important contributing factors to modern marine biodiversity in the Indo-Pacific region. One such barrier was the Torres Strait land bridge between continental Australia and New Guinea that persisted through much of the late Pleistocene and separated Indian and Pacific Ocean taxa. Here, we examine the patterns of mitochondrial DNA diversity for marine animals with present-day distributions spanning the Torres Strait. Specifically, we investigate whether there are concordant signatures across species, consistent with either vicariance or recent colonization from either ocean basin. We survey four species of reef fishes (Apogon doederleini, Pomacentrus coelestis, Dascyllus trimaculatus, and Acanthurus triostegus) for mtDNA cytochrome oxidase 1 and control region variation and contrast these results to previous mtDNA studies in diverse marine animals with similar distributions. We find substantial genetic partitioning (estimated from F-statistics and coalescent approaches) between Indian and Pacific Ocean populations for many species, consistent with regional persistence through the late Pleistocene in both ocean basins. The species-specific estimates of genetic divergence, however, vary greatly and for reef fishes we estimate substantially different divergence times among species. It is likely that Indian and Pacific Ocean populations have been isolated for multiple glacial cycles for some species, whereas for other species genetic connections have been more recent. Regional estimates of genetic diversity and directionality of gene flow also vary among species. Thus, there is no apparent consistency among historical patterns across the Torres Strait for these co-distributed marine animals.
References
Aljanabi SM, Martinez I (1997) Universal and rapid salt-extraction of high quality genomic DNA from PCR-based techniques. Nucleic Acids Res 25:4692–4693
Atema J, Kingsford MJ, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160
Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, Cambridge, MA
Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: The mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522
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
Bay LK, Choat JH, van Herwerden L, Robertson DR (2004) High genetic diversities and complex genetic structure in an Indo-Pacific tropical reef fish (Chlorurus sordidus): evidence of an unstable evolutionary past? Mar Biol 144:757–767
Begg GA, Keenan CP, Sellin MJ (1998) Genetic variation and stock structure of school mackerel and spotted mackerel in northern Australian waters. J Fish Biol 53:543–559
Bermingham E, McCafferty SS, Martin AP (1997) Fish biogeography and molecular clocks: perspectives from the Panamanian Isthmus Molecular Systematics. Academic Press, San Diego, pp 113–128
Bernardi G, Holbrook SJ, Schmitt RJ (2001) Gene flow at three spatial scales in a coral reef fish, the three-spot dascyllus, Dascyllus trimaculatus. Mar Biol 138:457–465
Bernardi G, Holbrook SJ, Schmitt RJ, Crane NL, DeMartini E (2002) Species boundaries, populations and colour morphs in the coral reef three-spot damselfish (Dascyllus trimaculatus) species complex. Proc R Soc Lond B Biol Sci 269:599–605
Carter RM, Johnson DP (1986) Sea-level controls on the post-glacial development of the Great Barrier Reef, Queensland. Mar Geol 71:137–164
Chappell J, Shackleton NJ (1986) Oxygen isotopes and sea level. Nature 324:137–140
Chenoweth SF, Hughes JM (2003) Oceanic interchange and nonequilibrium population structure in the estuarine dependent Indo-Pacific tasselfish, Polynemus sheridani. Mol Ecol 12:2387–2397
Chenoweth SF, Hughes JM, Keenan CP, Lavery S (1998) When oceans meet: A teleost shows secondary intergradation at an Indian-Pacific interface. Proc R Soc Lond B Biol Sci 265:415–420
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Collins LB, Zhu ZR, Wyrvoll KH, Eisenhauer A (2003) Late Quaternary structure and development of the northern Ningaloo Reef, Australia. Sediment Geol 159:81–94
Dethmers KEM, Broderick D, Moritz C, Fitzsimmons NN, Limpus CJ, Lavery S, Whiting S, Guinea M, Prince RIT, Kennett R (2006) The genetic structure of Australasian green turtles (Chelonia mydas): exploring the geographical scale of genetic exchange. Mol Ecol 15:3931–3946
Dudgeon CL, Broderick D, Ovenden JR (2009) IUCN classification zones concord with, but underestimate, the population genetic structure of the zebra shark, Stegostoma fasciatum in the Indo-Pacific. Mol Ecol 18:248–261
Duncan KM, Martin AP, Bowen BW, de Couet HG (2006) Global phylogeography of the scalloped hammerhead shark (Sphyrna lewini). Mol Ecol 15:2239–2251
Elliott NG (1996) Allozyme and mitochondrial DNA analysis of the tropical saddle-tail sea perch, Lutjanus malabaricus (Schneider), from Australian waters. Mar Freshw Res 47:869–876
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863
Gopurenko D, Hughes JM (2002) Regional patterns of genetic structure among Australian populations of the mud crab, Scylla serrata (Crustacea: Decapoda): evidence from mitochondrial DNA. Mar Freshw Res 53:849–857
Gopurenko D, Hughes JM, Keenan CP (1999) Mitochondrial DNA evidence for rapid colonisation of the Indo-West Pacific by the mudcrab Scylla serrata. Mar Biol 134:227–233
Greenstein BJ, Pandolfi JM (2008) Escaping the heat: range shifts of reef coral taxa in coastal Western Australia. Global Change Biol 14:513–528
Hellberg ME (2007) Footprints on water: the genetic wake of dispersal among reefs. Coral Reefs 26:463–473
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790
Hickerson MJ, Stahl EA, Lessios HA (2006) Test for simultaneous divergence using approximate Bayesian computation. Evolution 60:2435–2453
Hickerson MJ, Stahl E, Takebayeyashi N (2007) msBayes: Pipeline for testing comparative phylogeographic histories using hierarchical approximate Bayesian computation. BMC Bioinformatics 8:268
Hickerson MJ, Carstens BC, Cavender-Bares J, Crandall KA, Graham CH, Johnson JB, Rissler L, Victoriano PF, Yoder AD (2010) Phylogeography’s past, present, and future: 10 years after Avise, 2000. Mol Phylogenet Evol 54:291–301
Imron, Jeffry B, Hale P, Degnan BM, Degnan SM (2007) Pleistocene isolation and recent gene flow in Haliotis asinina, an Indo-Pacific vetigastropod with limited dispersal capacity. Mol Ecol 16:289-304
Jordan DS (1908) The law of geminate species. Am Nat 42:73–80
Klanten OS, Choat JH, van Herwerden L (2007) Extreme genetic diversity and temporal rather than spatial partitioning in a widely distributed coral reef fish. Mar Biol 150:659–670
Knowlton N, Weigt LA (1998) New dates and new rates for divergence across the Isthmus of Panama. Proc R Soc Lond B Biol Sci 265:2257–2263
Lee W-J, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66
Leray M, Beldade R, Holbrook SJ, Schmitt RJ, Planes S, Bernardi G (2010) Allopatric divergence and speciation in coral reef fish: the three-spot dascyllus, Dascyllus trimaculatus, species complex. Evolution 64:1218–1230
Lessios HA, Kessing BD, Pearse JS (2001) Population structure and speciation in tropical seas: global phylogeography of the sea urchin Diadema. Evolution 55:955–975
Lukoschek V, Waycott M, Marsh H (2007) Phylogeography of the olive sea snake, Aipysurus laevis (Hydrophiinae) indicates Pleistocene range expansion around northern Australia but low contemporary gene flow. Mol Ecol 16:3406–3422
Margvelashvili N, Saint-Cast F, Condie S (2008) Numerical modelling of the suspended sediment transport in Torres Strait. Cont Shelf Res 28:2241–2256
Marshall JF, Davies PJ (1984) Last interglacial reef growth beneath modern reefs in the Southern Great Barrier Reef. Nature 307:44–46
Mayr E (1954) Geographic speciation in tropical echinoids. Evolution 8:1–18
Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Montaggioni LF (2005) History of Indo-Pacific coral reef systems since the last glaciation: development patterns and controlling factors. Earth Sci Rev 71:1–75
Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov Chain Monte Carlo approach. Genetics 158:885–896
Palumbi SR (1994) Genetic divergence, reproductive isolation, and marine speciation. Annu Rev Ecol Syst 25:547–572
Patarnello T, Volckaert FAMJ, Castilho R (2007) Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographic break? Mol Ecol 16:4426–4444
Pelc RA, Warner RR, Gaines SD (2009) Geographical patterns of genetic structure in marine species with contrasting life histories. J Biogeogr 36:1881–1890
Planes S (1993) Genetic differentiation in relation to restricted larval dispersal of the convict surgeonfish, Acanthurus triostegus, in French Polynesia. Mar Ecol Prog Ser 98:237–246
Planes S, Fauvelot C (2002) Isolation by distance and vicariance drive genetic structure of a coral reef fish in the Pacific Ocean. Evolution 56:378–399
Planes S, Parroni M, Chauvet C (1998) Evidence of limited gene flow in three species of coral reef fishes in the lagoon of New Caledonia. Mar Biol 130:361–368
Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818
Rambaut AE (1996) Se-Al: sequence alignment editor v2.0a11. Available at http://evolve.zoo.ox.ac.uk/
Reeves JM, Chivas AR, Garcia A, Holt S, Couapel MJJ, Jones BG, Cendon DI, Fink D (2008) The sedimentary record of palaeoenvironments and sea-level change in the Gulf of Carpentaria, Australia, through the last glacial cycle. Quaternary Int 183:3–22
Reid DG, Lal K, Mackenzie-Dodds J, Kaligis F, Littlewood DTJ, Williams ST (2006) Comparative phylogeography and species boundaries in Echinolittorina snails in the central Indo-West Pacific. J Biogeogr 33:990–1006
Riginos C, Victor BC (2001) Larval spatial distributions and other early life-history characteristics predict genetic differentiation in eastern Pacific blennioid fishes. Proc R Soc Lond B Biol Sci 268:1931–1936
Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography. doi:10.1111/j.1600-0587.2010.06511.x
Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analysis by the coalescent and other methods. Bioinformatics 19:2496–2497
Swofford DL (1998) PAUP*, Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts
Tager D, Webster JM, Potts DC, Renema W, Braga JC, Pandolfi JM (2010) Community dynamics of Pleistocene coral reefs during alternative climatic regimes. Ecology 91:191–200
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Takeyama T, Okuda N, Yanagisawa Y (2007) Filial cannibalism as a conditional strategy in males of a paternal mouthbrooding fish. Evol Ecol 21:109–119
Tittensor DP, Mora C, Jetz W, Lotze HK, Ricard D, Vanden Berghe E, Worm B (2010) Global patterns and predictors of marine biodiversity across taxa. Nature 466:1098–1102
Uthicke S, Benzie JAH (2003) Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific. Mol Ecol 12:2635–2648
van Herwerden L, Choat JH, Newman SJ, Leray M, Hillersøy G (2009) Complex patterns of population structure and recruitment of Plectropomus leopardus (Pisces: Epinephelidae) in the Indo-West Pacific: implications for fisheries management. Mar Biol 156:1595–1607
Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167
Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Philos Trans R Soc Lond B Biol Sci 360:1847–1857
Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Mol Ecol 11:1131–1144
Waters JM, King TM, O’Loughlin PM, Spencer HG (2005) Phylogeographical disjunction in abundant high-dispersal littoral gastropods. Mol Ecol 14:2789–2802
Waters JM, McCulloch GA, Eason JA (2007) Marine biogographical structure in two highly dispersive gastropods: implications for trans-Tasman dispersal. J Biogeogr 34:678–687
Watts PC, Thorpe JP (2006) Influence of contrasting larval developmental types upon the population-genetic structure of cheilostome bryozoans. Mar Biol 149:1093–1101
Weersing K, Toonen RJ (2009) Population genetics, larval dispersal, and connectivity in marine systems. Mar Ecol Prog Ser 393:1–12
Williams ST, Jara J, Gomez E, Knowlton N (2002) The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr Comp Biol 42:941–952
Wolanski E, Ridd P, Inoue M (1988) Currents through the Torres Strait. J Phys Oceanogr 18:1535–1545
Acknowledgements
Thanks to J. D. Aguirre-Davies and F. MacKenzie for assistance in the field, and two anonymous reviewers for comments. The Computational Biology Service Unit from Cornell University, which is partially funded by Microsoft Corporation, was used for some analyses. Funding for this work was provided by the Australian Research Council (DP0878306 to CR), and the World Wildlife Fund (to EAT). Fishes were collected under permits from the Department of the Environment, Water, Heritage, and the Arts (AU-COM2008042), Great Barrier Reef Marine Park Authority and Department of Environment and Resource Management (G08/28114.1), Queensland Government Dept. of Primary Industries & Fisheries (118636), and WA Department of Environment and Conservation (SF006619). This study complies with Animal Ethics standards for the University of Queensland (permit SIB/817/08/ARC).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Biology Editor Dr. Ruth Gates
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mirams, A.G.K., Treml, E.A., Shields, J.L. et al. Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge. Coral Reefs 30, 937–949 (2011). https://doi.org/10.1007/s00338-011-0767-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00338-011-0767-x