Genetic diversity from pre-bottleneck to recovery in two sympatric pinniped species in the Northwest Atlantic

Abstract

Conservation successes of the past several decades provide natural settings to study post-bottleneck evolutionary processes in species undergoing recovery. Here, we study the impact of demographic change on genetic diversity in parallel natural experiments of historical decline and subsequent recovery in two sympatric pinniped species in the Northwest Atlantic, the gray seal (Halichoerus grypus atlantica) and harbor seal (Phoca vitulina concolor). We compare genetic diversity at the mitochondrial control region today to diversity in archaeological specimens, which represent the populations prior to the regional bounties of the late 1800s to mid-1900s that drastically reduced population sizes and led to local extirpations. We further assess genetic diversity throughout recovery, using biological collections from ongoing long-term studies of both species. Overall, the genetic data are consistent with the historical presence of large, genetically diverse populations of pinnipeds prior to human exploitation, and suggest that gray seals were more dramatically impacted by historical bottlenecks than harbor seals in the Northwest Atlantic. Current mitochondrial diversity in both species is relatively high, and we observe little change over the past several decades during a period of roughly parallel rapid population increases. However, there remain large differences in haplotype composition between pinniped populations of pre-exploitation and today, a lasting genetic signature of historical exploitation that is likely to persist into the future.

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References

  1. Alter SE, Newsome SD, Palumbi SR (2012) Pre-whaling genetic diversity and population ecology in eastern Pacific gray whales: insights from ancient DNA and stable isotopes. PLoS ONE 7:e35039

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Amos W, Balmford A (2001) When does conservation genetics matter? Heredity 87:257–265

    Article  PubMed  CAS  Google Scholar 

  3. Andersen LW, Lydersen C, Frie AK et al (2011) A population on the edge: genetic diversity and population structure of the world’s northernmost harbour seals (Phoca vitulina). Biol J Linn Soc Lond 102:420–439

    Article  Google Scholar 

  4. Baker CS, Perry A, Bannister JL et al (1993) Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc Natl Acad Sci USA 90:8239–8243

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Boskovic R, Kovacs KM, Hammill MO, White BN (1996) Geographic distribution of mitochondrial DNA haplotypes in grey seals (Halichoerus grypus). Can J Zool 74:1787–1796

    Article  CAS  Google Scholar 

  6. Bowen WD, Lidgard D (2013) Marine mammal culling programs: review of effects on predator and prey populations. Mamm Rev 43:207–220

    Article  Google Scholar 

  7. Bowen WD, Ellis SL, Iverson SJ, Boness DJ (2003a) Maternal and newborn life-history traits during periods of contrasting population trends: implications for explaining the decline of harbour seals (Phoca vitulina), on Sable Island. J Zool 261:155–163

    Article  Google Scholar 

  8. Bowen WD, McMillan J, Mohn R (2003b) Sustained exponential population growth of grey seals at Sable Island, Nova Scotia. ICES J Mar Sci 60:1265–1274

    Article  Google Scholar 

  9. Bowen WD, McMillan JI, Blanchard W (2007) Reduced population growth of gray seals at Sable Island: evidence from pup production and age of primiparity. Mar Mamm Sci 23:48–64

    Article  Google Scholar 

  10. Bowen WD, den Heyer C, McMillan JI, Hammill MO (2011) Pup production at Scotian shelf grey seal (Halichoerus grypus) colonies in 2010. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2011/066

  11. Braje TJ, Rick TC (2011) Human impacts on seals, sea lions, and sea otters: integrating archaeology and ecology in the Northeast Pacific. University of California Press, Berkeley

    Google Scholar 

  12. Caro TM, Laurenson MK (1994) Ecological and genetic factors in conservation: a cautionary tale. Science 263:485–486

    Article  PubMed  CAS  Google Scholar 

  13. Chassin-Noria O, Abreu-Grobois A, Dutton PH, Oyama K (2004) Conservation genetics of the east Pacific green turtle (Chelonia mydas) in Michoacan, Mexico. Genetica 121:195–206

    Article  PubMed  CAS  Google Scholar 

  14. Collins CJ, Rawlence NJ, Prost S et al (2014) Extinction and recolonization of coastal megafauna following human arrival in New Zealand. Proc R Soc Lond B 281:20140097

    Article  Google Scholar 

  15. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. de Bruyn M, Hall BL, Chauke LF et al (2009) Rapid response of a marine mammal species to Holocene climate and habitat change. PLoS Genet 5:e1000554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. den Heyer CE, Lang SLC, Bowen WD, Hammill MO (2017) Pup production at Scotian shelf grey seal (Halichoerus grypus) colonies in 2016. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2016/nnn

  18. Dickerson BR, Ream RR, Vignieri SN, Bentzen P (2010) Population structure as revealed by mtDNA and microsatellites in Northern fur seals, Callorhinus ursinus, throughout their range. PLoS ONE 5:e10671

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. 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

    Article  PubMed  CAS  Google Scholar 

  20. Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Evans S, Godino IB, Álvarez M et al (2016) Using combined biomolecular methods to explore whale exploitation and social aggregation in hunter-gatherer-fisher society in Tierra del Fuego. J Arch Sci Rep 6:757–767

    Google Scholar 

  22. Ewonus PA, Cannon A, Yang DY (2011) Addressing seasonal site use through ancient DNA species identification of Pacific salmon at Dionisio Point, Galiano Island, British Columbia. J Arch Sci 38:2536–2546

    Article  Google Scholar 

  23. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  24. Fietz K, Graves JA, Olsen MT (2013) Control control control: a reassessment and comparison of GenBank and chromatogram mtDNA sequence variation in Baltic grey seals (Halichoerus grypus). PLoS ONE 8:e72853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Fietz K, Galatius A, Teilmann J et al (2016) Shift of grey seal subspecies boundaries in response to climate, culling and conservation. Mol Ecol 25:4097–4112

    Article  PubMed  Google Scholar 

  26. Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63

    Article  Google Scholar 

  27. Gaggiotti OE, Jones F, Lee WM et al (2002) Patterns of colonization in a metapopulation of grey seals. Nature 416:424–427

    Article  PubMed  CAS  Google Scholar 

  28. Gilbert JR, Waring GT, Wynne KM, Guldager N (2005) Changes in abundance of harbor seals in Maine, 1981–2001. Mar Mamm Sci 21:519–535

    Article  Google Scholar 

  29. Gilbert MTP, Binladen J, Miller W et al (2007) Recharacterization of ancient DNA miscoding lesions: insights in the era of sequencing-by-synthesis. Nucleic Acids Res 35:1–10

    Article  PubMed  CAS  Google Scholar 

  30. Goodall-Copestake WP, Tarling GA, Murphy EJ (2012) On the comparison of population-level estimates of haplotype and nucleotide diversity: a case study using the gene cox1 in animals. Heredity 109:50–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Goodman SJ (1998) Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using microsatellite DNA polymorphisms. Mol Biol Evol 15:104–118

    Article  PubMed  CAS  Google Scholar 

  32. Hailer F, Helander B, Folkestad AO et al (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319

    Article  PubMed  PubMed Central  Google Scholar 

  33. Hall A, Kershaw J (2012) Review of the status, trends and potential causes for the decline in abundance of harbour seals around the coast of Scotland. Sea Mammal Research Unit. Marine Mammal Scientific Support Research Programme MMSS/001/11

  34. Hammill MO, Gosselin JF, Stenson GB (2007) Abundance of Northwest Atlantic grey seals in Canadian waters. NAMMCO Sci Publ 6:99–115

    Article  Google Scholar 

  35. Hammill MO, den Heyer CE, Bowen WD (2014) Grey seal population trends in Canadian waters, 1960–2014. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2014/037

  36. Hansson B, Bensch S, Hasselquist D et al (2000) Increase of genetic variation over time in a recently founded population of great reed warblers (Acrocephalus arundinaceus) revealed by mirosatellites and DNA fingerprinting. Mol Ecol 9:1529–1538

    Article  PubMed  CAS  Google Scholar 

  37. Hasagawa M, Kishino H, Yano T (1985) Dating the human-ape splitting by molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  Google Scholar 

  38. Hoffman JI, Grant SM, Forcada J, Phillips CD (2011) Bayesian inference of a historical bottleneck in a heavily exploited marine mammal. Mol Ecol 20:3989–4008

    Article  PubMed  CAS  Google Scholar 

  39. Hofreiter M, Jaenicke V, Serre D, von Haeseler A, Pääbo S (2001a) DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res 29:4793–4799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Hofreiter M, Serre D, Poinar HN, Kuch M, Pääbo S (2001b) Ancient DNA. Nat Rev Genet 2:353–359

    Article  PubMed  CAS  Google Scholar 

  41. Ingraham RC, Robinson BS, Sobolik KD, Heller AS (2015) “Left for the tide to take back”: specialized processing of seals on Machias Bay, Maine. J Isl Coast Archaeol 11:89–106

    Article  Google Scholar 

  42. Irwin DL, Mitchelson KR, Findlay I (2003) PCR product cleanup methods for capillary electrophoresis. Biotechniques 34:932–936

    PubMed  CAS  Article  Google Scholar 

  43. Jensen J (2003) The prehistory of Denmark. Routledge, London

    Google Scholar 

  44. Johnson WE, Onorato DP, Roelke ME et al (2010) Genetic restoration of the Florida panther. Science 329:1641–1645

    Article  PubMed  CAS  Google Scholar 

  45. Johnston DW, Frungillo J, Smith A et al (2015) Trends in stranding and by-catch rates of gray and harbor seals along the northeastern coast of the United States: evidence of divergence in the abundance of two sympatric phocid species? PLoS ONE 10:e0131660

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  47. Katona SK, Rough V, Richardson DT (1993) A field guide to whales, dolphins, and seals from Cape Cod to Newfoundland, 4th edn. Smithsonian Institution Press, Washington

    Google Scholar 

  48. Keller LF, Jeffery KJ, Arcese P et al (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc R Soc Lond B 268:1387–1394

    Article  CAS  Google Scholar 

  49. Klimova A, Phillips CD, Fietz K et al (2014) Global population structure and demographic history of the grey seal. Mol Ecol 23:3999–4017

    Article  PubMed  CAS  Google Scholar 

  50. Lamb T, Lydeard C, Walker RB, Gibbons JW (1994) Molecular systematics of map turtles (Graptemys): a comparison of mitochondrial restriction site versus sequence data. Syst Biol 43:543–559

    Article  Google Scholar 

  51. Larson S, Jameson R, Etnier M, Fleming M, Bentzen P (2002) Loss of genetic diversity in sea otters (Enhydra lutris) associated with the fur trade of the 18th and 19th centuries. Mol Ecol 11:1899–1903

    Article  PubMed  CAS  Google Scholar 

  52. Lavigueur L, Hammill MO (1993) Distribution and seasonal movements of grey seals, Halichoerus grypus, born in the Gulf of St. Lawrence and eastern Nova Scotia shore. Can Field-Nat 107:329–340

    Google Scholar 

  53. Lawson JW, Renouf D (1985) Parturition in the Atlantic harbor seal, Phoca vitulina concolor. J Mamm 66:395–398

    Article  Google Scholar 

  54. Lelli B, Harris DE, Aboueissa A-M (2009) Seal bounties in Maine and Massachusetts, 1888 to 1962. Northeast Nat 16:239–254

    Article  Google Scholar 

  55. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  PubMed  CAS  Google Scholar 

  56. Lotze HK, Coll M, Magera AM, Ward-Paige C, Airoldi L (2011) Recovery of marine animal populations and ecosystems. Trends Ecol Evol 26:595–603

    Article  PubMed  Google Scholar 

  57. Magera AM, Mills Flemming JE, Kaschner K, Christensen LB, Lotze HK (2013) Recovery trends in marine mammal populations. PLoS ONE 8:e77908

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  58. McInerney P, Adams P, Hadi MZ (2014) Error rate comparison during polymerase chain reaction by DNA polymerase. Mol Biol Int 2014:287430

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. McLeod BA, Brown MW, Moore MJ et al (2008) Bowhead whales, and not right whales, were the primary target of 16th- to 17th-century Basque whalers in the western North Atlantic. Arctic 61:61–75

    Article  Google Scholar 

  60. McLeod BA, Frasier TR, Lucas Z (2014) Assessment of the extirpated Maritimes walrus using morphological and ancient DNA analysis. PLoS ONE 9:e99569

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Miller PS, Hedrick PW (2001) Purging of inbreeding depression and fitness decline in bottlenecked populations of Drosophila melanogaster. J Evol Biol 14:595–601

    Article  Google Scholar 

  62. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10

    Article  PubMed  Google Scholar 

  63. Noren SR, Boness DJ, Iverson SJ, McMillan J, Bowen WD (2008) Body condition at weaning affects the duration of the postweaning fast in gray seal pups (Halichoerus grypus). Physiol Biochem Zool 81:269–277

    Article  PubMed  Google Scholar 

  64. O’Brien SJ, Roelke ME, Marker L et al (1985) Genetic basis for species vulnerability in the cheetah. Science 227:1428–1434

    Article  PubMed  Google Scholar 

  65. Pääbo S, Poinar H, Serre D et al (2004) Genetic analyses from ancient DNA. Annu Rev Genet 38:645–679

    Article  PubMed  CAS  Google Scholar 

  66. Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  PubMed  CAS  Google Scholar 

  67. Parsons TJ, Muniec DS, Sullivan K et al (1997) A high observed substiution rate in the human mitochondrial DNA control region. Nat Genet 15:363–368

    Article  PubMed  CAS  Google Scholar 

  68. Phillips CD, Turjillo RG, Gelatt TS et al (2009) Assessing substitution patterns, rates and homoplasy at HVRI of Steller sea lions, Eumetopias jubatus. Mol Ecol 18:3379–3393

    Article  PubMed  CAS  Google Scholar 

  69. Pinsky ML, Newsome SD, Dickerson BR et al (2010) Dispersal provided resilience to range collapse in a marine mammal: insights from the past to inform conservation biology. Mol Ecol 19:2418–2429

    PubMed  CAS  Google Scholar 

  70. Prost S, Anderson CNK (2011) TempNet: a method to display statistical parsimony networks for heterochronous DNA sequence data. Methods Ecol Evol 2:663–667

    Article  Google Scholar 

  71. Rambaut A, Ho SYW, Drummond AJ, Shapiro B (2009) Accommodating the effect of ancient DNA damage on inferences of demographic histories. Mol Biol Evol 26:245–248

    Article  PubMed  CAS  Google Scholar 

  72. Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) Tracer v1.6. http://beast.bio.ed.ac.uk/Tracer. Accessed 1 Feb 2017

  73. Rawlence NJ, Collins CJ, Anderson CNK et al (2016) Human-mediated extirpation of the unique Chatham Islands sea lion and implications for the conservation management of remaining New Zealand sea lion populations. Mol Ecol 25:3950–3961

    Article  PubMed  CAS  Google Scholar 

  74. Reitz EJ (2004) “Fishing down the food web”: a case study from St. Augustine, Florida, USA. Am Antiq 69:63–83

    Article  Google Scholar 

  75. Richardson DT (1976) Assessment of harbor seal and gray seal populations in Maine 1974–1975. Report to the Marine Mammal Commission Contract No. MM4AC009

  76. Robinson BS, Jacobson GL, Yates MG, Spiess AE, Cowie ER (2009) Atlantic salmon, archaeology and climate change in New England. J Arch Sci 36:2184–2191

    Article  Google Scholar 

  77. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  78. Rough V (1991) Muskeget gray seals, winter and spring, 1991. Report to the Marine Mammal Commission

  79. Saccheri IJ, Brakefield PM, Nichols RA (1996) Severe inbreeding depression and rapid fitness rebound in the butterfly Bicyclus anynana (Satyridae). Evolution 50:2000–2013

    Article  PubMed  Google Scholar 

  80. Salis AT, Easton LJ, Robertson BC et al (2016) Myth or relict: Does ancient DNA detect the enigmatic Upland seal? Mol Phylogenet Evol 97:101–106

    Article  PubMed  Google Scholar 

  81. Savage AE, Becker CG, Zamudio KR (2015) Linking genetic and environmental factors in amphibian disease risk. Evol Appl 8:560–572

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Sjare B, Lebeuf M, Veinott G (2005) Harbour seals in Newfoundland and Labrador: a preliminary summary of new data on aspects of biology, ecology and contaminant profiles. Fisheries and Oceans Canada. Canadian Science Advisory Secretariat Research Document 2005/030

  83. Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  PubMed Central  CAS  Google Scholar 

  84. Speck GF (1935) Penobscot tales and religious beliefs. J Am Folklore 48:1–107

    Article  Google Scholar 

  85. Spiess AE, Lewis RA (2001) The Turner Farm fauna: 5000 years of hunting and fishing in Penobscot Bay, ME. Occas Publ Maine Archaeol 11:177

    Google Scholar 

  86. Stanley HF, Casey S, Carnahan JM et al (1996) Worldwide patterns of mitochondrial DNA differentiation in the harbor seal (Phoca vitulina). Mol Biol Evol 13:368–382

    Article  PubMed  CAS  Google Scholar 

  87. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Thomas MG, Weale ME, Jones AL et al (2002) Founding mothers of Jewish communities: geographically separated Jewish groups were independently founded by very few female ancestors. Am J Hum Genet 70:1411–1420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  89. Waring GT, Josephson E, Maze-Foley K, Rosel PE (2016) US Atlantic and Gulf of Mexico marine mammal stock assessments—2015. NOAA Tech Memo NMFS-NE-238

  90. Weale ME (2003) TEST_h_DIFF: testing for differences in h between two populations. http://www.ucl.ac.uk/mace-lab/resources/software. Accessed 10 Apr 2017

  91. Weber DS, Stewartt BS, Garza JC, Lehman N (2000) An empirical assessment of the severity of the northern elephant seal population bottleneck. Curr Biol 10:1287–1290

    Article  PubMed  CAS  Google Scholar 

  92. Weber DS, Stewart BS, Lehman N (2004) Genetic consequences of a severe population bottleneck in the Guadelupe fur seal (Arctocephalus townsendi). J Hered 95:144–153

    Article  PubMed  CAS  Google Scholar 

  93. Westemeier RL, Brawn JD, Simpson SA et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    Article  PubMed  CAS  Google Scholar 

  94. Wood SA, Frasier TR, McLeod BA et al (2011) The genetics of recolonization: an analysis of the stock structure of grey seals (Halichoerus grypus) in the Northwest Atlantic. Can J Zool 89:490–497

    Article  Google Scholar 

  95. Wood LaFond SA (2009) Dynamics of recolonization: a study of the gray seal (Halichoerus grypus) in the Northeast U.S. Dissertation, University of Massachusetts, Boston

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Acknowledgements

We thank the following individuals who helped with access to sample archives or ongoing collections: Christine Bubac, Johanne Guerin, Matthew Harnden, Nell den Heyer, Elizabeth Josephson, and Gordon Waring. We also thank Mike Simpkins, Per Palsbøll, Morten Tange Olsen, and an anonymous reviewer for their thoughtful feedback on the manuscript. The import/export of seal samples between Canada and the United States was conducted under NOAA Permit No. 17670-03 (issued to the NMFS Northeast Fisheries Science Center) and authorization from the NOAA National Marine Fisheries Service and Greater Atlantic Regional Fisheries Office (issued to Brian Robinson). Funding for the fieldwork was provided by the Department of Fisheries and Oceans Canada, Natural Sciences and Engineering Research Council of Canada, NOAA Northeast Fisheries Science Center, Northeast Fisheries Observer Program, and the NIH/NIAID Centers of Excellence for Influenza Research and Surveillance (HHSN272201400008C). K.M.C. was supported by a National Science Foundation Postdoctoral Research Fellowship in Biology under Grant No. 1523568. We are grateful to Brian Robinson’s early contributions to the work, through animated discussion, liaising with the Passamaquoddy Tribe, and providing access to his archaeological collections. Brian passed away prior to the completion of this work; we mourn his loss but continue to appreciate his lasting contributions to archaeology in Maine.

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Correspondence to Kristina M. Cammen.

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Cammen, K.M., Vincze, S., Heller, A.S. et al. Genetic diversity from pre-bottleneck to recovery in two sympatric pinniped species in the Northwest Atlantic. Conserv Genet 19, 555–569 (2018). https://doi.org/10.1007/s10592-017-1032-9

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Keywords

  • Halichoerus grypus
  • Phoca vitulina
  • Mitochondrial control region
  • Ancient DNA