Habitat-driven population structure of bottlenose dolphins, Tursiops truncatus, in the North-East Atlantic

Molecular Ecology

Volumn 23, Issue 4, 2014, Pages 857-874

  Louis, Marie ^a,b,c   Viricel, Amélia ^b   Lucas, Tamara ^b   Peltier, Hélène ^b   Alfonsi, Eric ^d,e   Berrow, Simon ^f,g   Brownlow, Andrew ^h   Covelo, Pablo ⁱ   Dabin, Willy ^b   Deaville, Rob ^j   De Stephanis, Renaud ^k   Gally, François ^c   Gauffier, Pauline ^l   Penrose, Rod ^m   Silva, Monica A ^n,o,p   Guinet, Christophe ^a   Simon Bouhet, Benoit ^b  

^a CENTRE D ETUDES BIOLOGIQUES DE CHIZÉ   (France)

^b UNIVERSITÉ DE LA ROCHELLE   (France)

^c Grp d'Etud des Cetaces du Cotentin   (France)

^d BioGemme Laboratory   (France)

^e UNIVERSITÉ EUROPÉENNE DE BRETAGNE   (France)

^f IRISH WHALE AND DOLPHIN GROUP   (Ireland)

^g Atlantic Technological University   (Ireland)

^h SAC Disease Surveillance Centre   (United Kingdom)

ⁱ SAC Disease Surveillance Centre ^*  (Spain)

^j INSTITUTE OF ZOOLOGY   (United Kingdom)

^k DEPARTMENT OF CONSERVATION BIOLOGY   (Spain)

^l CIRCE (Conservation   (Spain)

^m Marine Environmental Monitoring   (United Kingdom)

ⁿ UNIVERSITY OF THE AZORES   (Portugal)

^o Laboratory of Robotics and Systems in Engineering and Science   (Portugal)

^p WOODS HOLE OCEANOGRAPHIC INSTITUTION   (United States)

more..

Author keywords

cetaceans; conservation; ecotypes; feeding specializations; philopatry; population genetics

Indexed keywords

MICROSATELLITE DNA; MITOCHONDRIAL DNA;

ANIMAL; ARTICLE; ATLANTIC OCEAN; BOTTLENOSE DOLPHIN; CETACEANS; CONSERVATION; DNA SEQUENCE; ECOSYSTEM; ECOTYPES; FEEDING SPECIALIZATIONS; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHILOPATRY; POPULATION DENSITY; POPULATION GENETICS;

CETACEANS; CONSERVATION; ECOTYPES; FEEDING SPECIALIZATIONS; PHILOPATRY; POPULATION GENETICS;

ANIMALS; ATLANTIC OCEAN; BOTTLE-NOSED DOLPHIN; DNA, MITOCHONDRIAL; ECOSYSTEM; GENETIC VARIATION; GENETICS, POPULATION; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; POPULATION DENSITY; SEQUENCE ANALYSIS, DNA;

EID: 84893368595     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.12653     Document Type: Article

References (104)

1. Amaral AR, Beheregaray LB, Bilgmann K, Boutov D, Freitas L, (2012a) Seascape genetics of a globally distributed, highly mobile marine mammal: the short-beaked common dolphin (genus Delphinus). PLoS ONE, 7, e31482.
2. Amaral AR, Beheregaray LB, Bilgmann K, et al,. (2012b) Influences of past climatic changes on historical population structure and demography of a cosmopolitan marine predator, the common dolphin (genus Delphinus). Molecular Ecology, 21, 4854-4871.
3. Baker CS, Florez-Gonzalez L, Abernethy B, et al,. (1998) Mitochondrial DNA variation and maternal gene flow among humpback whales of the southern hemisphere. Marine Mammal Science, 14, 721-737.
4. Bandelt HJ, Forster P, Rohl A, (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37-48.
5. Begon M, Townsend CR, Harper JL, (2006) Ecology from Individuals to Ecosystems. Blackwell Pub, Malden, Massachusetts.
6. Bernatchez L, (1997) Mitochondrial DNA analysis confirms the existence of two glacial races of rainbow smelt Osmerus mordax and their reproductive isolation in the St Lawrence River estuary (Québec, Canada). Molecular Ecology, 6, 73-83.
7. Berrow S, O'Brien J, Groth L, Foley A, Voigh K, (2012) Abundance estimate of bottlenose dolphins (Tursiops truncatus) in the Lower River Shannon candidate Special Area of Conservation, Ireland. Aquatic Mammals, 38, 136-144.
8. Bilgmann K, Möller LM, Harcourt RG, Kemper CM, Beheregaray LB, (2011) The use of carcasses for the analysis of cetacean population genetic structure: a comparative study in two dolphin species. PLoS ONE, 6, e20103.
9. de Bruyn PJN, Tosh CA, Terauds A, (2013) Killer whale ecotypes: is there a global model? Biological Reviews, 88, 62-80.
10. Cantor M, Whitehead H, (2013) The interplay between social networks and culture: theoretically and among whales and dolphins. Philosophical Transactions of the Royal Society. B, Biological Sciences, 368, 20120340.
11. Certain G, Ridoux V, van Canneyt O, Bretagnolle V, (2008) Delphinid spatial distribution and abundance estimates over the shelf of the Bay of Biscay. Ices Journal of Marine Science, 64, 656-666.
12. Chen C, Durand E, Forbes F, Francois O, (2007) Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study. Molecular Ecology Notes, 7, 747-756.
13. Cheney B, Culloch RM, Durban JW, et al,. (2012) Integrating multiple data sources to assess the distribution and abundance of bottlenose dolphins Tursiops truncatus in Scottish waters. Mammal Review, 42, 71-88.
14. Curry BE, Smith J, (1998) Phylogeographic structure of the bottlenose dolphin (Tursiops truncatus): stock identification and implications for management. In: Molecular Genetics of Marine Mammals (eds, Dizon AE, Chivers SJ, Perrin WF,), pp. 227-247. The Society for Marine Mammalogy, Special Publication 3, Lawrence, Kansas.
15. Dalebout ML, Robertson KM, Frantzis A, et al,. (2005) Worldwide structure of mtDNA diversity among Cuvier's beaked whales (Ziphius cavirostris): implications for threatened populations. Molecular Ecology, 14, 3353-3371.
16. Dionne M, Caron F, Dodson JJ, Bernatchez L, (2008) Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Molecular Ecology, 17, 2382-2396.
17. Durand E, Chen E, Francois O, (2009a) Tess Version 2.3-Reference Manual.
18. Durand E, Jay F, Gaggiotti OE, Francois O, (2009b) Spatial inference of admixture proportions and secondary contact zones. Molecular Biology and Evolution, 26, 1963-1973.
19. Earl DA, Vonholdt BM, (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources, 4, 359-361.
20. Emlen ST, Oring LW, (1977) Ecology, sexual selection and the evolution of mating systems. Science, 197, 215-223.
21. Evanno G, Regnaut S, Goudet J, (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611-2620.
22. Fernandez R, Santos MB, Pierce GJ, et al,. (2011) Fine-scale genetic structure of bottlenose dolphins, Tursiops truncatus, in Atlantic coastal waters of the Iberian Peninsula. Hydrobiologia, 670, 111-125.
23. Fontaine MC, Baird SJE, Piry S, et al,. (2007) Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters. BMC Biology, 5, 30.
24. Foote AD, Vilstrup JT, de Stephanis R, et al,. (2011) Genetic differentiation among North Atlantic killer whale populations. Molecular Ecology, 20, 629-641.
25. Forcada J, Gazo M, Aguilar A, Gonzalvo J, Fernandez-Contreras M, (2004) Bottlenose dolphin abundance in the NW Mediterranean: addressing heterogeneity in distribution. Marine Ecology Progress Series, 275, 275-287.
26. Gaggiotti OE, Bekkevold D, Jorgensen HBH, et al,. (2009) Disentangling the effects of evolutionary, demographic, and environmental factors influencing genetic structure of natural populations: atlantic herring as a case study. Evolution, 63, 2939-2951.
27. Glaubitz JC, (2004) CONVERT: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes, 4, 309-310.
28. Gnone G, Bellingeri M, Dhermain F, et al,. (2011) Distribution, abundance, and movements of the bottlenose dolphin (Tursiops truncatus) in the Pelagos Sanctuary MPA (north-west Mediterranean Sea). Aquatic Conservation-Marine and Freshwater Ecosystems, 21, 372-388.
29. Goudet J, (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. Journal of Heredity, 86, 485-486.
30. Goudet J, Perrin N, Waser P, (2002) Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Molecular Ecology, 11, 1103-1114.
31. Greenwood PJ, (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour, 28, 1140-1162.
32. Guillot G, Leblois R, Coulon A, Frantz AC, (2009) Statistical methods in spatial genetics. Molecular Ecology, 18, 4734-4756.
33. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704.
34. Hall TA, (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.
35. Hammond PS, Macleod K, Gillespie D, et al,. (2009) Cetacean Offshore Distribution and Abundance in the European Atlantic (CODA). Final report to the European Commission. St Andrews: Sea Mammal Research Unit, 42 pp.
36. Hammond PS, Macleod K, Berggren P, et al,. (2013) Cetacean abundance and distribution in European Atlantic shelf waters to inform conservation and management. Biological Conservation, 64, 107-122.
37. Hare MP, Nunney L, Schwartz MK, et al,. (2011) Understanding and estimating effective population size for practical application in marine species management. Conservation Biology, 25, 438-449.
38. Hijmans RJ, Williams E, Vennes C, (2012) geosphere: Spherical Trigonometry. R package version 1.2-28. http://CRAN.R-project.org/package= geosphere.
39. 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. Journal of Heredity, 89, 121-128.
40. Hoelzel AR, Potter CW, Best PB, (1998b) 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.
41. Hoffman EA, Kolm N, Berglund A, Arguello JR, Jones AG, (2005) Genetic structure in the coral-reef-associated Banggai cardinalfish, Pterapogon kauderni. Molecular Ecology, 14, 1367-1375.
42. Holm S, (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics, 6, 65-70.
43. Jombart T, (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics, 24, 1403-1405.
44. Jombart T, Devillard S, Balloux F, (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11, 94.
45. Kawecki TJ, Ebert D, (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225-1241.
46. Konovalov DA, Manning C, Henshaw MT, (2004) KINGROUP: a program for pedigree relationship reconstruction and kin group assignments using genetic markers. Molecular Ecology Notes, 4, 779-782.
47. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE, (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conservation Genetics, 7, 295-302.
48. Lõpez A, (2003) Estatus dos pequenos cetáceos da plataforma de Galicia. PhD dissertation, Universidade de Santiago de Compostela.
49. Lowry DB, (2012) Ecotypes and the controversy over stages in the formation of new species. Biological Journal of the Linnean Society, 106, 241-257.
50. Mace GM, Lande R, (1991) Assessing extinction threats-towards a reevaluation of IUCN threatened species categories. Conservation Biology, 5, 148-157.
51. Martien KK, Baird RW, Hedrick NM, et al,. (2011) Population structure of island-associated dolphins: evidence from mitochondrial and microsatellite markers for common bottlenose dolphins (Tursiops truncatus) around the main Hawaiian Islands. Marine Mammal Science, 28, 208-232.
52. Mead JC, Potter CW, (1995) Recognizing two populations of the bottlenose dolphin (Tursiops truncatus) of the Atlantic coast of North America-morphologic and ecologic considerations. IBI Reports (International Marine Biological Research Institute, Kamogawa, Japan), 5, 31-44.
53. Michalakis Y, Excoffier L, (1996) A generic estimation of population subdivision using distances between alleles with special reference for microsatellite loci. Genetics, 142, 1061-1064.
54. Mirimin L, Miller R, Dillane E, et al,. (2011) Fine-scale population genetic structuring of bottlenose dolphins in Irish coastal waters. Animal Conservation, 14, 342-353.
55. Möller LM, (2011) Sociogenetic structure, kin associations and bonding in delphinids. Molecular Ecology, 21, 745-764.
56. Möller L, Valdez FP, Allen S, et al,. (2011) Fine-scale genetic structure in short-beaked common dolphins (Delphinus delphis) along the East Australian Current. Marine Biology, 158, 113-126.
57. Musiani M, Leonard JA, Cluff HD, et al,. (2007) Differentiation of tundra/taiga and boreal coniferous forest wolves: genetics, coat colour and association with migratory caribou. Molecular Ecology, 16, 4149-4170.
58. Natoli A, Peddemors VM, Hoelzel AR, (2004) Population structure and speciation in the genus Tursiops based on microsatellite and mitochondrial DNA analyses. Journal of Evolutionary Biology, 17, 363-375.
59. Natoli A, Birkun A, Aguilar A, Lopez A, Hoelzel AR, (2005) Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society. B, Biological Sciences, 272, 1217-1226.
60. Nichols C, Herman J, Gaggiotti OE, et al,. (2007) Genetic isolation of a now extinct population of bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society. B, Biological Sciences, 274, 1611-1616.
61. O'Brien JM, Berrow SD, Ryan C, et al,. (2009) A note on long-distance matches of bottlenose dolphins (Tursiops truncatus) around the Irish coast using photo-identification. Journal of Cetacean Research and Management, 11, 71-76.
62. Palstra FP, Ruzzante DE, (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Molecular Ecology, 17, 3428-3447.
63. Pante E, Simon-Bouhet B, (2013) Marmap: a package for importing, plotting and analyzing bathymetric and topographic data in R. PLoS ONE, 8, e73051.
64. Peltier H, Dabin W, Daniel P, et al,. (2012) The significance of stranding data as indicators of cetacean populations at sea: modelling the drift of cetacean carcasses. Ecological Indicators, 18, 278-290.
65. Perrin WF, Thieleking JL, Walker WA, Archer FI, Robertson KM, (2011) Common bottlenose dolphins (Tursiops truncatus) in California waters: cranial differentiation of coastal and offshore ecotypes. Marine Mammal Science, 27, 769-792.
66. Pesante G, Evans PGH, Baines ME, McMath M, (2008) Abundance and life history parameters of bottlenose dolphin in Cardigan Bay: monitoring 2005-2007. CCW Marine Monitoring Report 61, 75 pp.
67. Pilot M, Jedrzejewski W, Sidorovich VE, Meier-Augenstein W, Hoelzel AR, (2012) Dietary differentiation and the evolution of population genetic structure in a highly mobile carnivore. PLoS ONE, 7, e39341.
68. Pirotta E, Laesser EV, Hardaker A, et al,. (2013) Dredging displaces bottlenose dolphins from an urbanised foraging patch. Marine Pollution Bulletin, 14, 396-402.
69. Pritchard JK, Stephens M, Donnelly P, (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945-959.
70. Queller DC, Goodnight KF, (1989) Estimating relatedness using genetic markers. Evolution, 43, 258-275.
71. Quérouil S, Silva MA, Freitas L, et al,. (2007) High gene flow in oceanic bottlenose dolphins (Tursiops truncatus) of the North Atlantic. Conservation Genetics, 8, 1405-1419.
72. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
73. Raymond M, Rousset F, (1995) GENEPOP (version 1.2)-Population genetics software for exact tests and ecumenicism. Journal of Heredity, 86, 248-249.
74. Robinson JD, Moyer GR, (2013) Linkage disequilibrium and effective population size when generations overlap. Evolutionary Applications, 6, 290-302.
75. Robinson KP, O'Brien J, Berrow SD, et al,. (2012) Discrete or not so discrete: long distance movements by coastal bottlenose dolphins in UK and Irish waters. Journal of Cetacean Research and Management, 12, 365-371.
76. Rosel PE, (2003) PCR-based sex determination in Odontocete cetaceans. Conservation Genetics, 4, 647-649.
77. Rosel PE, Hansen L, Hohn AA, (2009) Restricted dispersal in a continuously distributed marine species: common bottlenose dolphins Tursiops truncatus in coastal waters of the western North Atlantic. Molecular Ecology, 18, 5030-5045.
78. Rozas J, Rozas R, (1999) DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics, 15, 174-175.
79. Sacks BN, Mitchell BR, Williams CL, Ernest HB, (2005) Coyote movements and social structure along a cryptic population genetic subdivision. Molecular Ecology, 14, 1241-1249.
80. Santos MB, Pierce GJ, Reid RJ, et al,. (2001) Stomach contents of bottlenose dolphins (Tursiops truncatus) in Scottish waters. Journal of the Marine Biological Association of the United Kingdom, 81, 873-878.
81. Sargeant BL, Mann J, (2009) Developmental evidence for foraging traditions in wild bottlenose dolphins. Animal Behaviour, 78, 715-721.
82. Segura I, Rocha-Olivares A, Flores-Ramirez S, Rojas-Bracho L, (2006) Conservation implications of the genetic and ecological distinction of Tursiops truncatus ecotypes in the Gulf of California. Biological Conservation, 133, 336-346.
83. 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. Conservation Genetics, 6, 715-728.
84. Serrouya R, Paetkau D, McLellan BN, et al,. (2012) Population size and major valleys explain microsatellite variation better than taxonomic units for caribou in western Canada. Molecular Ecology, 21, 2588-2601.
85. Silva MA, Prieto R, Magalhaes S, et al,. (2008) Ranging patterns of bottlenose dolphins living in oceanic waters: implications for population structure. Marine Biology, 156, 179-192.
86. Skrbinsek T, Jelencic M, Waits L, et al,. (2012) Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches. Molecular Ecology, 21, 862-875.
87. Spitz J, Rousseau Y, Ridoux V, (2006) Diet overlap between harbour porpoise and bottlenose dolphin: an argument in favour of interference competition for food? Estuarine Coastal and Shelf Science, 70, 259-270.
88. de Stephanis R, Cornulier T, Verborgh P, et al,. (2008) Summer spatial distribution of cetaceans in the Strait of Gibraltar in relation to the oceanographic context. Marine Ecology Progress Series, 353, 275-288.
89. Tallmon DA, Koyuk A, Luikart G, Beaumont MA, (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Molecular Ecology Resources, 8, 299-301.
90. Tallmon DA, Gregovich D, Waples RS, et al,. (2010) When are genetic methods useful for estimating contemporary abundance and detecting population trends? Molecular Ecology Resources, 10, 684-692.
91. Tamura K, Nei M, (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution, 10, 512-526.
92. Tezanos-Pinto G, Baker CS, Russell K, et al,. (2009) A worldwide perspective on the population structure and genetic diversity of bottlenose dolphins (Tursiops truncatus) in New Zealand. Journal of Heredity, 100, 11-24.
93. Thorpe RS, Reardon JT, Malhotra A, (2005) Common garden and natural selection experiments support ecotypic differentiation in the Dominican anole (Anolis oculatus). American Naturalist, 165, 495-504.
94. Turesson G, (1922a) The genotypical response of the plant species to the habitat. Hereditas, 3, 211-350.
95. Turesson G, (1922b) The species and the variety as ecological units. Hereditas, 3, 100-113.
96. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P, (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535-538.
97. Walker WA, (1981) Geographic variation in morphology and biology of bottlenose dolphins (Tursiops) in the eastern North Pacific. NOAA/NMFS Administrative Report LJ-81-0003c, 21 pp.
98. Waples RS, (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Molecular Ecology, 14, 3335-3352.
99. Waples RS, (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Molecular Ecology Resources, 10, 785-796.
100. Waples RS, Do C, (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Molecular Ecology Resources, 8, 753-756.
101. Waples RS, Do C, (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evolutionary Applications, 3, 244-262.
102. Waples RS, England PR, (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics, 189, 633-644.
103. Wells R, Scott MD, (1999) Bottlenose dolphin Tursiops truncatus (Montagu, 1821). In: Handbook of Marine Mammals (eds, Ridgway SH, Harrison R,), pp. 137-182. Academic Press, San Diego.
104. Wilson GA, Rannala B, (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics, 163, 1177-1191.