Abstract
In this paper we use mitochondrial and microsatellite DNA variation to investigate the mechanisms that underlie the evolution of population structure in a highly mobile marine mammal, the white-beaked dolphin. We found moderate genetic diversity (h) at mtDNA, but low nucleotide diversity (π) (0.7320 ± 0.0031 and 0.0056 ± 0.0004, respectively), consistent with expectations for a recent expansion. Analyses based on mismatch distributions further suggested a demographic expansion in the Norwegian-Barents Sea population and a spatial expansion in the British isles-North Sea population, implying distinct demographic histories. F ST values showed clear differentiation among these two populations, but no difference was found between putative populations separated by the English Channel. Our data suggest a stepwise pattern of expansion, dependent on available coastal habitat. The conservation implications are a need to protect local populations isolated by an expanse of deep water, and in particular, a population along the British coasts and in the North Sea as separate from the North Norway-Barents Sea population. It is also evident that overall diversity was reduced, probably during the last glacial epoch.
Similar content being viewed by others
References
Adams SM, Lindmeier JB, Duvernell DD (2006) Microsatellite analysis of the phylogeography, pleistocene history and secondary contact hypothesis for the killifish, Fundulus heteroclitus. Mol Ecol 15:1109–1123
Alling AK, Whitehead HP (1987) A preliminary study of the status of white-beaked dolphins, Lagenorhynchus albirostris, and other small cetaceans off the coast of Labrador. Can Field Nat 1012:131–135
Andersen LW, Ruzzante DE, Walton M, Berggren P, Bjørge A, Lockyer C (2001) Conservation genetics of harbour porpoises, Phocoena phocoena, in eastern and central North Atlantic. Conserv Genet 2:309–324
Austerlitz F, JungMuller B, Godelle B, Gouyon PH (1997) Evolution of coalescence times, genetic diversity and structure during colonization. Theor Popul Biol 51:148–164
Avise JC, Walker D, Johns GC (1998) Speciation durations and Pleistocene effects on vertebrate phylogeography. Proc R Soc Lond 265:1707–1712
Bahri-Sfar L, Lemaire C, Ben Hassine OK, Bonhomme F (2000) Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proc R Soc B 267:929–935
Bandelt HJ, Forster P, Röhl A (1999) Median joining networks for inferring intraespecific phylogenies. Mol Biol Evol 16:37–48
Bérubé M, Aguilar A, Dendanto D, Larsen F, Notarbartolo DS, Sears GR, Sigurjónsson J, Urban R, Palsbøll PJ (1998) Population genetic structure of North Atlantic, Mediterranean Sea and Sea of Cortez fin whales, Balaenoptera physalus Linnaeus 1758: analysis of mitochondrial and nuclear loci. Mol Ecol 7:585–599
Buchanan FC, Friesen MK, Littlejohn RP, Clayton JW (1996) Microsatellites from the beluga whale, Delphinapterus leucas. Mol Ecol 5:571–575
Carleton KL, Streelman JT, Lee BY, Garnhart N, Kidd M, Kocher TD (2002) Rapid isolation of CA microsatellites from the tilapia genome. Anim Genet 33:140–144
Carr SM, Marshall HD (2008) Intraspecific phylogeographic genomics from multiple complete mtDNA genomes in Atlantic cod (Gadus morhua): origins of the “codmother”, transatlantic vicariance and midglacial population expansion. Genetics 180:381–389
Cassens I, Van Waerebeek K, Best PB, Crespo EA, Reyes J, Milinkovitch MC (2003) The phylogeography of dusky dolphins Lagenorhynchus obscurus: a critical examination of network methods and rooting procedures. Mol Ecol 12:1781–1792
Cassens I, Van Waerebeek K, Best PB, Tzika A, Van Helden AL, Crespo EA, Milinkovitch MC (2005) Evidence for male dispersal along the coasts but no migration in pelagic waters in dusky dolphins Lagenorhynchus obscurus. Mol Ecol 14:107–121
Castello HP (1996) An introduction to the whales and dolphin. In Simmonds M, Hutchinson JD (eds) The conservation of whales and dolphin. Wiley, London
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Costedoat C, Chapazz R, Barascud B, Guillard O, Gilles A (2006) Heterogeneous colonization pattern of European cyprinids, as highlighted by the dace complex Teleostei:Cyprinidae. Mol Phylogenet Evol 41:127–148
Dalebout ML, Ruzzante DE, Whitehead H, Oien NI (2006) Nuclear and mitochondrial markers reveal distinctiveness of a small population of bottlenose whales Hyperoodon ampullatus in the western North Atlantic. Mol Ecol 15:3115–3129
DeBruyn M, Hall BL, Chauke LF, Baroni C, Koch PL, Hoelzel AR (2009) Rapid response of a marine mammal species to Holocene climate and habitat change. PLoS Genet 5:e1000554
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170
Domingues VS, Stefanni S, Brito A, Santos RS, Almada VC (2008) Phylogeography and demography of the Blenniid Parablennius parvicornis and its sister species P. sanguinolentus from the northeastern Atlantic Ocean and the western Mediterranean Sea. Mol Phylogenet Evol 46:397–402
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
Evans PGH (1992) Status review of cetaceans in British and Irish waters. UK Department of the Environment, London
Evans PGH, Hammond PS (2004) Monitoring cetaceans in European waters. Mamm Rev Vol 34:131–156
Excoffier L (2004) Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol 13:853–864
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
Excoffier L, Laval G, Schneider SL (2007) Arlequin versión 3.11: a sofware for population genetic data analysis. Genetic and Biometry laboratory, University of Geneva Switzerland
Fu YX (1997) Statistical neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Garza JCE, Williamson E (2001) Detection of reduction in population size using data from microsatellite DNA. Mol Ecol 10:305–318
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)
Guarniero I, Franzellitti S, Ungaro N, Tommasini S, Piccinetti C, Tinti F (2002) Control region haplotype variation in the central Mediterranean common sole indicates geographical isolation and population structuring in Italian stocks. J Fish Biol 60:1459–1474
Guo SW, Thompson EA (1992) Performing the exact test for Hardy Weinberg proportions for multiple alleles. Biometric 48:361–372
Gysels ES, Hellemans B, Pampoulie C, Volckaert F (2004) Phylogeography of the common goby, Pomatoschistus microps, with particular emphasis on the colonization of the mediterranean and the North Sea. Mol Ecol 13:403–417
Hammond PS, Berggren P, Benke H, Borchers DL, Collet A, Heide-Jorgensen MP, Heimlich S, Hiby AR, Leopold MF, Oiens N (2002) Abundance of harbour porpoise and other cetaceans in the North Sea and adjacent water. J Appl Ecol 39:361–376
Hammond PS, Bearzi G, Bjørge A, Forney K, Karczmarski L, Kasuya T, Perrin WF, Scott MD, Wang JY, Wells RS, Wilson B (2008) Lagenorhynchus albirostris. In: IUCN 2009. IUCN red list of threatened species. Version 2009.1
Haney RA, Silliman BR, Fry AJ, Layman CA, Rand DM (2007) The Pleistocene history of the sheepshead minnow Cyprinodon variegatus: non-equilibrium evolutionary dynamics within a diversifying species complex. Mol Phylogenet Evol 43:743–754
Harlin AD, Markowitz T, Baker CS, Würsig B, Honeycutt RL (2003) Genetic structure, diversity, and historical demography of New Zealand’s dusky dolphin Lagenorhynchus obscurus. J Mamm 84:702–717
Harlin-Cognato AD, Markowitz T, Würsig B, Honeycut RL (2007) Multi-locus phylogeography of the dusky dolphin Lagenorhynchus obscurus: passive dispersal via the west-wind drift or response to prey species and climate change? BMC Evol Biol 7:1–17
Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–600
Hasegawa M, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174
Hayano H, Yoshioka M, Tanaka M, Amano M (2004) Population differentiation in the pacific white-sided Dolphin Lagenorhynchus obliquidens inferred from mitochondrial DNA and microsatellite analyses. Zool Sci 21:989–999
Hewitt GM (1996) Some genetic consequences of ice ages and their role in divergence and speciation. Biol J Linn Soc 58:247–276
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913
Hewitt GM (2004) Genetic consequences of climatic oscillations in the Quaternary. Phil Trans R Soc Lond B Biol Sci 359:183–195
Ho SYW, Kolokotronis SO, Allaby RG (2007) Elevated substitution rates estimated from ancient DNA sequences. Biol Lett Mol Evol 18:1–5
Hoelzel AR (2009) Evolution of population structure in marine mammals. In: Haufe H et al (eds) Population genetics for animal conservation. Cambridge University Press, Cambridge
Hoelzel AR, Green A (1998) PCR protocols and population analysis by direct DNA sequencing and PCR-based fingerprinting. In Hoelzel AR (ed) Molecular genetic analysis of population, a practical approach, 2nd edn. Oxford University Press
Hoelzel AR, Potter CW, Best P (1998a) Genetic differentiation between parapatric ‘nearshore’ and ‘offshore’ populations of the bottlenose dolphin. Proc R Soc B 265:1–7
Hoelzel AR, Dahlheim M, Stern SJ (1998b) Low genetic variation among killer whales Orcinus orca in the Eastern North Pacific and genetic differentiation between foraging specialist. J Hered 89:121–128
Hoelzel AR, Natoli A, Dahlheim ME, Olavarria C, Baird RW, Black NA (2002) Low worldwide genetic diversity in the killer whale Orcinus orca: implications for demographic history. Proc R Soc Lond 269:467–1473
Hudson RR (1990) Gene genealogies and the coalescent process. Oxf Surv Evol Biol 7:1–44
IUCN (2007) European mammal assessment. http://ec.europa.eu/especies/ema
Jefferson TA, Leatherwood S, Webber MA (1993) Marine mammals of the world: FAO species identification guide united nation environment programme and food and agricultural organization of the UN. 320 pp
Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738
Kimura A, Ohta T (1978) Stepwise mutation model and distribution of allelic frequencies in a finite population. Proc Natl Acad Sci USA 75:2868–2872
Leatherwood S, Caldwell DK, Winn HE (1976) Whales, dolphins, and porpoises of the western North Atlantic. A guide to their identification. U.S. Department of Commerce, NOAA Tech. Rep. NMFS Circ. 396. 176 pp
Lien J, Nelson D, Hai DJ (2001) Status of the White-beaked Dolphin, Lagenorhynchus albirostris, in Canada. Can Field-Nat 115:118–126
MacLeod CD, Weir CR, Pierpoint C, Harland EJ (2007) The habitat preferences of marine mammals in the west of Scotland UK. J Mar Biol Assoc UK 87:157–164
Mikkelsen AMH, Lund A (1994) Intraespecific variation in the dolphins Lagenorhynchus albirostris and L. acutus Mammalia, cetacean in metrical and nonmetrical skull characters, with remarks on occurrence. J Zool (London) 234:289–299
Milinkovitch MC, LeDuc R, Tiedemann R, Dizon A (2002) Applications of molecular data in cetacean taxonomy and population genetics with special emphasis on defining species boundaries. In: Evans PGH, Raga JA (eds) Marine mammals: biology and conservation. Kluwer Academic Press, NY, pp 325–359
Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR (2005) Habitat structure and the dispersal of male and female bottlenose dolphins Tursiops truncatus. Proc R Soc B Biol Sci 272:1217–1226
Natoli A, Cañadas A, Peddemors VM, Aguilar C, Vaquero C, Fernandez-Piqueras P, Hoelzel AR (2006) Phylogeography and alpha taxonomy of the common dolphin Delphinus sp. J Evol Biol 19:943–954
Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Montecarlo approach. Genetics 158:885–896
Northridge SP, Tasker ML, Webb A, Willians JM (1995) Distribution and relative abundance of harbor porpoises Phocoena-phocoena, white-beaked dolphins lagenorhynchus-albirostris Gray, and minke whales balaenoptera-acutorostrata lacepede around the british-isles. Ices J Mar Sci 52:55–66
Northridge SP, Tasker ML, Webb A, Camphuysen K, Leopold M (1997) White-beaked Lagenorhynchus albirostris and Atlantic white-sided dolphin L. acutus distributions in Northwest European and U.S. North Atlantic waters, vol 47. Reports of the International Whaling Commission, pp 797–805
Perez-Losada M, Guerra A, CarvalhoGR Sanjuan A, Shaw PW (2002) Extensive population subdivision of the cuttlefish Sepia officinalis (Mollusca: cephalopoda) around the Iberian Peninsula indicated by microsatellite DNA variation. Heredity 89:417–424
Pichler FB, Baker CS (2000) Loss of genetic diversity in the endemic Hector’s dolphin due to fisheries-related mortality. Proc R Soc Lond B Biol Sci 267:97–102
Querouil S, Silva MA, Freitas L, Prieto R, Magalhaes S, Dinis A, Alves F, Matos JA, Mendonca D, Hammond PS (2007) High gene flow in oceanic bottlenose dolphins Tursiops truncatus of the North Atlantic. Conserv Genet 8:1405–1419
Ray N, Currat M, Excoffier L (2003) Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol 20:76–86
Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49:1280–1283
Reeb CA, Avise JC (1990) A genetic discontinuity in a continuously distributed species -mitochondrial-DNA in the American oyster, Crassostrea virginica. Genetics 124:397–406
Reeves RR, Smeenk C, Brownell L, Kinze CC (1999) Atlantic white-sided dolphin Lagenorhynchus acutus Gray, 1828 In: Ridgway SH, Harrison SR (eds) Handbook of marine mammals, vol 6. The Second book of dolphins and porpoises. Academic Press, San Diego, pp 31–56
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569
Rooney AP, Merrit DB, Derr JN (1999) Microsatellite diversity in captive bottlenose dolphins Tursiops truncatus. J Hered 90:228–231
Rosa S, Milinkovitch MC, Van Waerebeek K, Berck J, Oporto J, Alfaro-Shigueto J, Van Bressem M, Goodall N, Cassens I (2005) Population structure of nuclear and mitochondrial DNA variation among South American Burmeister’s porpoises Phocoena spinipinnis. Conserv Genet 6:431–443
Rosel PE, France SC, Wangs JY, Kocher TD (1999) Genetic structure of harbour porpoise Phocoena phocoena populations in the northwest Atlantic based on mitochondrial and nuclear markers. Mol Ecol 8:S41–S51
Rousset F, Raymond M (1995) Testing heterozygote excess and deficiency. Genetics 140:1413–1419
Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analices by coalescent and other methods. Bioinformatics 19:2496–2497
Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Shapiro B, Drummond AJ, Rambaut A, Wilson MC, Matheus PE (2004) Rise and fall of the Beringian steppe bison. Science 306:1561–1565
Shinohara X, Domingo-Roura J, Takenata O (1997) Microsatellites in the bottlenose dolphin Tursiops truncatus. Mol Ecol 6:695–696
Simard P, Lawlor JL, Gowans S (2006) Temporal variability of cetaceans near Halifax, Nova Scotia. Can Field Nat 120:93–99
Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462
Slatkin M, Hudson RR (1991) Pairwise comparison of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony and other methods, v. 4.0 β10. Sinauer Associates, Sunderland, MA
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464
Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601
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) MEGA 4: molecular evolutionary genetics analysis MEGA software version 4.0. Mol Biol Evol 24:1596–1599
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Valsecchi E, Amos W (1996) Microsatellite markers for the study the cetacean populations. Mol Ecol 5:151–156
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Wares JP (2002) Community genetics in the Northwestern Atlantic intertidal. Mol Ecol 11:1131–1144
Wares JP, Cunningham CW (2001) Phylogeography and historical ecology of the North Atlantic intertidal. Evolution 55:2455–2469
Wegmann D, Currat M, Excoffier L (2006) Molecular diversity after a range expansion in heterogeneous environments. Genetics 174:2009–2020
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Weir CR, Stockin KA, Pierce GJ (2007) Spatial and temporal trends in the distribution of harbour porpoises, white-beaked dolphins and minke whales off Aberdeenshire UK, north-western North Sea. J Mar Biol 87:327–338
Wright S (1951) The genetic structure of populations. Ann Eugen 15:323–354
Acknowledgements
We thank Charlie Shaw, Fernando Gast Harders and Theresa Mackinven for assistance and support. We thank Charlie Potter, Rob Deaville, Mary Harman, Emer Rogan, Mirimin Luca, and staff at the Natural History Museum Rotterdam, National Museum of Natural History (Naturalis) Leiden, and the Smithsonian Museum of Natural History for help with the acquisition of samples (Samples catalogue numbers using in this study for L. albirostris are available from the author). This project was supported by the Programme Alβan, European Union Programme of high level Scholarship for Latin America (Identification number EO3D17203CO); The Alexander von Humboldt Biological Resources Research Institute, the Colombian Institute of Studies Abroad (ICETEX), and Ustinov College, University of Durham. The UK Cetacean Strandings Project, from which many samples were acquired, is funded by UK, The Department for Environment Food and Rural Affairs, with further financial support from the Scottish Government.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Banguera-Hinestroza, E., Bjørge, A., Reid, R.J. et al. The influence of glacial epochs and habitat dependence on the diversity and phylogeography of a coastal dolphin species: Lagenorhynchus albirostris . Conserv Genet 11, 1823–1836 (2010). https://doi.org/10.1007/s10592-010-0075-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-010-0075-y