Conservation Genetics

, Volume 12, Issue 6, pp 1435–1446 | Cite as

Genetically effective population sizes of Antarctic seals estimated from nuclear genes

  • Caitlin Curtis
  • Brent S. Stewart
  • Stephen A. KarlEmail author
Research Article


We analyzed eight nuclear microsatellite loci in three species of Antarctic seals; Weddell seal (Leptonychotes weddellii; mean N = 163), crabeater seal (Lobodon carcinophaga; 138) and Ross seal (Ommatophoca rossii; 35). We estimated genetic diversity (Θ) and effective population size (N E) for each species. Autosomal microsatellite based N E estimates were 151,200 for Weddell seals, 880,200 for crabeater seals, and 254,500 for Ross seals. We screened one X-linked microsatellite (Lw18), which yielded similar N E estimates to the autosomal loci for all species except the Ross seals, where it was considerably larger (~103 times). Microsatellite N E estimates were comparable with previously published N E estimates from mitochondrial DNA, but both are substantially lower than direct estimates of population size in all species except the Ross seals. The ratio of maternally versus biparentally derived estimates of N E for Ross seals was not consistent with the hypothesis that they are a polygynous species. We found no sign of a recent, sustained genetic bottleneck in any of the species.


Leptonychotes weddellii Lobodon carcinophaga Ommatophoca rossii Theta Microsatellite Phocid carnivore 



This research was funded by an American Museum of Natural History Lerner-Gray grant to CC, NSF OPP 98-16011 and OPP 98-16035 grants to BSS, and NSF DEB 98-06905 and DEB 03-21924 grants to SAK. Much of the research was conducted in the Department of Biology, University of South Florida (Tampa, FL, USA) in partial fulfillment of the doctoral research of CC. We thank H. Xu for generously providing statistical analysis software and four anonymous reviewers for critical comments. Part of this work was carried out by using the resources of the Computational Biology Service Unit from Cornell University, which is partially funded by Microsoft Corporation. This research was authorized by research permits 976 under the United States Marine Mammal Protection Act and 2000–2001 under The United States Antarctic Conservation Act and was approved by the Institutional Animal Care and Use Committee of Hubbs-SeaWorld Research Institute, which is registered as a Research Facility with the United States Department of Agriculture-Animal and Plant Health Inspection Service. This is SOEST contribution No. 8210 and HIMB contribution No. 1453.


  1. Amos W, Hutter CM, Schug MD, Aquadro CF (2003) Directional evolution of size coupled with ascertainment bias for variation in Drosophila microsatellites. Mol Biol Evol 20:660–662PubMedCrossRefGoogle Scholar
  2. Andolfatto P (2001) Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol 18:279–290PubMedGoogle Scholar
  3. Arnason U, Gullberg A, Janke A, Kullberg M, Lehman N, Petrov EA, Vainola R (2006) Pinniped phylogeny and a new hypothesis for their origin and dispersal. Mol Phylogenet Evol 41:345–354PubMedCrossRefGoogle Scholar
  4. Barker JS, Frydenberg J, Gonzalez J, Davies HI, Ruiz A, Sorensen JG, Loeschcke V (2009) Bottlenecks, population differentiation and apparent selection at microsatellite loci in Australian Drosophila buzzatti. Heredity 102:389–401PubMedCrossRefGoogle Scholar
  5. Bartsh SS, Johnston SD, Siniff DB (1992) Territorial behavior and breeding frequency of male Weddell seals (Leptonychotes weddellii) in relation to age, size, and concentrations of serum testosterone and cortisol. Can J Zool 70:680–692CrossRefGoogle Scholar
  6. Bazin E, Glemin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science 312:570–572PubMedCrossRefGoogle Scholar
  7. Bengtson JL, Laake JL, Boveng PL, Cameron MF, Hanson MB, Stewart BS (2011) Distribution, density, and abundance of pack-ice seals in the Amundsen and Ross Seas, Antarctica. Deep-Sea Res II 58:1261–1267Google Scholar
  8. Betancourt AJ, Kim Y, Orr HA (2004) A pseudohitchhiking model of X vs autosomal diversity. Genetics 168:2261–2269PubMedCrossRefGoogle Scholar
  9. Blix AS, Nordøy ES (2007) Ross seal (Ommatophoca rossii) annual distribution, diving behaviour, breeding and moulting, off Queen Maud Land, Antarctica. Polar Biol 30:1449–1458CrossRefGoogle Scholar
  10. Burg TM, Trites AW, Smith MJ (1999) Mitochondrial and microsatellite DNA analyses of harbour seal population structure in the northeast Pacific Ocean. Can J Zool 77:930–943CrossRefGoogle Scholar
  11. Cameron MF, Siniff DB (2004) Age-specific survival, abundance, and immigration rates of a Weddell seal (Leptonychotes weddellii) population in McMurdo Sound, Antarctica. Can J Zool 82:601–615CrossRefGoogle Scholar
  12. Caudron AK, Negro SS, Fowler M, Boren L, Poncin P, Robertson BC, Gemmell NJ (2010) Alternative mating tactics in the New Zealand fur seal (Arctocephalus forsteri): when non-territorial males are successful too. Aust J Zool 57:409–421CrossRefGoogle Scholar
  13. Coltman DW, Bowen WD, Wright JM (1996) PCR primers for harbour seal (Phoca vitulina concolour) microsatellites amplify polymorphic loci in other pinniped species. Mol Ecol 5:161–163PubMedCrossRefGoogle Scholar
  14. Crawford AM, Cuthbertson RP (1996) Mutations in sheep microsatellites. Genome Res 6:876–879PubMedCrossRefGoogle Scholar
  15. Curtis C, Stewart BS, Karl SA (2007) Sexing pinnipeds with ZFX and ZFY loci. J Hered 98:280–285PubMedCrossRefGoogle Scholar
  16. Curtis C, Stewart BS, Karl SA (2009) Pleistocene population expansions of Antarctic pack-ice seals. Mol Ecol 18:2112–2121PubMedCrossRefGoogle Scholar
  17. Dallas JF (1992) Estimation of microsatellite mutation rates in recombinant inbred strains of mouse. Mamm Genome 3:452–456PubMedCrossRefGoogle Scholar
  18. Davis CS, Stirling I, Strobeck C (2000) Genetic diversity of Antarctic pack ice seals in relation to life history characteristics. In: Davison W, Howard-Williams P, Broady P (eds) Antarctic ecosystems: models for a wider ecological understanding. Caxton Press, Christchurch, New Zealand, pp 56–62Google Scholar
  19. Davis CS, Gelatt TS, Siniff D, Strobeck C (2002) Dinucleotide microsatellite markers from the Antarctic seals and their use in other pinnipeds. Mol Ecol Notes 2:203–208Google Scholar
  20. Davis CS, Stirling I, Strobeck C, Coltman DW (2008) Population structure of ice-breeding seals. Mol Ecol 17:3078–3094PubMedCrossRefGoogle Scholar
  21. de Oliveira LR, Hoffman JI, Hingst-Zaher E, Majluf P, Muelbert MMC, Morgante JS, Amos W (2008) Morphological and genetic evidence for two evolutionary significant units (ESUs) in the South American fur seal, Arctocephalus australis. Conserv Genet 9:1451–1466CrossRefGoogle Scholar
  22. Decker D, Stewart BS, Lehman N (2002) Major histocompatibility complex class II DOA sequences from three Antarctic seal species verify stabilizing selection on the dog locus. Tissu Ant 60:533–537Google Scholar
  23. Dib C, Faure S, Fizames C, Samson D, Drouot N, Vignal A, Millasseau P, Marc S, Hazan J, Seboum E, Lathrop M, Gyapay G, Morissette J, Weissenback J (1996) A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380:152–154. Note: the extended reprint is available at As of 07/01/2011, however, the mutation rate information is missingGoogle Scholar
  24. 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:e10671PubMedCrossRefGoogle Scholar
  25. diRienzo 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 91:3166–3170CrossRefGoogle Scholar
  26. Ellegren H (2000) Microsatellite mutations in the germline: implications for evolutionary inference. Trend Genet 16:551–558CrossRefGoogle Scholar
  27. Erickson AW, Hanson MB (1990) Continental estimates and population trends of Antarctic ice seals. In: Kerry KR, Hempel G (eds) Antarctic ecosystems, ecological change, conservation. Springer-Verlag, Berlin and Heidelberg, pp 253–264Google Scholar
  28. Estoup A, Angers B (1998) Microsatellite and minisatellites for molecular ecology: theoretical and empirical considerations. In: Carvalho GR (ed) Advances in molecular ecology. IOS Press, Amsterdam, Netherlands, pp 55–86Google Scholar
  29. Fabiani A, Galimberti F, Sanvito S, Hoelzel AR (2004) Extreme polygyny among southern elephant seals on Sea Lion Island, Faukland Islands. Behav Ecol 15:961–969CrossRefGoogle Scholar
  30. Felsenstein J (2005) Accuracy of coalescent likelihood estimates: do we need more sites, more sequence, or more loci? Mol Biol Evol 23:691–700PubMedCrossRefGoogle Scholar
  31. Frankham R (1995) Effective population size/adult population size in wildlife: a review. Genet Res 66:95–107CrossRefGoogle Scholar
  32. Galbusera P, van Dongen S, Matthysen E (2000) Cross-species amplification of microsatellites in passerine birds. Conserv Genet 1:163–168CrossRefGoogle Scholar
  33. Gao H, Shengli C, Binlun Y, Baiyao C, Fei Y (2009) Discrepancy variation of dinucleotide microsatellite repeats in eukaryotic genomes. Biol Res 42:365–375PubMedCrossRefGoogle Scholar
  34. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318PubMedCrossRefGoogle Scholar
  35. Gelatt T, Davis C, Cameron M, Siniff D, Strobeck C (2000) The old and the new: integrating population ecology and population genetics of Weddell seals. In: Davison W, Howard-Williams P, Broady P (eds) Antarctic ecosystems: models for a wider ecological understanding. Caxton Press, Christchurch, New Zealand, pp 63–70Google Scholar
  36. Goodman SJ (1998) Patterns of extensive genetic differentiation and variation among European harbor seals (Phoca vitulina vitulina) revealed using DNA microsatellite polymorphisms. Mol Biol Evol 15:104–118PubMedGoogle Scholar
  37. Graves JA, Helyar A, Biuw M (2009) Microsatellite and mtDNA anaysis of the population structure of grey seals (Halichoerus grypus) from three breeding areas in the Baltic Sea. Conserv Genet 10:59–68CrossRefGoogle Scholar
  38. Han JB, Sun FY, Gao XG, He CB, Wang PL, Ma ZQ (2010) Low microsatellite variation in spotted seal (Phoca largha) shows a decrease in population size in the Liaodong Gulf colony. Ann Zool Fenn 47:15–27Google Scholar
  39. Hartl DL, Clark AG (2007) Principles of population genetics, 4th edn. Sinauer Associates, Sunderland, MassachusettsGoogle Scholar
  40. Hayes SA, Pearse DE, Costa D, Harvey JT, LeBoeuf BJ, Garza JC (2006) Mating system and reproductive success in eastern Pacific harbour seals. Mol Ecol 15:3023–3034PubMedCrossRefGoogle Scholar
  41. Hernandez-Velazquez FD, Galindo-Sanchez E, Taylor MI, De La Rosa-Velez J, Cote IM, Schramm Y, Aurioles-Gamboa D, Rico C (2005) New polymorphic microsatellite markers for California sea lions (Zalophus californianus). Mol Ecol Notes 5:140–142CrossRefGoogle Scholar
  42. Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920PubMedCrossRefGoogle Scholar
  43. Hey J, Nelson R (2004) Multilocus methods for estimating population sizes, migration rates and divergence times, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760PubMedCrossRefGoogle Scholar
  44. Higdon JW, Bininda-Edmonds ORP, Beck RMD, Ferguson SH (2007) Phylogeny and divergence of the pinnipeds (Carnivora: Mammaila) assessed using a multigene dataset. BMC Evol Biol 7:216PubMedCrossRefGoogle Scholar
  45. Hoffman JI (2009) A panel of new microsatellite loci for genetic studies of Antarctic fur seals and other otariids. Conserv Genet 10:989–992CrossRefGoogle Scholar
  46. Hoffman JI, Steinfartz S, Wolf JBW (2007) Ten novel dinucleotide microsatellite loci cloned from the Galapagos sea lion (Zalophus californianus wollebaeki) are polymorphic in other pinniped species. Mol Ecol Notes 7:103–105CrossRefGoogle Scholar
  47. Hoffman JI, Damsmahaparta KK, Nichols HJ (2008) Ten novel polymorphic dinucleotide microsatellite loci cloned from the Antarctic fur seal Arctocephalus gazella. Mol Ecol Resour 8:459–461PubMedCrossRefGoogle Scholar
  48. Hutter CM, Schug MD, Aquadro CF (1998) Microsatellite variation in Drosophila melanogaster and Drosophila simulans: a reciprocal test of the ascertainment bias hypothesis. Mol Biol Evol 15:1620–1636PubMedGoogle Scholar
  49. International Whaling Commission Report, Annex G (2005) Document SC/57/021. Report of the Sub-committee on In-depth Assessment (IA), p 9Google Scholar
  50. Kashi Y, Soller M (1999) Functional roles of microsatellites and minisatellites. In: Goldstein DB, Schlötterer C (eds) Microsatellites: evolution, applications. Oxford University Press Ind, New York, pp 10–23Google Scholar
  51. Kauer M, Zangerl B, Dieringer D, Schlötterer C (2002) Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster. Genetics 160:247–256PubMedGoogle Scholar
  52. Kingston JJ, Gwillium J (2007) Hybridization between two sympatrically breeding species of fur seals at Iles Crozet revealed by genetic analysis. Con Gen 8:1133–1145Google Scholar
  53. Kretzmann M, Mentzer L, DiGiovanni R, Leslie MS, Amato G (2006) Microsatellite diversity and fitness in stranded juvenile harp seals (Phoca groenlandica). J Hered 97:555–560PubMedCrossRefGoogle Scholar
  54. Lancaster ML, Arnould JPY, Kirkwood R (2010) Genetic status of an endemic marine mammal, the Australian fur seal, following historical harvesting. Anim Conserv 13:247–255CrossRefGoogle Scholar
  55. Laws RM (1977) Seals and whales of the Southern Ocean. Philos Trans R Soc Lond B 279:81–96CrossRefGoogle Scholar
  56. Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237CrossRefGoogle Scholar
  57. Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354PubMedCrossRefGoogle Scholar
  58. Palo JU, Makinen HS, Helle E, Stenman O, Vainola R (2001) Microsatellite variation in ringed seals (Phoca hispida): genetic structure and history of the Baltic Sea population. Heredity 86:609–617PubMedCrossRefGoogle Scholar
  59. Palo JU, Hyvärinen H, Helle E, Mäkinen HS, Väinölä R (2003) Postglacial loss of microsatellite variation in the landlocked Lake Saimaa ringed seal. Conserv Genet 4:117–128CrossRefGoogle Scholar
  60. Park SDE (2001) Trypanotolerance in West African cattle and the population genetic effects of selection. Ph.D. thesis, University of DublinGoogle Scholar
  61. Pastor T, Garza JC, Aguilar A, Tounta E, Androukaki E (2007) Genetic diversity and differentiation between the two remaining populations of the critically endangered Mediterranean monk seal. Anim Conserv 10:461–469CrossRefGoogle Scholar
  62. Payseur BA, Nachman MW (2002) Natural selection at linked sites in humans. Gene 300:31–42PubMedCrossRefGoogle Scholar
  63. Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  64. Poland VF, Pomeroy PP, Twiss SD, Graves JA (2008) A fine scale study finds limited evidence of kin clustering in a grey seal colony. Mar Mamm Sci 24:371–387CrossRefGoogle Scholar
  65. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  66. Riijks JM, Hoffman JI, Kuiken T, Osterhaus ADME, Amos W (2008) Heterozygosity and lungworm burden in harbor seals (Phoca vitulina). Heredity 100:587–593CrossRefGoogle Scholar
  67. Schlötterer C (2000) Evolutionary dynamics of microsatellite DNA. Chromosoma 109:365–371PubMedCrossRefGoogle Scholar
  68. Schultz JK, Baker JD, Toonen RJ, Bowen BW (2009) Extremely low genetic diversity in the endangered Hawaiian monk seal (Monachus schauinslandi). J Hered 100:25–33PubMedCrossRefGoogle Scholar
  69. Scientific Committee for Antarctic Research (2006) Proposal to de-list Antarctic fur seals as specially protected species. Antarctic Treaty Consultative Meeting, 2006.
  70. Serikawa T, Kuramoto T, Hilbert P, Mori M, Yamada J, Dubay CJ, Lindpainter K, Ganten D, Cuenet JL, Lathrop GM, Beckmann JS (1992) Rat gene mapping using PCR-analyzed microsatellites. Genetics 131:701–721PubMedGoogle Scholar
  71. Simonsen BT, Siegismund HR, Arctander P (1998) Population structure of African buffalo inferred from mtDNA sequences and microsatellite loci: high variation but low differentiation. Mol Ecol 7:225–237PubMedCrossRefGoogle Scholar
  72. Siniff DB, Stirling I, Bengston JL, Reichle RA (1979) Social and reproductive behavior of crabeater seals (Lobodon carcinophagus) during the austral spring. Can J Zool 57:2243–2255CrossRefGoogle Scholar
  73. Southwell C, Paxton CGM, Borchers D, Boveng P, Nordøy ES, Blix ES (2008) Estimating population status under conditions of uncertainty: the Ross seal in east Antarctica. Antarct Sci 20:123–133CrossRefGoogle Scholar
  74. Southwell C, Bengtson J, Bester M, Blix AS, Bornemann H, Boveng P, Cameron M, Forcada J, Laake J, Nordøy E, Plötz J, Rogers T, Southwell D, Steinhage D, Stewart BS, Trathan P (in press) A review of data on abundance, trends in abundance, habitat use and diet of ice-breeding seals in the Southern Ocean. CCAMLR SciGoogle Scholar
  75. Stewart BSS (2007) Current status of the Ross seal (Ommatophoca rossii): a specially protected species under Annex II (Appendix I). XXX Antarctic Treaty Consultative Meeting, Scientific Committee on Antarctic Research, May 2007Google Scholar
  76. Swanson BJ, Kelly BP, Maddox CK, Moran JR (2006) Shed skin as a source of DNA for genotyping seals. Mol Ecol Notes 6:1006–1009CrossRefGoogle Scholar
  77. Szibor R (2007) X-chromosomal markers: past, present and future. Forensic Sci Int Genet 1:93–99PubMedCrossRefGoogle Scholar
  78. Twiss SD, Poland VF, Graves JA, Pomeroy PP (2006) Finding fathers: spatio-temporal analysis of paternity assignment in grey seals (Halichoerus grypus). Mol Ecol 15:1939–1953PubMedCrossRefGoogle Scholar
  79. 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 4:535–538CrossRefGoogle Scholar
  80. Vowles EJ, Amos W (2006) Quantifying ascertainment bias and species-specific length differences in human and chimpanzee microsatellites using genome sequences. Mol Biol Evol 23:598–607PubMedCrossRefGoogle Scholar
  81. Weber JL, Wong C (1993) Mutation of short tandem repeats. Hum Mol Genet 2:1123–1128PubMedCrossRefGoogle Scholar
  82. Wilson EA (1907) Mammalia. Pgs 1–66 in National Antarctic Expedition 1901–1904, Natural History II. Zoology. British Museum, London. vol 2, pt 1Google Scholar
  83. Yu N, Fu Y-X, Li W-H (2002) DNA polymorphisms in a worldwide sample of human X chromosomes. Mol Biol Evol 19:2131–2141PubMedGoogle Scholar
  84. Yue GH, Beeckmann P, Geldermann H (2002) Mutation rate at swine microsatllite loci. Genetics 114:113–119Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Caitlin Curtis
    • 1
    • 2
  • Brent S. Stewart
    • 3
  • Stephen A. Karl
    • 4
    Email author
  1. 1.Department of Biology, SCA 110University of South FloridaTampaUSA
  2. 2.Florida Fish and Wildlife Research InstituteSt. PetersburgUSA
  3. 3.Hubbs-SeaWorld Research InstituteSan DiegoUSA
  4. 4.Hawai`i Institute of Marine BiologyUniversity of Hawai`i at MānoaKane`oheUSA

Personalised recommendations