Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Habitat type promotes rapid and extremely localised genetic differentiation in dolphins

Luciana M. Möller A B C , Joanna Wiszniewski A B , Simon J. Allen A and Luciano B. Beheregaray B

A Marine Mammal Research Group, Graduate School of the Environment, Macquarie University, NSW 2109, Australia.

B Molecular Ecology Group for Marine Research, Department of Biological Sciences, Macquarie University, NSW 2109, Australia.

C Corresponding author. Email: luciana.moller@gse.mq.edu.au

Marine and Freshwater Research 58(7) 640-648 http://dx.doi.org/10.1071/MF06218
Submitted: 20 November 2006  Accepted: 21 May 2007   Published: 27 July 2007

Abstract

The high potential for dispersal of many marine organisms often results in low population differentiation over large distances. Here, we report that dolphin communities living in very close geographic proximity (<16 km) but in two different environments – open coast and enclosed embayment – exhibit unexpected genetic differentiation at nine microsatellite loci. Results based on a fixation index and a Bayesian clustering approach suggested that gene flow between communities within an embayment is high, as is gene flow between coastal communities. However, lower gene flow between embayment and open coast communities translated into substantial genetic differentiation between dolphin communities from the two environments, and assignment of individuals into two populations. Along with patterns observed in 403 bp of the mitochondrial DNA control region, the results suggest that restriction of gene flow likely occurred in the last 6000 years, after coastal dolphins colonised the embayment. We hypothesise that factors such as fidelity to the local area and resource and behavioural specialisations may have played a major role in promoting and maintaining genetic subdivision between dolphins of the two environments. Importantly, our study shows that habitat type can rapidly promote extremely fine-scale genetic structure in a long-lived, highly mobile marine mammal.

Additional keywords: dispersal, Indo–Pacific bottlenose dolphin, phylogeography, population genetics, Tursiops aduncus.


References

Balloux F. Lugon-Moulin N. 2002 The estimation of population differentiation with microsatellite markers. Molecular Ecology 11 155 165 doi:10.1046/J.0962-1083.2001.01436.X

Baker C. S. Perry A. Bannister J. L. Weinrich M. T. Abernethy R. B. et al. 1993 Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proceedings of the National Academy of Sciences of the USA 90 8239 8243 doi:10.1073/PNAS.90.17.8239

Barber P. H. Palumbi S. R. Erdmann M. V. Moosa M. K. 2000 A marine Wallace’s line. Nature 406 692 693 doi:10.1038/35021135

Barros N. B. Wells R. S. 1998 Prey and feeding patterns of resident bottlenose dolphins (Tursiops truncatus) in Sarasota Bay, Florida. Journal of Mammalogy 79 1045 1060 doi:10.2307/1383114

Beheregaray L. B. Sunnucks P. 2001 Fine-scale genetic structure, estuarine colonisation and incipient speciation in the marine silverside fish Odontesthes argentinensis. Molecular Ecology 10 2849 2866 doi:10.1046/J.1365-294X.2001.T01-1-01406.X

Bilgmann K. Griffiths O. J. Allen S. J. Möller L. M. 2007 A biopsy pole system for bow-riding dolphins: sampling success, behavioral responses and test for sampling bias. Marine Mammal Science 23 218 225 doi:10.1111/J.1748-7692.2006.00099.X

Clement M. Posada D. Crandall K. A. 2000 TCS: a computer program to estimate gene genealogies. Molecular Ecology 9 1657 1659 doi:10.1046/J.1365-294X.2000.01020.X

Cornuet J.-M. Piry S. Luikart G. Estoup A. Solignac M. 1999 New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153 1989 2000

Curry B. E. , and Smith J. (1997). Phylogeographic structure of the bottlenose dolphin (Tursiops truncatus): Stock identification and implications for management. In ‘Molecular Genetics of Marine Mammals’. (Eds A. E. Dizon, S. J. Chivers and W. F. Perrin.) pp. 227–247. (Society for Marine Mammalogy: Lawrence, FL.)

Defran R. H. Weller D. W. 1999 The occurrence, distribution, and site fidelity of bottlenose dolphins (Tursiops truncatus) in San Diego, California. Marine Mammal Science 15 366 380
doi:10.1111/J.1748-7692.1999.TB00807.X

Excoffier L. Smouse P. E. Quattro J. M. 1992 Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131 479 491

Favre L. Balloux F. Goudet J. Perrin N. 1997 Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London. Series B. Biological Sciences 264 127 132
doi:10.1098/RSPB.1997.0019

Felsenstein J. (1997). PHYLIP v. 3.5c (phylogeny inference package) (University of Washington: Seattle, WA.)

Gaggiotti O. E. Lange O. Rassmann K. Gliddon C. 1999 A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Molecular Ecology 8 1513 1520 doi:10.1046/J.1365-294X.1999.00730.X

Gilson A. Syvanen M. Levine K. F. Banks J. D. 1998 Deer gender determination by polymerase chain reaction: validation study and application to tissues, bloodstains, and hair forensic samples from California. California Fish and Game 84 159 169

Goodnight K. F. , and Queller D. C. (1998). ‘RELATEDNESS 5.4.’ Goodnight software. Available at
http://www.bioc.rice.edu-kfg/Gsoft.html.

Goudet J. (2001). ‘FSTAT, a Program to Estimate and Test Gene Diversities and Fixation Indices (Version 2.9.3).’ Available at http://www.unil.ch/izea/softwares/fstat.html.

Hale P. T. Barreto A. S. Ross G. J. B. 2000 Comparative morphology and distribution of the aduncus and truncatus forms of bottlenose dolphin Tursiops in the Indian and Western Pacific Oceans. Aquatic Mammals 26 101 110

Hoelzel A. R. 1998 Genetic structure of cetacean populations in sympatry, parapatry and mixed assemblages: implications for conservation policy. Journal of Heredity 89 451 458


Hoelzel A. R. Potter C. W. Best P. B. 1998 Genetic differentiation between parapatric ‘nearshore’ and ‘offshore’ populations of the bottlenose dolphin. Proceedings of the Royal Society of London. Series B. Biological Sciences 265 1177 1183
doi:10.1098/RSPB.1998.0416

Kimura M. 1980 A simple method for estimating evolutionary rate of base subsitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16 111 120 doi:10.1007/BF01731581

Krützen M. Valsecchi E. Connor R. C. Sherwin W. B. 2001 Characterization of microsatellite loci in Tursiops aduncus. Molecular Ecology Notes 1 170 172 doi:10.1046/J.1471-8278.2001.00065.X

Krützen M. Barré L. M. Möller L. M. Heithaus M. R. Simms C. Sherwin W. B. 2002 A biopsy system for small cetaceans: darting success and wound healing in Tursiops spp. Marine Mammal Science 18 863 878 doi:10.1111/J.1748-7692.2002.TB01078.X

Krützen M. Mann J. Heithaus M. R. Connor R. C. Bejder L. Sherwin W. B. 2005 Cultural transmission of tool use in bottlenose dolphins. Proceedings of the National Academy of Sciences of the USA 102 8939 8943 doi:10.1073/PNAS.0500232102

LeDuc R. G. Perrin W. F. Dizon A. E. 1999 Phylogenetic relationships among the delphinid cetaceans based on full cytochrome b sequences. Marine Mammal Science 15 619 648 doi:10.1111/J.1748-7692.1999.TB00833.X

Manly B. F. J. (1997). ‘RT, a Program for Randomisation Testing, Version 2.1.’ (Centre for Applications of Statistics and Mathematics: University of Otago, Dunedin.)

Möller L. M. Allen S. J. Harcourt R. G. 2002 Group characteristics, site fidelity and abundance of bottlenose dolphins (Tursiops aduncus) in Jervis Bay and Port Stephens, southeastern Australia. Australian Mammalogy 24 11 21

Möller L. M. (2001). Social organization and genetic relationships of coastal bottlenose dolphins in southeastern Australia. PhD Thesis, Macquarie University, Sydney.

Möller L. M. Beheregaray L. B. 2001 Coastal bottlenose dolphins from southeastern Australia are Tursiops aduncus according to sequences of the mitochondrial DNA control region. Marine Mammal Science 17 249 263
doi:10.1111/J.1748-7692.2001.TB01269.X

Möller L. M. Beheregaray L. B. 2004 Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops aduncus). Molecular Ecology 13 1607 1612 doi:10.1111/J.1365-294X.2004.02137.X

Möller L. M. Beheregaray L. B. Krützen M. Harcourt R. G. 2001 Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proceedings of the Royal Society of London. Series B. Biological Sciences 268 1941 1947 doi:10.1098/RSPB.2001.1756

Möller L. M. Beheregaray L. B. Allen S. J. Harcourt R. G. 2006 Association patterns and kinship in female Indo–Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Behavioral Ecology and Sociobiology 61 109 117 doi:10.1007/S00265-006-0241-X

Natoli A. Birkun A. Aguilar A. Lopez A. Hoelzel A. R. 2005 Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society of London. Series B. Biological Sciences 272 1217 1226 doi:10.1098/RSPB.2005.3076

Nei M. 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89 583 590

Palumbi S. R. 1992 Marine speciation on a small planet. Trends in Ecology & Evolution 7 114 118
doi:10.1016/0169-5347(92)90144-Z

Palumbi S. R. Warner R. R. 2003 Why gobies are like Hobbits. Science 299 51 52 doi:10.1126/SCIENCE.1080775

Petit R. J. El Mousadik A. Pons O. 1998 Identifying populations for conservation on the basis of genetic markers. Conservation Biology 12 844 855 doi:10.1046/J.1523-1739.1998.96489.X

Pritchard J. K. Stephens M. Donnelly P. 2000 Inference of population structure using multilocus genotype data. Genetics 155 945 959

Rannala B. Mountain J. L. 1997 Detecting immigration by using multi-locus genotypes. Proceedings of the National Academy of Sciences of the United States of America 94 9197 9201
doi:10.1073/PNAS.94.17.9197

Raymond M. Rousset F. 1995 Population genetics software for exact tests and ecumenicism. Journal of Heredity 86 248 249

Rice D. W. (1998). ‘Marine Mammals of the World: Systematics and Distribution.’ (Society for Marine Mammalogy: Lawrence, FL.)

Rice W. 1989 Analysing tables of statistical tests. Evolution 43 223 225
doi:10.2307/2409177

Ross G. J. B. , and Cockcroft V. G. (1990). Comments on Australian bottlenose dolphins and the taxonomic status of Tursiops aduncus (Ehrenberg, 1832). In ‘The Bottlenose Dolphin’. (Eds S. Leatherwood and R. R. Reeves.) pp. 101–128. (Academic Press: San Diego, CA.)

Roy P. S. 1984 Holocene sedimentation histories of estuaries in southeastern Australia. Western Australian Department of Conservation and Environment Bulletin 161 23 59

Schneider S. , Roessli D. , and Excoffier L. (2000). ‘Arlequin: A Software for Population Genetics Data Analysis.’ Ver 2.000. (Genetics and Biometry Lab, Department of Anthropology, University of Geneva: Geneva.)

Sellas A. B. Wells R. S. Rosel P. E. 2005 Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. Conservation Genetics 6 715 728
doi:10.1007/S10592-005-9031-7

Shane S. H. Wells R. S. Würsig B. 1986 Ecology, behavior and social organization of the bottlenose dolphin: a review. Marine Mammal Science 2 34 63 doi:10.1111/J.1748-7692.1986.TB00026.X

Shinohara M. Domingoroura X. Takenaka O. 1997 Microsatellites in the bottlenose dolphin Tursiops truncatus. Molecular Ecology 6 695 696 doi:10.1046/J.1365-294X.1997.00231.X

Smolker R. A. Richards A. F. Connor R. C. Mann J. Berggren P. 1997 Sponge-carrying by Indian Ocean bottlenose dolphins: possible tool-use by a delphinid. Ethology 103 454 465

Slatkin M. 1995 A measure of population subdivision based on microsatellite allele frequencies. Genetics 139 457 462


Sunnucks P. Hales D. F. 1996 Numerous transposed sequences of mitochondrial cytochrome oxidase I-II in aphids of the genus Sitobion (Hemiptera: Aphididae). Molecular Biology and Evolution 13 510 523


Sunnucks P. Wilson A. C. C. Beheregaray L. B. Zenger K. French J. Taylor A. C. 2000 SSCP is not so difficult: the application and utility of single-stranded conformation polymorphism in evolutionary biology and molecular ecology. Molecular Ecology 9 1699 1710
doi:10.1046/J.1365-294X.2000.01084.X

Swofford D. Selander R. 1981 BIOSYS-1: a FORTRAN program for the comprehensive analysis of electrophoretic data in population genetics and systematics. The Journal of Heredity 72 281 283

Taylor M. S. Hellberg M. E. 2003 Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299 107 10
doi:10.1126/SCIENCE.1079365

Templeton A. R. Crandall K. A. Sing C. F. 1992 A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132 619 633

Valsecchi E. Amos W. 1996 Microsatellite markers for the study of cetacean populations. Molecular Ecology 5 151 156


Wang J. Y. Chou L. S. White B. N. 1999 Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Molecular Ecology 8 1603 1612
doi:10.1046/J.1365-294X.1999.00741.X

Watts R. J. Johnson M. S. 2004 Estuaries, lagoons and enclosed embayments: habitats that enhance population subdivision of inshore fishes. Marine and Freshwater Research 55 641 651 doi:10.1071/MF04051

Wells R. S. , Scott M. D. , and Irvine A. B. (1987). The social structure of free-ranging bottlenose dolphins. In ‘Current Mammalogy’. (Ed. H. H. Genoways.) pp. 247–305. (Plenum Press: New York.)

Weir B. S. Cockerham C. C. 1984 Estimating F-statistics for the analysis of population structure. Evolution 38 1358 1370 doi:10.2307/2408641



Rent Article Export Citation Cited By (41)