Skip to main content

Advertisement

SpringerLink
Log in

Siberian tiger’s recent population bottleneck in the Russian Far East revealed by microsatellite markers

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Because size reduced, or bottlenecked, populations are more prone to adverse events, the detection of genetic bottleneck signatures in wildlife species is highly relevant for conservation. Here we applied 11 microsatellite markers to the endangered Siberian tiger (Panthera tigris altaica) using tissue and blood samples of animals from the Primorsky region of the Russian Far East. Excess heterozygosity and mode shift in allele frequencies tests were positive, while the M-ratio test was negative, indicating the likelihood of a contemporary rather than a historical population bottleneck. The recent genetic population bottleneck could be attributed to the well-documented demographic collapse of the Siberian tiger population in the 1940s, when population size hit bottom with 20–30 surviving animals. The mean effective population size Ne was 14 Siberian tigers (CI95: 12–25 animals), and the effective population size/census size ratio (Ne/N ratio) was 0.028. This is the first molecular evidence of a recent Siberian tiger population bottleneck, which is of great interest for further conservation and management plans of the highly endangered largest felid species, while the worryingly low effective population size challenges the optimism for the recovery of the huge Siberian cat.

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

Similar content being viewed by others

Abbreviations

N e :

effective population size

CI95:

confidence interval at 95%

HWE:

Hardy-Weinberg equilibrium

H E :

expected heterozygosity

H O :

observed heterozygosity

H EQ :

heterozygosity at mutation-drift equilibrium

LD:

linkage disequilibrium

TPM:

two-phase model

SMM:

stepwise mutation model

References

  • Broquet, T., Angelone, S., Jaquiery, J., Joly, P., Léna, J.P., Lengagne, T., Plénet, S., Luquet, E., Perrin, N., 2010. Genetic bottlenecks driven by population disconnection. Conservation Biology 24, 1596–1605.

    Article  PubMed  Google Scholar 

  • Busch, J.D, Waser, P.M., DeWoody, J.A., 2007. Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Molecular Ecology 16, 2450–2462.

    Article  CAS  PubMed  Google Scholar 

  • Carroll, C., Miquelle, D.G., 2006. Spatial viability analysis of Amurtiger Panthera tigris altaica in the Russian Far East: the role of protected areas and landscape matrix in population persistence. Journal of Applied Ecology 43, 1056–1068.

    Article  Google Scholar 

  • Chikhi, L., Sousa, V.C., Luisi, P., Goossens, B., Beaumont, M.A., 2010. The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186, 983–995.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cristescu, R., Sherwin, W.B., Handasyde, K., Cahill, V., Cooper, D.W., 2010. Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: the importance of the microsatellite structure. Conservation Genetics 11, 1043–1049.

    Article  Google Scholar 

  • Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M., Freimer, N.B., 1994. Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences 91, 3166–3170.

    Article  Google Scholar 

  • Garza, J.C., Williamson, E.G., 2001. Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10, 305–318.

    Article  CAS  PubMed  Google Scholar 

  • Glaubitz, J.C., 2004. CONVERT: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Molecular Ecology Notes 4, 309–310.

    Article  CAS  Google Scholar 

  • Handt, O., Höss, M., Krings, M., Pääbo, S., 1994. Ancient DNA-methodological challenges. Experientia 50, 524–529.

    Article  CAS  PubMed  Google Scholar 

  • Henry, P., Miquelle, D., Sugimoto, T., Mccullough, D.R., Caccone, A., 2009. In situ population structure and ex situ representation of the endangered Amur tiger. Molecular Ecology 18, 3173–3184.

    Article  CAS  PubMed  Google Scholar 

  • Heptner, V.G., Sludskii, A.A., 1972. Carnivora (hyaenas and cats). In: Heptner, V.G., Naumov, N.P. (Eds.), Mammals of the Soviet Union. Amerind Publishing Co., New Delhi, India, pp. 95–193.

    Google Scholar 

  • Johnson, J.A., Dunn, P.O., Bouzat, J.L., 2007. Effects of recent population bottlenecks on reconstructing the demographic history of prairie-chickens. Molecular Ecology 16, 2203–22022.

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski, S.T., Taper, M.L., 2006. Maximum likelihood estimation of the frequency of null alleles at microsatellite loci. Conservation Genetics 7, 991–995.

    Article  CAS  Google Scholar 

  • Kaplanov, L.G., 1948. Tigers in Sikhote-Alin. In: Tiger, Red Deer, and Moose, Materialy k poznaniyu fauny i flory SSSR, Novaya Seria, Moscow. Izd. Mosk. Obschestva Ispytateley Prirody, pp. 18–49.

  • Kitchener, A.C., Dugmore, A.J., 2000. Biogeographical change in the tiger, Panthera tigris. Animal Conservation 3, 113–124.

    Article  Google Scholar 

  • Luikart, G., Allendorf, F.W., JCornuet, J.M., Sherwin, W.B., 1998. Distortion of allele frequency distributions provides a test for recent population bottlenecks. Heredity 89, 238–2247.

    Article  CAS  Google Scholar 

  • Luikart, G., Cornuet, J.M., 1998. Empirical evaluation ofa test for identifying recently bottlenecked populations from allele frequency data. Conservation Biology 12, 228–237.

    Article  Google Scholar 

  • Luo, S.J., Kim, J.H., Johnson, W.E., van der Walt, J., Martenson, J., Yuhki, N., Miquelle, D.G., Uphyrkina, O., Goodrich, J.M., Quigley, H.B., Tilson, R., Brady, G., Martelli, P., Subramaniam, V., McDougal, C., Hean, S., Huang, S.Q., Pan, W., Karanth, K., Sunquist, M., Smith, J.L.D., O’Brien, S.J., 2004. Phylogeography and genetic ancestry of tigers (Panthera tigris). PLoS Biology 2 (12), e442.

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo, S.J., Johnson, W.E., Martenson, Antunes, A., Martelli, P., Uphyrkina, O., Traylor-Holzer, K., Smith, J.L.D., O’Brien, S.J., 2008. Subspecies genetic assignments of worldwide captive tigers increase conservation value of captive populations. Current Biology 18, 592–596.

    Article  CAS  PubMed  Google Scholar 

  • Matyushkin, E.N., Pikunov, D.G., Dunishenko, Y.M., Miquelle, D.G., Nikolaev, I.G., Smirnov, E.N., Salkina, G.P., Abramov, V.K., Bazilnikov, B.I., Yudin, V.G., Korkiskho, V.G., 1999. Distribution and numbers of Amurtigers in the Russian Far East in the mid-1990s. In: Aristova, A.A. (Ed.), Rare mammal species of Russia and neighboring territories (in Russian). Russian Academy of Sciences Therological Society, Moscow, pp. 242–271.

    Google Scholar 

  • Menotti-Raymond, M., David, V.A., Chen, Z.Q., Menotti, K.A., Sun, S., Sun, S., Schäffer, A.A., Agarwala, R., Tomlin, J.F., O’brien, S.J., Murphy, W.J., 2003. Second-generation integrated genetic linkage/radiation hybrid maps of the domestic cat (Felis catus). Journal of Heredity 94, 95–106.

    Article  CAS  PubMed  Google Scholar 

  • Miquelle, D.G., Merrill, T., Dunishenko, Y.M., Smirnov, E.N., Quigley, H.B., Pikunov, D.G., Hornocker, M.G., 1999. A habitat protection plan for the Amur tiger: developing political and ecological criteria for a viable land-use plan. In: Seidensticker, J., Christie, S., Jackson, P. (Eds.), Riding the Tiger; Meeting the Needs of People and Wildlife in Asia. Cambridge University Press, Cambridge UK, pp. 273–295.

    Google Scholar 

  • Miquelle, D.G., Smirnov, E.N., Salkina, G.A., Abramov, V.K., 2005. The importance of protected areas in Amur tiger conservation: a comparison of tiger and prey abundance in protected areas versus unprotected areas. Results of protection and research of the Sikhote-Alin natural landscape. In: Potikha, I.V., Miquelle, D.G., Gromyko, M.N., Pimenova, E.A., Khobtoneva, L.P., Yu Zaumyslova, O., Labetskaya, N.E., Ivanova, L.V. (Eds.), Papers Presented at the International Science and Management Conference Devoted to the 70th Anniversary of the Sikhote-Alin State Reserve. Terney, Primorksiy Region, September 20–23, 2005. Primpoligraphkombinat, Vladivostok, Russia, pp. 70–74 (in Russian with English abstract).

    Google Scholar 

  • Miquelle, D., Darman, Y., Seryodkin, I., 2010a. Panthera tigris spp. altaica. In: IUCN 2010. IUCN Red List of Threatened Species. Version 2010.4., http://www.iucnredlist.org.

  • Miquelle, D.G., Goodrich, J.M., Smirnov, E.N., Stephens, P.A., Zaumyslova, O.Yu., Chapron, G., Kerley, L., Murzin, A.A., Hornocker, M.G., Quigley, H.B., 2010b. The Amur Tiger: a case study of living on the edge. In: Macdonald, D.W., Loveridge, A. (Eds.), Biology and Conservation of Wild Felids. Oxford University Press, Oxford, UK, pp. 325–339.

    Google Scholar 

  • Miquelle, D.G., Pikunov, D.G., 2003. Status of the Amurtiger and Far Eastern leopard. In: Newell, J.P. (Ed.), The Russian Far East: A Reference Guide for Conservation and Development. Daniel and Daniel Publishers, McKinleyville, California, pp. 106–109.

    Google Scholar 

  • Miquelle, D.G., Pikunov, D.G., Dunishenko, Y.M., Aramilev, V.V., Nikolaev, I.G., Abramov, V.K., Smirnov, E.N., Salkina, G.P., Seryodkin, I.V., Gaponov, V.V., Fomenko, P.V., Litvinov, M.N., Kostyria, A.V., Yudin, V.G., Korkishko, V.G., Murzin AA, 2007. 2005 AmurTiger Census. Cat News 46, 14–16.

    Google Scholar 

  • Morris, W.F., Doak, D.F., 2002. Quantitative Conservation Biology. Theory and Practice of Population Viability Analysis. Sinauer Associates, Sunderland.

    Google Scholar 

  • Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., 2004. MICRO-CHECKER: software for identifying and correcting geno-typing errors in microsatellite data. Molecular Ecology Notes 4, 535–538.

    Article  Google Scholar 

  • Palstra, F.P., Ruzzante, D.E., 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.

    Article  PubMed  Google Scholar 

  • 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. Journal of Heredity 90, 502–503.

    Article  Google Scholar 

  • Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Raymond, M., Rousset, F., 1995. GENEPOP version 1.2: a population genetics software for exact test and ecumenicism. Journal of Heredity 86, 248–249.

    Article  Google Scholar 

  • Russello, M., Gladyshev, E., Miquelle, D., Caccone, A., 2004. Potential genetic consequences of a recent bottleneck in the Amur Tiger of the Russian Far East. Conservation Genetics 5, 707–713.

    Article  CAS  Google Scholar 

  • Sambrook, J., Fritsch, E.F., Maniatis, T, 1989. Molecular Cloning: a Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.

    Google Scholar 

  • Tallmon, D.A., Beaumont, M.A., Luikart, G.H., 2004. Effective population size estimation using approximate Bayesian computation. Genetics 167, 977–988.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tallmon, D.A., Koyuk, A., Luikart, G.H., Beaumont, M.A., 2008. ONESAMP: a program to estimate effective population size using approximate Bayesian computation. Molecular Ecology Resources 8, 299–301.

    Article  PubMed  Google Scholar 

  • Tilson, R., Nyhus, P., Franklin, F., 2001. Tiger restoration in Asia: ecological reality and sociological reality. In: Maher, D., Noss, R., Larkin, J. (Eds.), Large Mammal Restoration: Ecological and sociological challenges in the 21st Century. Island Press.

  • Wakeley, J., 1999. Nonequilibrium migration in human history. Genetics 153, 1863–1871.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson-Natesan, E.G., 2005. Comparison of methods for detecting bottlenecks from microsatellite loci. Conservation Genetics 6, 551–562.

    Article  Google Scholar 

  • Wilting, A., Christiansen, P., Kitchener, A.C., Kemp, Y.J.M., Ambu, L., Fickel, J., 2010. Geo- graphical variation in and evolutionary history of the Sunda clouded leopard (Neofelis diardi) (Mammalia: Carnivora: Felidae) with the description of a new subspecies from Borneo. Molecular Phylogenetics and Evolution, doi:10.1016/j.ympev.2010.11.007.

Download references

Author information

Authors and Affiliations

  1. Estación Biológica de Doñana, Consejo Superior de Investigaciones Científicas (CSIC), Avda. Américo Vespucio s/n, 41092, Sevilla, Spain

    Samer Alasaad & Ramón C. Soriguer

  2. Institute of Biology & Soil Science, Far Eastern Branch of the Russian Academy of Sciences, 690022, Vladivostok, Russia

    Samer Alasaad & Galina Chelomina

  3. Khankaisky State Biosphere Nature Reserve, Spassk-Dalny, Russia

    Yury Petrovich Sushitsky

  4. Research Group Evolutionary Genetics, Leibniz-Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. 17, D-10315, Berlin, Germany

    Samer Alasaad & Joerns Fickel

Authors
  1. Samer Alasaad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ramón C. Soriguer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Galina Chelomina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yury Petrovich Sushitsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joerns Fickel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Samer Alasaad or Joerns Fickel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alasaad, S., Soriguer, R.C., Chelomina, G. et al. Siberian tiger’s recent population bottleneck in the Russian Far East revealed by microsatellite markers. Mamm Biol 76, 722–726 (2011). https://doi.org/10.1016/j.mambio.2011.01.011

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2011.01.011

Keywords

Search

Navigation