Skip to main content
SpringerLink
Log in

Gene flow and the restoration of genetic diversity in a fluctuating collared pika (Ochotona collaris) population

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Changes in the density of small mammal populations can alter their genetic diversity and structure over time. Repeated density declines may gradually erode a population’s genetic variability, and ultimately undermine its long-term viability. We investigated changes in the genetic diversity and structure of a fluctuating collared pika (Lagomorpha: Ochotona collaris) population over 12 years. There are concerns that the long-term persistence of the collared pika is at risk due to climate change, as pika populations are sensitive to environmental variability and inhabit a region undergoing particularly rapid warming. The study population declined abruptly during 2000 and 2003; however, it subsequently recovered and failed to show any genetic signature of having undergone a bottleneck. There was also no evidence for widespread inbreeding before or after the population declines. Using a spatial autocorrelation analysis, we also documented positive fine-scale genetic structure (<250 m) in the population during 7 out of the 12 years examined. Although the genetic structure is consistent with low average dispersal distances, a GeneClass2 analysis indicated that the collared pika population received immigrants from other populations, some of which survived and bred. Thus, like many other fluctuating small mammal populations, the collared pika population studied here appears to be resilient to density fluctuations. Dispersal distances were adequate for allowing gene flow into the study population and preventing declines in genetic variability.

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

Similar content being viewed by others

References

  • Beever EA, Ray C, Mote PW, Wilkening JL (2010) Testing alternative models of climate-mediated extirpations. Ecol Appl 20:164–178

    Article  PubMed  Google Scholar 

  • Berthier K, Charbonnel N, Galan M, Chaval Y, Cosson J-F (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676

    Article  CAS  PubMed  Google Scholar 

  • Busch JD, Waser PM, DeWoody JA (2009) The influences of density and sex on patterns of fine-scale genetic structure. Evolution 63:2302–2314

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • COSEWIC (2011) COSEWIC assessment and status report on the Collared Pika Ochotona collaris in Canada. Committee on the Status of Endangered Wildlife in Canada, Ottawa

    Google Scholar 

  • Duarte LC, Bouteiller C, Fontanillas P, Petit E, Perrin N (2003) Inbreeding in the greater white-toothed shrew, Crocidura russula. Evolution 57:638–645

    CAS  PubMed  Google Scholar 

  • Eikenaar C, Komdeur J, Richardson DS (2008) Natal dispersal patterns are not associated with inbreeding avoidance in the Seychelles warbler. J Evol Biol 21:1106–1116

    Article  CAS  PubMed  Google Scholar 

  • El Mousadik A, Petit RJ (1996) High level of genetic differentiation of allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839

    Article  PubMed  Google Scholar 

  • Franken F (2002) Demography and metapopulation dynamics of pikas. M.Sc Dissertation, University of Alberta, Edmonton, Canada

  • Franken RJ, Hik DS (2004a) Influence of habitat quality, patch size, and connectivity on colonization and extinction dynamics of collared pikas (Ochotona collaris). J Anim Ecol 73:889–896

    Article  Google Scholar 

  • Franken RJ, Hik DS (2004b) Interannual variation in timing of parturition and growth of collared pikas (Ochotona collaris) in the southwest Yukon. Integr Comp Biol 44:186–193

    Article  PubMed  Google Scholar 

  • Goudet J (1995) Fstat version 1.2: a computer program to calculate F statistics. J Hered 86:485–486

    Google Scholar 

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

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106

    Article  PubMed  Google Scholar 

  • Keller LF, Jeffery KJ, Arcese P, Beaumont MA, Hochachka WM, Smith JNM, Bruford MW (2001) Immigration and the ephemerality of a natural population bottleneck: evidence from molecular markers. Proc Biol Sci 268:1387–1394

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krebs CJ (1996) Cycles revisited. J Mammal 77:8–24

    Article  Google Scholar 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and nonequilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    CAS  PubMed  Google Scholar 

  • McEachern MB, Eadie JM, Van Vuren DH (2007) Local genetic structure and relatedness in a solitary mammal, Neotoma fuscipes. Behav Ecol Sociobiol 61:1459–1469

    Article  Google Scholar 

  • McEachern MB, Van Vuren DH, Floyd CH, May B, Eadie JM (2011) Bottlenecks and rescue effects in a fluctuating population of golden-mantled ground squirrels (Spermophilus lateralis). Conserv Genet 12:285–296

    Article  Google Scholar 

  • McIntire EJB, Hik DS (2005) Influences of chronic and current season grazing by collared pikas on above-ground biomass and species richness in subarctic alpine meadows. Oecologia 145:288–297

    Article  PubMed  Google Scholar 

  • Meshriy MG, Randall JA, Parra L (2011) Kinship associations of a solitary rodent, Dipodomys ingens, at fluctuating population densities. Anim Behav 82:643–650

    Article  Google Scholar 

  • Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008) Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322:261–264

    Article  CAS  PubMed  Google Scholar 

  • Morrison SF, Hik DS (2007) Demographic analysis of a declining pika Ochotona collaris population: linking survival to broad-scale climate patterns via spring snowmelt patterns. J Anim Ecol 76:899–907

    Article  PubMed  Google Scholar 

  • Morrison SF, Hik DS (2008) Discrimination of intra- and inter-specific forage quality by collared pikas (Ochotona collaris). Can J Zool 86:456–461

    Article  Google Scholar 

  • Morrison SF, Pelchat GG, Donahue A, Hik DS (2009) Influence of food hoarding behaviour on the over-winter survival of pikas in strongly seasonal environments. Oecologia 159:107–116

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Paetkau D, Calvert W, Stirling I, Strobeck C (1995) Microsatellite analysis of population structure in Canadian polar bears. Mol Ecol 4:347–354

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Patil VP (2010) The interactive effects of climate, social structure, and life history on the population dynamics of hoary marmots (Marmota caligata). M.Sc Dissertation, University of Alberta, Edmonton, Canada

  • Peacock MM (1997) Determining natal dispersal patterns in a population of North American pikas (Ochotona princeps) using direct mark-resight and indirect genetic methods. Behav Ecol 8:340–350

    Article  Google Scholar 

  • Peacock MM, Smith AT (1997) The effect of habitat fragmentation on dispersal patterns, mating behavior, and genetic variation in a pika (Ochotona princeps) metapopulation. Oecologia 4:524–533

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel: population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Ruibal M, Lindenmayer DB (2003) Spatial autocorrelation analysis offers new insights into gene flow in the Australian bush rat, Rattus fuscipes. Evolution 57:1182–1195

    PubMed  Google Scholar 

  • Pilot M, Dąbrowski MJ, Jancewicz E, Schtickzelle N, Gliwicz J (2010) Temporally stable genetic variability and dynamic kinship structure in a fluctuating population of the root vole Microtus oeconomus. Mol Ecol 19:2800–2812

    Article  PubMed  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 

  • 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  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Říčanová S, Bryja J, Cosson J-F, Gedeon C, Choleva L, Ambros M, Sedláček F (2011) Depleted genetic variation of the European ground squirrel in Central Europe in both microsatellite and the major histocompatibility complex gene: implications for conservation. Conserv Genet 12:1115–1129

    Article  Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62

    Article  Google Scholar 

  • Rubidge EM, Patton JL, Lim M, Burton AC, Brashares JS, Moritz C (2012) Climate-induced range contraction drives genetic erosion in an alpine mammal. Nat Clim Change 2:285–288

    Article  Google Scholar 

  • Smith AT (1987) Population structure of pikas: dispersal versus philopatry. In: Chepko-Sade BD, Halpin ZT (eds) Mammalian dispersal patterns: the effects of social structure on population genetics. The University of Chicago Press, Chicago, pp 128–145

    Google Scholar 

  • Smith AT, Formozov NA, Hoffmann RS, Changlin Z, Erbajeva MA (1990) The pikas. In: Chapman JA, Flux JEC (eds) Rabbits, hares and pikas: status survey and conservation action plan, Chap. 3. IUCN, Gland, pp 14–60

    Google Scholar 

  • Vignieri SN (2007) Cryptic behaviours, inverse genetic landscapes, and spatial avoidance of inbreeding in the Pacific jumping mouse. Mol Ecol 16:853–866

    Article  PubMed  Google Scholar 

  • Vilà C, Sundqvist AK, Flagstad Ø, Seddon J, Björnerfeldt S, Kojola I, Casulli A, Sand H, Wabakken P, Ellegren H (2003) Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant. Proc Natl Acad Sci USA 270:91–97

    Google Scholar 

  • Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215

    CAS  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wilson RJ, Gutiérrez D (2011) Effects of climate change on the elevational limits of species ranges. In: Beever EA, Belant JL (eds) Ecological consequences of climate change: mechanisms, conservation, and management. CRC Press, Boca Raton, pp 107–132

    Chapter  Google Scholar 

  • Winters JB, Waser PM (2003) Gene dispersal and outbreeding in a philopatric mammal. Mol Ecol 12:2251–2259

    Article  CAS  PubMed  Google Scholar 

  • Wright S (1978) Evolution and the genetics of populations. Variability within and among natural populations, vol 4. University of Chicago Press, Chicago

  • Zgurski JM, Hik DS (2012) Polygynandry and even-sexed dispersal in a population of collared pikas, Ochotona collaris. Anim Behav 83:1075–1082

    Article  Google Scholar 

  • Zgurski JM, Davis CS, Hik DS (2009) Isolation and characterization of microsatellite loci for the collared pika (Ochotona collaris) and their cross-amplification in five other Ochotona species. Mol Ecol Resour 9:867–871

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank the staff at the Molecular Biology Service Facility at the University of Alberta for assistance with molecular work, Dr. Jocelyn Hall for use of lab space, Scott Williamson for help preparing Fig. 1, and the many people who have contributed to the collared pika dataset over the years, including John Boulanger, Renee Franken, Shawn Morrison and Kieran O’Donovan. Financial support for D.S.H. was provided by the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canada Foundation for Innovation and the Canada Research Chairs Program. J.M.Z was supported by funding from NSERC, the Alberta Ingenuity Fund, the Northern Studies Training Program, the Canadian Circumpolar Institute and the Department of Biological Sciences. This work was conducted under permits issued by the Yukon and Canadian governments and the University of Alberta. We also thank the Kluane First Nation for permission to conduct research on their traditional territory.

Author information

Authors and Affiliations

  1. Department of Biological Sciences, University of Alberta, Edmonton, AB, Canada

    J. M. Zgurski & D. S. Hik

Authors
  1. J. M. Zgurski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. S. Hik
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. M. Zgurski.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 53 kb)

Supplementary material 2 (DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zgurski, J.M., Hik, D.S. Gene flow and the restoration of genetic diversity in a fluctuating collared pika (Ochotona collaris) population. Conserv Genet 15, 37–48 (2014). https://doi.org/10.1007/s10592-013-0519-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-013-0519-2

Keywords

Search

Navigation