Skip to main content
SpringerLink
Log in

Present genetic structure revealed by microsatellites reflects recent history of the Finnish moose (Alces alces)

  • Original Paper
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

Genetic structures of Holarctic species are largely formed by Pleistocene colonisation history, dispersal capacity and interactions between biotic and abiotic factors, even though the human impact can also be significant. The Holarctic moose (Alces alces) arrived in Fennoscandia around 9,000–8,000 years ago, and it has been exploited by humans ever since. During the last 400 years, the Finnish moose population has suffered from several population declines, and even local and regional extirpations have occurred. The purpose of the present study is to describe the genetic variation and population structure of the Finnish moose in order to clarify how historical events and human exploitation have influenced the present-day genetic patterns. Altogether 130 moose individuals from seven sampling sites in Finland were analysed at ten microsatellite loci. A variety of population genetic and coalescent-based methods was applied. The Finnish moose population was found to be divided into southern and northern subpopulations with additional lower hierarchical genetic structure. The estimated time of divergence between these two subpopulations was about 96–238 years ago. In addition, an isolation-by-distance pattern was discovered.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Figure 6

Similar content being viewed by others

References

  • Allendorf FW, England PR, Luikart G, Ritchie PA, Ryman N (2008) Genetic effects of harvest on wild animal populations. Trends Ecol Evol 23:327–337

    Article  PubMed  Google Scholar 

  • Allendorf FW, Hard JJ (2009) Human-induced evolution caused by unnatural selection through harvest of wild animals. P Natl Acad Sci USA 106:9987–9994

    Article  CAS  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Catch F (2004) GENETIX 4.0.5.2., software under Windows™ for the genetics of the populations. Laboratory Genome, Populations, Interactions, CNRS UMR 5000. University of Montpellier II, Montpellier, France

    Google Scholar 

  • Bishop MD, Kappes SM, Keele JW, Stone RT, Sunden SLF, Hawkins GA, Toldo SS, Fries R, Grosz MD, Yoo J, Beattie CW (1994) A genetic linkage map for cattle. Genetics 136:619–639

    PubMed  CAS  Google Scholar 

  • Buchanan FC, Crawford AM (1993) Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OarFCB304 loci. Anim Genet 145

  • Buchanan FC, Galoway SM, Crawford AM (1994) Ovine microsatellites at the OarFCB5, OarFCB19, OarFCB20, OarFCB48, OarFCB129 and OarFCB226 loci. Anim Genet 25:60

    PubMed  CAS  Google Scholar 

  • Busch JD, Waser PM, DeWoody JA (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462

    Article  PubMed  CAS  Google Scholar 

  • Charlier J, Laikre L, Ryman N (2008) Genetic structure and evidence of a local bottleneck in moose in Sweden. J Wildl Manag 72:411–415

    Article  Google Scholar 

  • Clark PU, Mix AC (2002) Ice sheets and sea level of the last glacial maximum. Quat Sci Rev 21:1–7

    Article  Google Scholar 

  • Cornuet JM, Luikart G (1996) Description and power analysis of two tests for inferring recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • Cornuet JM, Santos F, Beaumont MA, Robert CP, Marin JM, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to approximate Bayesian computations. Bioinformatics 24:2713–2719

    Article  PubMed  CAS  Google Scholar 

  • Davydov AV, Kholodova MV, Meshshersky IG, Tsarev SA, Gubar JuP, Linkov AB, Pronjajev AV, Ovsjukova NE, Rozhkova LV, Rozhkov JuI (2006) Populjatsionnoje delenije jevropeiskogo losja (Alces alces alces L.) i problema antropogennogo razdroblenija ego areala. - Sostojanije sredy obitanija i fauna okhotnichjih zhivotnyh Rossii. Materialy vserossijskoi nauchno-prakticheskoi konferentsii. Moskva 21.-22. 2.2006, 1–9. (In Russian)

  • Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Mol Ecol 11:2571–2581

    Article  PubMed  CAS  Google Scholar 

  • Escudero A, Iriondo JM, Torres ME (2003) Spatial analysis of genetic diversity as a tool for plant conservation. Biol Conserv 113:351–365

    Article  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  PubMed  CAS  Google Scholar 

  • Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Frantz AC, Cellina S, Krier A, Schley L, Burke T (2009) Using Bayesian methods to determine the genetic structure of a continuously distribute population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Gaillard J-M (2007) Are moose only a large deer? Some life history considerations. Alces 43:1.11

    Google Scholar 

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • Gill R (1990) Monitoring the status of European and North American cervids. United Nations Environment programme. The Global Environment Monitoring System (GEMS) information series No 8, 277pp. Nairobi

  • 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.html

  • Haanes H, Røed KH, Solberg EJ, Herfindal I, Sæther B-E (2011) Genetic discontinuities in a continuously distribute and highly mobile ungulate, the Norwegian moose. Conserv Genet 12:1131–1143

    Article  Google Scholar 

  • Hardy OJ (2003) Estimation of pairwise relatedness between individuals and characterization of isolation-by-distance processes using dominant genetic markers. Mol Ecol 12:1577–1588

    Article  PubMed  Google Scholar 

  • Hardy OJ, Vekemans X (2002) SPAGeDi: a versatile computer program to analyze spatial genetic structure at individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Harris RB, Wall WA, Allendorf F (2002) Genetic consequences of hunting: what do we know and what should we do? Wildl Soc B 30:634–643

    Google Scholar 

  • Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112

    Article  Google Scholar 

  • Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  PubMed  CAS  Google Scholar 

  • Hey J (2010) Isolation with migration models for more than two populations. Mol Biol Evol 27:905–920

    Article  PubMed  CAS  Google Scholar 

  • Hey J (2009) IMa documentation: using the IMa program. http://lifesci.rutgers.edu/~heylab/ProgramsandData/Programs/IM/Using_IMa_12_17_09.pdf. Accessed 28 November 2012

  • Hulme DJ, Silk JP, Redwin JM, Barendse W, Beh KJ (1994) Ten polymorphic ovine microsatellites. Anim Genet 25:434–435

    Article  PubMed  CAS  Google Scholar 

  • Hundertmark KJ, Bowyer RT (2004) Genetics, evolution and phylogeography of moose. Alces 40:103–122

    Google Scholar 

  • Hundertmark KJ, Shields GF, Udina IG, Bowyer RT, Danilkin AA, Schwartz CC (2002) Mitochondrial phylogeography of moose (Alces alces): late Pleistocene divergence and population expansion. Mol Phylogenet Evol 22:375–387

    Article  PubMed  CAS  Google Scholar 

  • Hundertmark KJ, Van Daele LJ (2010) Founder effect and bottleneck signatures in an introduced, insular population of elk. Conserv Genet 11:139–147

    Article  Google Scholar 

  • Jedrzejewska B, Jedrzejewski W, Bunevich AN, Milkowski L, Krasinski ZA (1997) Factors shaping population densities and increase rates of ungulates in Bialowieza Primeval Forest (Poland and Belarus) in the 19th and 20th centuries. Acta Theriol 42:399–451

    Google Scholar 

  • Kruglyak S, Durrett RT, Schug MD, Aquadro CF (1998) Equilibrium distributions of microsatellite repeat length resulting from a balance between slippage events and point mutations. P Natl Acad Sci USA 95:10774–10778

    Article  CAS  Google Scholar 

  • Lavsund S, Nygrén T, Solberg EJ (2003) Status of moose populations and challenges to moose management in Fennoscandia. Alces 39:109–130

    Google Scholar 

  • Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). Am J Bot: 1420–25

  • Luikart G, Cornuet JM (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237

    Article  Google Scholar 

  • Markgren G (1974) The moose in Fennoscandia. Nat Can 101:185–194

    Google Scholar 

  • Miller MP (1997) Tool for population genetic analyses (TFPGA). A Windows program for the analysis of allozyme and molecular population genetic data. Department of Biological Sciences. Northern Arizona University, USA

  • Moore SS, Byrne K, Berger KT, Barendse W, McCarthy F, Womack JE, Hetzel DJS (1994) Characterization of 65 bovine microsatellites. Mamm Genome 5:84–90

    Article  PubMed  CAS  Google Scholar 

  • Mysterud A, Langvatn R, Yocoz NG, Stenseth NC (2002) Large-scale habitat variability, delayed density effects and red deer populations in Norway. J Anim Ecol 71:569–580

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Nygrén T (1987) The history of moose in Finland. Swed Wildl Res Suppl 1:49–54

    Google Scholar 

  • Nygrén T (1990) Hirvikannan tila ja hirvitutkimusten nykyvaihe Lapissa. Riistantutki-musosaston tiedote 104: 1–21. Finnish Game and Fisheries Research Institute, Helsinki, Finland (In Finnish)

  • Nygrén T (1996) Hirvikanta pienimmillään 19 vuoteen, rakenne entistäkin naarasvaltaisempi. Riistantutkimusosaston tiedote 145: 1–29. Finnish Game and Fisheries Research Institute, Helsinki, Finland (In Finnish)

  • Nygrén T (2009) Biology and policies in Finnish moose population regulation and management. Dissertation. University of Joensuu, Finland

    Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hered 95:536–539

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Gen 6:847–846

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Provan J, Bennet KD (2008) Phylogeographic insights into cryptic glacial refugia. Trends Ecol Evol 23:564–571

    Article  PubMed  Google Scholar 

  • 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 4:535–538

    Article  Google Scholar 

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. P Natl Acad Sci USA 94:9197–9201

    Article  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Rozhkov JI, Kholodova MV, Davydov AV, Meshshersky IG, Piskunov OD (2005) Spatial differentiation of moose in European (Alces alces L.) by results of the mitochondrial DNA analysis. Vestnik Okhotovedenija 2:287–290 (In Russian)

    Google Scholar 

  • Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Røed KH, Midthjell L (1998) Microsatellites in reindeer, Rangifer tarandus, and their use in other Cervids. Mol Ecol 7:1771–1788

    Article  Google Scholar 

  • Ryman N, Beckman G, Bruun-Petersen G, Reuterwall C (1977) Variability of red cell enzymes and genetic implications of management policies in Scandinavian moose (Alces alces). Hereditas 85:157–162

    Article  Google Scholar 

  • Ryman N, Reuterwall C, Nygrén K, Nygrén T (1980) Genetic variation and differentiation in Scandinavian moose (Alces alces): are large mammals monomorphic? Evolution 34:1037–1049

    Article  Google Scholar 

  • Schmidt JI, Hundertmark KJ, Bowyer T, McCraken KG (2009) Population structure and genetic diversity of moose in Alaska. J Hered 100:170–180

    Article  PubMed  CAS  Google Scholar 

  • Schmölcke U, Zachos FE (2005) Holocene distribution and extinction of the moose (Alces alces, Cervidae) in Central Europe. Mamm Biol 6:329–344

    Google Scholar 

  • Schwartz MK, McKelvey KS (2008) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Slatkin M (1995) A measure of population subdivision based on microsatellite allele frequencies. Genetics 139:457–462

    PubMed  CAS  Google Scholar 

  • Solberg EJ, Røed KH, Flagstad Ø, Sæther BE, Heim M, Andersen R, Rolandsen CM (2009) Elgens genetiske struktur i Norge. NINA rapport 467, Trondheim, Norway. (In Norwegian)

  • Swabrick PA, Dietz AB, Womack JE, Crawford AM (1992) Ovine and bovine dinucleotide repeat polymorphism at the MAF46 locus. Anim Genet 23:182

    Article  Google Scholar 

  • Sæther B-E, Engen S, Solberg EJ (2009) Effective size of harvested ungulate populations. Anim Conserv 12:488–495

    Google Scholar 

  • Taavitsainen J-P (1980) Distribution of the moose in Finland in prehistoric times in the light of archaeological evidence. Suomen Riista 28:5–14 (In Finnish with English summary)

    Google Scholar 

  • Telfer ES (1984) Circumpolar distribution and habitat requirements of moose (Alces alces). In: Olson R, Hastings R, Geddes F (ed) Northern ecology and resource management, The University of Alberta Press, pp 154–182

  • Tiilikainen R, Nygrén T, Pusenius J, Ruusila V (2010) Variation in growth pattern of male moose after two contrasted periods of hunting. Ann Zool Fenn 47:159–172

    Article  Google Scholar 

  • Ukkonen P (1993) The post-glacial history of the Finnish mammalian fauna. Ann Zool Fenn 30:249–264

    Google Scholar 

  • Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562

    Article  Google Scholar 

  • Wilson GA, Strobeck C, Wu L, Coffin JW (1997) Characterization of microsatellite loci in caribou Rangifer tarandus, and their use in other Artiodactyls. Mol Ecol 6:697–699

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We would like to thank the Fish and Wildlife Health Unit of the Finnish Food Safety Authority Evira for providing the blood samples. We would also like to thank Arthur L. Pelegrin and Nelli Rönkä for proofreading the manuscript. This work was supported by the North Ostrobothnia Regional fund of the Finnish Cultural Foundation, Finnish Game Management Foundation, Biological Society of Finland Vanamo and Oulun Luonnonystävät by providing funds for V-MK.

Author information

Authors and Affiliations

  1. Department of Biology, University of Oulu, PO Box 3000, 90014, Oulu, Finland

    Veli-Matti Kangas, Laura Kvist & Jouni Aspi

  2. Nurminiementie 2, 93600, Kuusamo, Finland

    Sauli Laaksonen

  3. Finnish Game and Fisheries Research Institute, Yliopistontie 4b, 82900, Ilomantsi, Finland

    Tuire Nygrén

Authors
  1. Veli-Matti Kangas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura Kvist
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sauli Laaksonen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tuire Nygrén
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jouni Aspi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Veli-Matti Kangas.

Additional information

Communicated by: C. Gortazar

Appendix

Appendix

Table 4 Summary of the different sets of microsatellites used in four studies on moose population genetics in Finland, Sweden, Norway and Alaska (in the USA). Applied loci (with their original references) in each study, their total number and estimated heterozygosity H e over these loci are represented
Full size table

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kangas, VM., Kvist, L., Laaksonen, S. et al. Present genetic structure revealed by microsatellites reflects recent history of the Finnish moose (Alces alces). Eur J Wildl Res 59, 613–627 (2013). https://doi.org/10.1007/s10344-013-0712-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10344-013-0712-0

Keywords

Search

Navigation