Skip to main content

Advertisement

SpringerLink
Log in

Genetic variation and fine-scale population structure in American pikas across a human-modified landscape

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

Abstract

Natural resource extraction can represent a major human modification to the landscape. Habitat reclamation is becoming an increasingly important strategy for abating the loss of biodiversity associated with these developments; however, the demographic and genetic consequences of colonizing artificial habitat remain unknown in many species. Here, we investigated the genetic consequences of landscape modifications for the American pika (Ochotona princeps) relative to two major developments in British Columbia, Canada: a large open-pit copper mine (Highland Valley Copper) under partial reclamation and a bisecting major highway (97C). We assessed microsatellite genotypic data for 109 individuals across 15 sites located either within the mine on artificial habitat or on adjacent natural habitat both north and south of the highway. There were no significant differences in levels of heterozygosity, allelic richness or inbreeding between natural (n = 7) and artificial sites (n = 8). However, pikas residing on artificial habitat exhibited significantly higher relatedness estimates. Bayesian clustering analyses revealed two distinct genetic units corresponding to north and south of the highway, with further substructure detected in the south. Likewise, high genetic friction was detected in the central region of the area, largely corresponding to the highway and modified landscape associated with the mine. At a finer scale, pairwise estimates of differentiation and migration rates suggest little gene flow may be occurring among sites across the sampling area, with some evidence for directional migration from artificial to natural sites. Overall, artificial habitat has been successful in promoting occupancy for American pikas, however, barriers to gene flow likely associated with resource extraction and road construction limit connectivity across the landscape.

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

  • Baguette M, Mennechez G, Petit S, Schtickzelle N (2003) Effect of habitat fragmentation on dispersal in the butterfly Proclossiana eunomia. C R Biol 326:200–209. doi:10.1016/S1631-0691(03)00058-1

    Article  Google Scholar 

  • Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164. doi:10.1111/j.1365-294X.2009.04322.x

    Article  PubMed  Google Scholar 

  • Beever EA, Ray C, Mote PW, Wilkening JL (2010) Testing alternative models of climate-mediated extirpations. Ecol Appl 20:164–178. doi:10.1890/08-1011.1

    Article  PubMed  Google Scholar 

  • Beever EA, Dobrowski SZ, Long J et al (2013) Understanding relationships among abundance, extirpation, and climate at ecoregional scales. Ecology 94:1563–1571. doi:10.1890/12-2174.1

    Article  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L et al (2004) Genetix 4.05, logiciel sous Windows TM pour la génétique des populations. Lab. génome Popul. Interact. CNRS Umr 5000. Univ. Montpellier II, Montpellier

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Serise B 57:289–300

    Google Scholar 

  • Bloodgood MA, Gizikoff KG, Jones CE (1998) Biosolids amendment of waste rock and tailings as reclamation treatment at Highland Valley Copper. In: 22nd British Columbia Mine Reclamation Symposium. Penticton, BC, Canada, pp 15–25

  • British Columbia Ministry of Transportation and Highways (2009) British Columbia Traffic Data Program. In: Traffic data Logan lake–28-950NS-N. http://www.th.gov.bc.ca/trafficData/TRADAS/tradas.asp?loc=28-950NS

  • Buchmann CM, Schurr FM, Nathan R, Jeltsch F (2013) Habitat loss and fragmentation affecting mammal and bird communities: the role of interspecific competition and individual space use. Ecol Inform 14:90–98. doi:10.1016/j.ecoinf.2012.11.015

    Article  Google Scholar 

  • Castillo JA, Epps CW, Davis AR, Cushman SA (2014) Landscape effects on gene flow for a climate-sensitive montane species, the American pika. Mol Ecol 23:843–856. doi:10.1111/mec.12650

    Article  PubMed  Google Scholar 

  • Duforet-Frebourg N, Blum MGB (2014) Nonstationary patterns of isolation-by-distance: inferring measures of local genetic differentiation with bayesian kriging. Evolution (NY) 68:1110–1123. doi:10.1111/evo.12342

    Article  Google Scholar 

  • Durka W (1999) Genetic diversity in peripheral and subcentral populations of Corrigiola litoralis L. (Illecebraceae). Heredity 83:476–484. doi:10.1038/sj.hdy.6886000

    Article  CAS  PubMed  Google Scholar 

  • Earl DA, VonHoldt BM (2011) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conserv Genet Resour 4:359–361. doi:10.1007/s12686-011-9548-7

    Article  Google Scholar 

  • Eaton BR, Fisher JT, McKenna GT, Pollard J (2014) An ecological framework for wildlife habitat design for oil sands mine reclamation. Oil Sands Research and Information Network, University of Alberta, School of Energy and the Environment, Edmonton, Alberta. OSRIN Report No. TR-67. 83

  • Eckert CG, Samis KE, Lougheed SC (2008) Genetic variation across species’ geographical ranges: the central-marginal hypothesis and beyond. Mol Ecol 17:1170–1188. doi:10.1111/j.1365-294X.2007.03659.x

    Article  CAS  PubMed  Google Scholar 

  • Estes-Zumpf WA, Rachlow JL, Waits LP, Warheit KI (2010) Dispersal, gene flow, and population genetic structure in the pygmy rabbit (Brachylagus idahoensis). J Mammal 91:208–219. doi:10.1644/09-MAMM-A-032R.1

    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. doi:10.1111/j.1365-294X.2005.02553.x

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi:10.1111/j.1755-0998.2010.02847.x

    Article  PubMed  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. doi:10.1111/j.1466-8238.2006.00287.x

    Article  Google Scholar 

  • Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508

    Article  Google Scholar 

  • Freberg MR, Gizikoff KG (1999) Development and utilization of an end land use plan for highland valley copper. In: Proceendings of the 23rd Annual British Columbia Mine Reclamation Symposium. Kamploops, BC, Canada, pp 46–56

  • Gaines MS, Diffendorfer JE, Tamarin RH, Whitttam TS (1997) The effects of habitat fragmentation on the genetic structure of small mammal populations. J Hered 88:294–304

    Article  CAS  PubMed  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy-Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  CAS  PubMed  Google Scholar 

  • Hafner DJ, Sullivan RM (1995) Historical and ecological biogeography of neararctic pikas (Lagomorpha: Ochotonidae). J Mammal 76:302–321

    Article  Google Scholar 

  • Henry P, Sim Z, Russello MA (2012) Genetic evidence for restricted dispersal along continuous altitudinal gradients in a climate change-sensitive mammal: the American pika. PLoS One 7:e39077. doi:10.1371/journal.pone.0039077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howie R (2007) Habitat locations for the American pika (Ochotona princeps) in the Highmont area. Aspen Park Consult Kamploops, BC, Canada 1–13

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service. BMC Genet 6:13. doi:10.1186/1471-2156-6-13

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalinowski ST (2005) Hp-Rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189. doi:10.1111/j.1471-8286.2004.00845.x

    Article  CAS  Google Scholar 

  • Keyghobadi N (2007) The genetic implications of habitat fragmentation for animals. Can J Zool 85:1049–1064. doi:10.1139/Z07-095

    Article  Google Scholar 

  • Kreuzer MP, Huntly NJ (2003) Habitat-specific demography: evidence for source-sink population structure in a mammal, the pika. Oecologia 134:343–349. doi:10.1007/s00442-002-1145-8

    Article  CAS  PubMed  Google Scholar 

  • Lamb CT, Robson KM, Russello MA (2013) Development and application of a molecular sexing protocol in the climate change-sensitive American pika. Conserv Genet Resour 6:17–19. doi:10.1007/s12686-013-0034-2

    Article  Google Scholar 

  • Leberg PL (2002) Estimating allelic richness: effects of sample size. Mol Ecol 11:2445–2449

    Article  CAS  PubMed  Google Scholar 

  • Lesica P, Allendorf FW (1995) When are peripheral valuable populations for conservation? Conserv Biol 9:753–760

    Article  Google Scholar 

  • Martínez-Cruz B, Godoy JA, Negro JJ (2007) Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Mol Ecol 16:477–486. doi:10.1111/j.1365-294X.2007.03147.x

    Article  PubMed  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Harvard Univeristy Press, Cambridge, MA

    Book  Google Scholar 

  • Meredith SJ (2002) The impact of habitat spatial structure on pika (Ochotona princeps) dispersal dynamics. University of Nevada, Reno, NV

    Google Scholar 

  • Moilanen A, Smith AT, Hanski I (1998) Long-term dynamics in a metapopulation of the American pika. Am Nat 152:530–542. doi:10.1086/286188

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286

    Article  CAS  PubMed  Google Scholar 

  • 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 (1997a) Nonrandom mating in pikas Ochotona princeps: evidence for inbreeding between individuals of intermediate relatedness. Mol Ecol 6:801–811

  • Peacock MM, Smith AT (1997b) The effect of habitat fragmentation on dispersal patterns, mating behavior, and genetic variation in a pika (Ochotona princeps) metapopulation. Oecologia 112:524–533

  • Peacock MM, Kirchoff VS, Merideth SJ (2002) Identification and characterization of nine polymorphic microsatellite loci in the North American pika, Ochotona princeps. Mol Ecol Notes 2:360–362. doi:10.1046/j.1471-8278

    Article  CAS  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. doi:10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

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

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Soc Study Evol 43:258–275

    Google Scholar 

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

    Article  Google Scholar 

  • R Core Team (2015) R: A language and environment for statstical computing, Vienna, Austria. https://www.R-project.org/

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution Int J org Evolution 43:223–225

    Article  Google Scholar 

  • Robson KM, Lamb CT, Russello MA (2016) Low genetic diversity, restricted dispersal and elevation-specific patterns of population decline in American pikas in an atypical environment. J Mammal 1–9. doi:10.1093/jmammal/gyv191

  • Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. doi:10.1111/j.1471-8286.2007.01931.x

    Article  PubMed  Google Scholar 

  • Ruiz-Jaen MC, Aide TM (2005) Restoration success: how is it being measured? Restor Ecol 13:569–577. doi:10.1111/j.1526-100X.2005.00072.x

    Article  Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32

    Article  Google Scholar 

  • Sauvajot RM, Buechner M, Kamradt DA, Schonewald CM (1998) Patterns of human disturbance and response by small mammals and birds in chaparral near urban development. Urban Ecosyst 2:279–297

    Article  Google Scholar 

  • Sgrò CM, Lowe AJ, Hoffmann AA (2011) Building evolutionary resilience for conserving biodiversity under climate change. Evol Appl 4:326–337. doi:10.1111/j.1752-4571.2010.00157.x

    Article  PubMed  Google Scholar 

  • Smith AT (1974) The distribution and dispersal of pikas: influences of behavior and climate. Ecology 55:1368–1376

    Article  Google Scholar 

  • Smith AT (1980) Temporal changes in insular populations of the pika (Ochotona princeps). Ecology 61:8–13. doi:10.2307/1937147

    Article  Google Scholar 

  • Smith AT, Weston ML (1990) Ochotona princeps. Am Soc Mammal 352:1–8

    Google Scholar 

  • Smith O, Wang J (2014) When can noninvasive samples provide sufficient information in conservation genetics studies? Mol Ecol Resour 14:1011–1023. doi:10.1111/1755-0998.12250

    CAS  PubMed  Google Scholar 

  • Stewart JAE, Perrine JD, Nichols LB et al (2015) Revisiting the past to foretell the future: summer temperature and habitat area predict pika extirpations in California. J Biogeogr n/a–n/a. doi:10.1111/jbi.12466

    Google Scholar 

  • Teck Resources Limited (2012) Generations: Teck Sustainability Report. Vancouver, BC, Canada

  • 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. doi:10.1111/j.1471-8286.2004.00684.x

    Article  Google Scholar 

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

    CAS  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Richard Doucette (Teck) for support during this project, Evelyn Jensen and Andrew Veale for feedback on analysis, Ashley Boksteyn for her assistance with lab work, Amber Merko and Eric Spilker for their assistance in the field, and Kelly Klinger and Mary Peacock for sharing unpublished data. Funding for this work was provided by Teck Resources Ltd. to KL and the Natural Sciences and Engineering Research Council of Canada to MR (Discovery Grant # 341711).

Author information

Authors and Affiliations

  1. Department of Biology, University of British Columbia, Okanagan Campus, 3247 University Way, Kelowna, BC, V1V 1V7, Canada

    Matthew D. Waterhouse & Michael A. Russello

  2. Department of Natural Resource Sciences, Thompson Rivers University, 900 McGill Road, Kamloops, BC, V2C 0C8, Canada

    Cheryl Blair & Karl W. Larsen

Authors
  1. Matthew D. Waterhouse
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheryl Blair
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karl W. Larsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michael A. Russello
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael A. Russello.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 53 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Waterhouse, M.D., Blair, C., Larsen, K.W. et al. Genetic variation and fine-scale population structure in American pikas across a human-modified landscape. Conserv Genet 18, 825–835 (2017). https://doi.org/10.1007/s10592-017-0930-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-017-0930-1

Keywords

Search

Navigation