Conservation Genetics

, 8:1405 | Cite as

High gene flow in oceanic bottlenose dolphins (Tursiops truncatus) of the North Atlantic

  • Sophie Quérouil
  • Mónica A. Silva
  • Luís Freitas
  • Rui Prieto
  • Sara Magalhães
  • Ana Dinis
  • Filipe Alves
  • José A. Matos
  • Diogo Mendonça
  • Philip S. Hammond
  • Ricardo S. Santos
Original Article

Abstract

Despite the openness of the oceanic environment, limited dispersal and tight social structure often induce genetic structuring in marine organisms, even in large animals such as cetaceans. In the bottlenose dolphin, mitochondrial and nuclear DNA analyses have revealed the existence of genetic differentiation between pelagic (or offshore) and coastal (or nearshore) ecotypes in the western North Atlantic, as well as between coastal populations. Because previous studies concentrated on continental margins, we analysed the population structure of bottlenose dolphins in two of the most isolated archipelagos of the North Atlantic: the Azores and Madeira. We analysed 112 samples collected on live animals in the two archipelagos, and nine samples collected on stranded animals in Madeira and mainland Portugal. Genetic analyses consisted in molecular sexing, sequencing of part of the mitochondrial hyper-variable region, and screening of ten microsatellite loci. We predicted that: (1) there is at least one pelagic and one or more coastal populations in each archipelago; (2) populations are differentiated between and possibly within archipelagos. Contrary to these predictions, results indicated a lack of population structure in the study area. In addition, comparison with published sequences revealed that the samples from the Azores and Madeira were not significantly differentiated from samples of the pelagic population of the western North Atlantic. Thus, bottlenose dolphins occurring in the pelagic waters of the North Atlantic belong to a large oceanic population, which should be regarded as a single conservation unit. Unlike what is known for coastal populations, oceanic bottlenose dolphins are able to maintain high levels of gene flow.

Keywords

Cetaceans Azores Madeira Population genetics Ecotypes 

References

  1. Abe H, Goto M, Pastene LA (2001) Practical use of multiplex fluorescent PCR for cetacean sex identification. Mar Mammal Sci 17(3):657–664CrossRefGoogle Scholar
  2. Balloux F, Goudet J (2002) Statistical properties of population differentiation estimators under stepwise mutation in a finite island model. Mol Ecol 11:771–783PubMedCrossRefGoogle Scholar
  3. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48PubMedGoogle Scholar
  4. Beerli P (2004) Migrate Version 2.0: documentation and program, part of LAMARC. Revised 23/12/2004. Distributed over the Internet: http://evolution.gs.washington.edu/lamarc.htmlGoogle Scholar
  5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2001) Genetix, a Windows software for population Genetics. Laboratoire Génome, Populations, Interactions, CNRS UPR 9060. Université de Montpellier II, Montpellier, FranceGoogle Scholar
  6. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32:314–331PubMedGoogle Scholar
  7. Buchanan F, Friesen M, Littlejohn R, Clayton J (1996) Microsatellites from the beluga whale (Delphinapterus leucas). Mol Ecol 5:571–575PubMedCrossRefGoogle Scholar
  8. 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 12:1781–1792PubMedCrossRefGoogle Scholar
  9. Connor RC, Wells RS, Mann J (2000) The bottlenose dolphins: social relationships in a fission-fusion society. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Cetacean societies. Field studies of dolphins and whales. The University of Chicago Press, ChicagoGoogle Scholar
  10. Crandall KA (1996) Multiple interspecies transmissions of human and simian T-cell leukemia/lymphoma virus type I sequences. Mol Biol Evol 13(1):115–131PubMedGoogle Scholar
  11. DiRienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Nat Acad Sci USA 91:3166–3170CrossRefGoogle Scholar
  12. Excoffier L, Laval G, Schneider S (2005) Arlequin ver 3.0: An integrated software package for population genetics data analysis. Evol Bioinformatics Online 1:47–50Google Scholar
  13. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  14. Gaggiotti OE, Lange O, Rassmann K, Gliddon C (1999) A comparison of two indirect methods for estimating average levels of gene flow using microsatellite data. Mol Ecol 8(9):1513–1520PubMedCrossRefGoogle Scholar
  15. Gagneux P, Gonder MK, Goldberg TL, Morin PA (2001) Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time. Phil Trans R Soc London B 356:889–897CrossRefGoogle Scholar
  16. Gemmel NJ, Akiyama S (1996) An efficient method for the extraction of DNA from vertebrate tissues. TREE 12(9):338–339Google Scholar
  17. Goodman SJ (1997) RST CALC: A collection of computer programs for calculating unbiased estimates of genetic differentiation and determining their significance for microsatellite data. Mol Ecol 6:881–885CrossRefGoogle Scholar
  18. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from http://www.unil.ch/izea/softwares/fstat.htmlGoogle Scholar
  19. Hardy OJ, Vekemans X (2002) SPAGeDI: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  20. Hayano A, 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 21:989–999PubMedCrossRefGoogle Scholar
  21. Hoelzel AR, Hancock JM, Dover GA (1991) Evolution of the cetacean mitochondrial D-loop region. Mol Biol Evol 8(3):475–493PubMedGoogle Scholar
  22. Hoelzel AR, Dahlheim M, Stern SJ (1998a) Low genetic variation among killer whales (Orcinus orca) in the Eastern North Pacific and genetic differentiation between foraging specialists. J Hered 89:121–128CrossRefGoogle Scholar
  23. Hoelzel AR, Potter CW, Best PB (1998b) Genetic differentiation between parapatric ‘nearshore’ and ‘offshore’ populations of the bottlenose dolphin. Proc R Soc London B 265:1177–1183CrossRefGoogle Scholar
  24. Hoelzel AR, Goldsworthy SD, Fleischer RC (2002) Population genetic structure. In: Hoelzel AR (ed) Marine mammal biology. Blackwell Science Ltd, Oxford, UKGoogle Scholar
  25. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics, 61:893–903Google Scholar
  26. Knutsen H, Jorde PE, André C, Stenseth NC (2003) Fine-scaled geographic population structuring in a highly mobile marine species: the Atlantic cod. Mol Ecol 12:385–394PubMedCrossRefGoogle Scholar
  27. Krützen M, Valsecchi E, Connor RC, Sherwin WB (2001) Characterization of microsatellite loci in Tursiops aduncus. Mol Ecol Notes 1:170–172CrossRefGoogle Scholar
  28. Krützen M, Sherwin WB, Berggren P, Gales N (2004) Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia. Mar Mammal Sci 20(1):28–47CrossRefGoogle Scholar
  29. Marshall TC, Slate J, Kruuk L, Pemberton JM (1998) Statistical confidence for likelihood-based paternity inference in natural populations. Mol Ecol 7(5):639–655PubMedCrossRefGoogle Scholar
  30. Miller M (2005) Alleles In Space (AIS): Computer software for the joint analysis of interindividual spatial genetic information. J Hered 96:722–724PubMedCrossRefGoogle Scholar
  31. Möller LM, Beheregaray LB (2004) Genetic evidence for sex-biased dispersal in resident bottlenose dolphins (Tursiops truncatus). Mol Ecol 13:1607–1612PubMedCrossRefGoogle Scholar
  32. Natoli A, Peddemors VM, Hoelzel AR (2004) Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. J Evol Biol 17:363–375PubMedCrossRefGoogle Scholar
  33. Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus) based on microsatellite and mitochondrial DNA analyses. Proc R Soc London B 272:1217–1226CrossRefGoogle Scholar
  34. Natoli A, Cañadas A, Peddemors VM, Aguilar A, Vaquero C, Fernández-Piqueras P, Hoelzel AR (2006) Phylogeography and alpha taxonomy of the common dolphin (Delphinus sp.). J Evol Biol 19:943–954PubMedCrossRefGoogle Scholar
  35. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data II. Gene frequency data. J Mol Evol 19:153–170PubMedCrossRefGoogle Scholar
  36. Ohta T, Kimura M (1973) The model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a genetic population. Genetic Res 22:201–204CrossRefGoogle Scholar
  37. Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. PhD dissertation, University of DublinGoogle Scholar
  38. Parsons KM, Noble LR, Reid RJ, Thompson PM (2002) Mitochondrial genetic diversity and population structuring of UK bottlenose dolphins (Tursiops truncatus): is the NE Scotland population demographically and geographically isolated? Biol Conserv 108:175–182CrossRefGoogle Scholar
  39. Parsons KM, Durban JW, Claridge DE, Herzing DL, Balcomb KC, Noble LR (2006) Population genetic structure of coastal bottlenose dolphins (Tursiops truncatus) in the northern Bahamas. Mar Mamm Sci 22:276–298CrossRefGoogle Scholar
  40. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  41. Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  42. Richard KR, Whitehead H, Wright JM (1996) Polymorphic microsatellites from sperm whales and their use in the genetic identification of individuals from naturally sloughed pieces of skin. Mol Ecol 5:313–315PubMedCrossRefGoogle Scholar
  43. Ritland K. (2000) Marker-inferred relatedness as a tool for detecting heritability in nature. Mol Ecol 9:1195–1204PubMedCrossRefGoogle Scholar
  44. Rosel PE, Dizon AE, Heyning JE (1994) Genetic analysis of sympatric morphotypes of common dolphins (genus Delphinus). Mar Biol 119:159–167CrossRefGoogle Scholar
  45. Santos RS, Hawkins S, Monteiro LR, Alves M, Isidro EJ (1995) Case studies and reviews: Marine research, resources and conservation in the Azores. Aquat Conserv - Mar Freshw Ecosys 5:311–354CrossRefGoogle Scholar
  46. Segura I, Rocha-Olivares A, Flores-Ramírez S, Rojas-Bracho L (2006) Conservation implications of the genetic and ecological distinction of Tursiops truncatus ecotypes in the Gulf of California. Biol Conserv 133:336–346CrossRefGoogle Scholar
  47. Sellas AB, Wells RS, Rosel PE (2005) Mitochondrial and nuclear DNA analyses reveal fine scale geographic structure in bottlenose dolphins (Tursiops truncatus) in the Gulf of Mexico. Conserv Genet 6:715–728CrossRefGoogle Scholar
  48. Shaw PW, Pierce GJ, Boyle PR (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Mol Ecol 8:407–417CrossRefGoogle Scholar
  49. Shinohara M, Domingo-Roura X, Takenaka O (1997) Microsatellites in the bottlenose dolphin Tursiops truncatus. Mol Ecol 6:95–696CrossRefGoogle Scholar
  50. Silva MA (2006) Population biology of bottlenose dolphins in the Azores Archipelago. Unpublished PhD thesis. University of St AndrewsGoogle Scholar
  51. Silva MA, Prieto R, Magalhães S, Cabecinhas R, Cruz A, Gonçalves JM, Santos RS (2003) Occurrence and distribution of cetaceans in the waters around the Azores (Portugal), Summer and Autumn 1999–2000. Aquat Mammal 29(1):77–83CrossRefGoogle Scholar
  52. Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462PubMedGoogle 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. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  55. Torres LG, Rosel PE, D’Agrosa C, Read AJ (2003) Improving management of overlapping bottlenose dolphin ecotypes through spatial analysis and genetics. Mar Mamm Sci 19:502–514CrossRefGoogle Scholar
  56. Valsecchi E, Amos W (1996) Microsatellite markers for the study of cetacean populations. Mol Ecol 5:151–156PubMedGoogle Scholar
  57. Wang JY, Chou LS, White BN (1999) Mitochondrial DNA analysis of sympatric morphotypes of bottlenose dolphins (genus: Tursiops) in Chinese waters. Mol Ecol 8:1603–1612PubMedCrossRefGoogle Scholar
  58. Wang JY, Chou LS, White BN (2000) Osteological differences between two sympatric forms of bottlenose dolphins (genus Tursiops) in Chinese waters. J Zool Lond 252:147–162CrossRefGoogle Scholar
  59. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  60. Wells RS, Rhinehart HL, Cunningham P, Whaley J, Baran M, Koberna C, Costa DP (1999) Long distance offshore movements of bottlenose dolphins. Mar Mammal Sci 15:1098–1114CrossRefGoogle Scholar
  61. Wright S (1978) Evolution and the genetics of populations. Vol. 4: variability within and among natural populations. University of Chicago Press, ChicagoGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Sophie Quérouil
    • 1
    • 2
    • 3
  • Mónica A. Silva
    • 2
    • 4
  • Luís Freitas
    • 5
  • Rui Prieto
    • 2
  • Sara Magalhães
    • 2
  • Ana Dinis
    • 5
  • Filipe Alves
    • 5
  • José A. Matos
    • 3
  • Diogo Mendonça
    • 3
  • Philip S. Hammond
    • 4
  • Ricardo S. Santos
    • 2
  1. 1.UR175 CAVIARIRD–GAMETMontpellier Cedex 5France
  2. 2.Departamento de Oceanografia e PescasInstituto do Mar (IMAR) da Universidade dos AçoresHortaPortugal
  3. 3.INETI/Departamento de BiotecnologiaEdifício E - 1° andarLisboaPortugal
  4. 4.Sea Mammal Research Unit Gatty Marine LaboratoryUniversity of St. AndrewsSt. AndrewsScotland, UK
  5. 5.Museu da Baleia - Município de MachicoLargo Manuel AlvesCaniçalPortugal

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