Conservation Genetics

, Volume 4, Issue 2, pp 117–128 | Cite as

Postglacial loss of microsatellite variation in the landlocked Lake Saimaa ringed seal

  • J.U. PaloEmail author
  • H. Hyvärinen
  • E. Helle
  • H.S. Mäkinen
  • R. Väinölä


The Lake Saimaa ringed sealPhoca hispida saimensis has lived as anisolated landlocked population in easternFinland since the early post-glacial. In thelast century, the population crashed down to c.200 individuals, and is under a constant threatof extinction. We evaluated the genetic historyof the Saimaa population through a comparisonwith the conspecific sister populations in theArctic Ocean and the Baltic Sea, which haveretained high levels of variation since thedeglaciation. At eight microsatellite loci, thecurrent gene diversity (heterozygosity) of theSaimaa seal was 69% lower than in thereference populations. Allowing reasonablemutation rates (μ = 10−4), thisimplies a long-term post-glacial effectivepopulation size of Ne ≃ 350,and a slow average rate of inbreeding ΔF≃ 0.15% per generation during the c.860 generations (9 500 years) of isolation. Thecurrent Ne is an order of magnitudesmaller and ΔF correspondinglylarger. Whereas the additional loss of markervariation in the short term will not be highrelative to that already taken place, it seemsunwarranted to suppose that the past, slowinbreeding would have effectively purged thepopulation of genetic load and reduced thegenetic risks from small population size.Although the population is now clearlygeographically subdivided in the complex lakesystem, we found little genetic differentiationbetween main breeding areas (FST =0.02). However, at the current low populationdensities, the subdivision may markedly furtherincrease the future rate of inbreeding.

effective population size inbreeding microsatellite variation Phoca hispida saimensis postglacial isolation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allen PJ, Amos W, Pomeroy PP, Twiss SD (1995) Microsatellite variation in grey seals (Halichoerus grypus) shows evidence of genetic differentiation between two British breeding colonies. Mol. Ecol., 4, 653–662.Google Scholar
  2. Ballou JD (1997) Ancestral inbreeding only minimally affects inbreeding depression in mammalian populations. J. Hered., 88, 169–178.Google Scholar
  3. Balloux F (2001) easypop (version 1.7), A computer program for population genetics simulation. J. Hered., 92, 301–302.Google Scholar
  4. Berthier P, Beaumont MA, Cornuet JM, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: A genealogical approach. Genetics, 100, 741–751.Google Scholar
  5. Bruford MW, Hanotte O, Brookfield JFY, Burke T (1992) Singlelocus and multilocus DNA fingerprinting. In: Molecular Genetic Analysis of Populations. A Practical Approach (ed. Hoelzel AR), pp. 225–269. Oxford University Press, Oxford/New York/ Tokyo.Google Scholar
  6. Bürger R, Lynch M (1997) Adaptation and extinction in changing environments. In: Environmental Stress, Adaptation and Evolution (eds. Bijlsma R, Loeschke V), pp. 209–239. Birkhäuser Verlag, Basel, Switzerland.Google Scholar
  7. Charlesworth B (1998) Measures of divergence between populations and the effect of forces that reduce variability. Mol. Biol. Evol., 15, 538–543Google Scholar
  8. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu. Rev. Ecol. Syst., 18, 237–268.Google Scholar
  9. Coltman DW, Bowen WD, Wright JM (1998) Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond., Ser. B: Biol. Sci., 265, 803–809.Google Scholar
  10. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred Soay sheep in a freeliving, island population. Evolution, 53, 1259–1267.Google Scholar
  11. Comps B, Gömöry D, Letouzey J, Thiébaut T, Petit RJ (2001) Diverging trends between heterozygosity and allelic richness during postglacial colonization in the European Beech. Genetics, 157, 389–397.Google Scholar
  12. 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.Google Scholar
  13. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity, 83, 260–270.Google Scholar
  14. Donner J (1995) The Quaternary History of Scandinavia. Cambridge University Press, Cambridge, UK.Google Scholar
  15. Eldridge MDB, King JM, Loupis AK, Spencer PBS, Taylor AC, Pope LC, Hall GP (1999) Unprecedented low levels of genetic variation and inbreeding depression in an island population of the black-footed rock-wallaby. Cons. Biol., 13, 531–541.Google Scholar
  16. Estoup A, Angers B (1998) Microsatellites and minisatellites for molecular ecology: Theoretical and empirical considerations. In: Advances in Molecular Ecology (ed. Carvalho GR). IOS Press, Amsterdam, Netherlands.Google Scholar
  17. Forstén A, Alhonen P (1975) The Subfossil seals of Finland and their relation to the history of the Baltic Sea. Boreas, 4, 10–22.Google Scholar
  18. Frankham R (1995) Effective population size/adult population size ratios in wildlife: A review. Genet. Res., 66, 95–107.Google Scholar
  19. Franklin IR (1980) Evolutionary changes in small populations. In: Conservation Biology (eds. Soulé ME, Wilcox BA), pp. 135–149. Sinauer, Sunderland, MA.Google Scholar
  20. Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim. Cons., 1, 69–73Google Scholar
  21. Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol. Ecol., 10, 305–318.Google Scholar
  22. Gilligan DM, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (1997) Is mutation accumulation a threat to the survival of endangered populations? Cons. Biol., 11, 1235–1241.Google Scholar
  23. Goodman SJ (1997) Dinucleotide repeat polymorphisms at seven anonymous microsatellite loci cloned from the European harbour seal (Phoca vitulina vitulina). Anim. Genet., 28, 310–311.Google Scholar
  24. Gotelli D, Sillero Zubiri C, Applebaum GD, Roy MS, Girman DJ, Garcia Moreno J, Ostrander EA, Wayne RK (1994) Molecular genetics of the most endangered canid: The Ethiopian wolf Canis simensis. Mol. Ecol., 3, 301–312.Google Scholar
  25. Goudet J (1995) FSTAT version 1.2: A computer program to calculate F-statistics. J. Hered., 86, 485–486.Google Scholar
  26. Hartl DL, Clark AC (1997) Principles of Population Genetics. Sinauer, Sunderland, MA.Google Scholar
  27. Hedrick PW (1994) Purging inbreeding depression and the probability of extinction: Full-sib mating. Heredity, 73, 363–372.Google Scholar
  28. Hoelzel AR (1999) Impact of population bottlenecks on genetic variation and the importance of life-history; a case study of the northern elephant seal. Bio. J. Linn. Soc., 68, 23–39.Google Scholar
  29. Hoelzel AR, LeBoeuf BJ, Campagna C, Reiter J (1999) Alpha male paternity in elephant seals. Behav. Ecol. Sociobiol., 46, 298–306.Google Scholar
  30. Houlden BA, England PR, Taylor AC, Greville WD, Sherwin WB (1996) Low genetic variability of the koala Phascolarctos cinereus in south-eastern Australia following a severe population bottleneck. Mol. Ecol., 5, 269–281.Google Scholar
  31. Hyvärinen H, Nieminen M (1990) Differentiation of the ringed seal in the Baltic Sea, Lake Ladoga and Lake Saimaa. Finnish Game Res., 47, 21–27.Google Scholar
  32. Hyvärinen H, Sipilä T (1992) Saimaannorppa Phoca (Pusa) hispida saimensis. In: Maailman uhanalaiset eläimet (ed. Elo U), pp. 68–71. Weilin &; Göös, Vantaa.Google Scholar
  33. Järvinen O, Varvio SL (1985) Proneness to extinction of small populations of seals: Demographic and genetic stochasticity vs. environmental stress. Finnish Game Res., 44, 6–18.Google Scholar
  34. Kirkpatrick M, Jarne P (2000) The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat., 155, 154–167.Google Scholar
  35. Kokko H, Lindström J, Ranta E (1997) Risk analysis of hunting of seal populations in the Baltic. Cons. Biol., 11, 917–927.Google Scholar
  36. Kokko H, Lindström J, Ranta E, Sipilä T, Koskela J (1998) Estimating the demographic effective population size of the Saimaa ringed seal (Phoca hispida saimensis Nordq.). Anim. Conserv., 1, 47–54.Google Scholar
  37. Kokko H, Helle E, Lindström J, Ranta E, Sipilä T, Courchamp F (1999) Backcasting population sizes of ringed and grey seals in the Baltic and Lake Saimaa during the 20th century. Ann. Zool. Fenn., 36, 65–73.Google Scholar
  38. Koskela JT, Kunnasranta M, Hämäläinen E, Hyvärinen H (2002) Movements and use of haul-out sites of radio-tagged Saimaa ringed seal (Phoca hispida saimensis Nordq.) during the openwater season. Ann. Zool. Fenn., 39 (in press).Google Scholar
  39. Kunnasranta M (2001) Behavioural Biology of Two Ringed Seal (Phoca hispida) Subspecies in the Large European Lakes Saimaa and Ladoga. PhD thesis. University of Joensuu, Joensuu, Finland.Google Scholar
  40. Kuusisto E (1999) Basins and balances. In: Saimaa–A Living Lake (ed. Kuusisto E.), pp. 21–39. Tammi, HelsinkiGoogle Scholar
  41. Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J. Mammal., 78, 320–335.Google Scholar
  42. Lande R (1995) Mutation and conservation. Cons. Biol., 9, 782–791.Google Scholar
  43. Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Cons. Biol., 12, 228–237.Google Scholar
  44. Nieminen M, Singer MC, Fortelius W, Schöps K, Hanski I (2001) Experimental confirmation that inbreeding depression increases extinction risk in butterfly populations. Am. Nat., 157, 237–244.Google Scholar
  45. Paetkau D, Waits LP, Clarkson PL, Craighead L, Vyse E, Ward R, Strobeck C (1998) Variation in genetic diversity across the range of North American brown bears. Cons. Biol., 12, 418–429.Google Scholar
  46. Palo JU, Mäkinen HS, Helle E, Stenman O, Väinölä R (2001) Microsatellite variation in ringed seals (Phoca hispida): Genetic structure and history of the Baltic Sea population. Heredity, 86, 609–617.Google Scholar
  47. Ranta E, Lindström J, Kokko H (1996) Ecological risk analysis: The case of the Saimaa ringed seal. Ambio, 25, 363–365.Google Scholar
  48. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered., 86, 248–249.Google Scholar
  49. Reijnders P, Brasseur S, van de Toorn J, van de Wolf P, Boyd I, Harwood J, Lavigne D, Lowry LL (1993) Status survey and Conservation Action Plan: Seals, Fur Seals, Sea Lions, and Walrus. The World Conservation Union IUCN.Google Scholar
  50. Simonsen V, Allendorf FW, Eanes WF, Kapel FO (1982) Electrophoretic variation in large mammals. III. The ringed seal, Pusa hispida, the harp seal, Pagophilus groenlandicus, and the hooded seal, Cystophora cristata. Hereditas, 97, 87–90.Google Scholar
  51. Sipilä T (1990) Lair structure and breeding habitat of the Saimaa ringed seal (Phoca hispida saimensis Nordq.) in Finland. Finnish Game Res., 47, 11–20.Google Scholar
  52. Sipilä T, Koskela J (2001) Saimaannorppien esiintymisalue keskittyy. Saimaan Luonto, 16, 5–7.Google Scholar
  53. Sipilä T, Helle E, Hyvärinen H (1990) Distribution, population size and reproductivity of the Saimaa ringed seal (Phoca hispida saimensis Nordq.) in Finland, 1980–1984. Finnish Game Res., 47, 3–10.Google Scholar
  54. Smith TG (1973) population dynamics of the ringed seal in the Canadian Eastern Arctic. Bull. Fish. Res. Board Canada, 181, 1–55.Google Scholar
  55. Taylor AC, Sherwin WB, Wayne RK (1994) Genetic variation of microsatellite loci in a bottlenecked species: The northern hairynosed wombat Lasiorhinus krefftii. Mol. Ecol., 3, 277–290.Google Scholar
  56. Ukkonen P (2002) The early history of seals in the northern Baltic. Ann. Zool. Fenn., 39, in press.Google Scholar
  57. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38, 1358–1370.Google Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  • J.U. Palo
    • 1
    Email author
  • H. Hyvärinen
    • 2
  • E. Helle
    • 3
  • H.S. Mäkinen
    • 1
  • R. Väinölä
    • 3
  1. 1.Department of Ecology and Systematics, Division of Population Biology, POB 65FIN-00014 University of HelsinkiFinland;
  2. 2.Department of BiologyUniversity of JoensuuFinland
  3. 3.Finnish Game and Fisheries Research Institute, POB 6HelsinkiFinland

Personalised recommendations