Skip to main content

Advertisement

SpringerLink
Log in

Forest cover mediates genetic connectivity of northwestern cougars

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

Abstract

Population structure, connectivity, and dispersal success of individuals can be challenging to demonstrate for solitary carnivores with low population densities. Though the cougar (Puma concolor) is widely distributed throughout North America and is capable of dispersing long distances, populations can be geographically structured and genetic isolation has been documented in some small populations. We described genetic structure and explored the relationship between landscape resistance and genetic variation in cougars in Washington and southern British Columbia using allele frequencies of 17 microsatellite loci for felids. We evaluated population structure of cougars using the Geneland clustering algorithm and spatial principal components analysis. We then used Circuitscape to estimate the landscape resistance between pairs of individuals based on rescaled GIS layers for forest canopy cover, elevation, human population density and highways. We quantified the effect of landscape resistance on genetic distance using multiple regression on distance matrices and boosted regression tree analysis. Cluster analysis identified four populations in the study area. Multiple regression on distance matrices and boosted regression tree models indicated that only forest canopy cover and geographic distance between individuals had an effect on genetic distance. The boundaries between genetic clusters largely corresponded with breaks in forest cover, showing agreement between population structure and genetic gradient analyses. Our data indicate that forest cover promotes gene flow for cougars in the Pacific Northwest, which provides insight managers can use to preserve or enhance genetic connectivity.

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
Fig. 6

Similar content being viewed by others

References

  • Anderson CR Jr, Lindzey FG, McDonald DB (2004) Genetic structure of cougar populations across the Wyoming Basin: metapopulation or megapopulation? J Mammal 85:1207–1214

    Article  Google Scholar 

  • Andreasen AM, Stewart KM, Longland WS, Beckmann JP, Forister ML (2012) Identification of source–sink dynamics in mountain lions of the Great Basin. Mol Ecol 21:5689–5701

    Article  PubMed  Google Scholar 

  • Balkenhol N (2009) Evaluating and improving analytical approaches in landscape genetics through simulations and wildlife case studies. Dissertation, University of Idaho, Moscow

  • Balkenhol N, Waits LP (2009) Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol Ecol 18:4151–4164

    Article  PubMed  Google Scholar 

  • Balkenhol N, Waits LP, Dezzani RJ (2009) Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data. Ecography 32:818–830

    Article  Google Scholar 

  • Balkenhol N, Holbrook JD, Onorato D, Zager P, White C, Waits LP (2014) A multi-method approach for analyzing hierarchical genetic structures: a case study with cougars Puma concolor. Ecography 37:1–12

    Article  Google Scholar 

  • Beausoleil RA, Warheit KI (2015) Using DNA to evaluate field identification of cougar sex by agency staff and hunters using trained dogs. Wildl Soc Bull 39:203–209

    Article  Google Scholar 

  • Beausoleil RA, Dawn D, Martorello DA, Morgan CP (2008) Cougar management protocols: a survey of wildlife agencies in North America. In: Toweill D, Nadeau S, Smith D (eds) Proceedings of the ninth Mountain Lion workshop. Idaho Department of Fish and Game, Boise, pp 205–241

    Google Scholar 

  • Beier P (1995) Dispersal of juvenile cougars in fragmented habitat. J Wildl Manag 59:228–237

    Article  Google Scholar 

  • Beier P (2010) A focal species for conservation planning. In: Hornocker MG, Negri S (eds) Cougar: ecology and conservation. University of Chicago Press, Chicago, pp 177–189

    Google Scholar 

  • Castilho CS, Marins-Sá LG, Benedet RC, Freitas TO (2011) Landscape genetics of mountain lions (Puma concolor) in southern Brazil. Mamm Biol 76:476–483

    Google Scholar 

  • Cooley HS, Wielgus RB, Koehler G, Maletzke B (2009) Source populations in carnivore management: cougar demography and emigration in a lightly hunted population. Anim Conserv 12:321–328

    Article  Google Scholar 

  • Crown Registry and Geographic Base (2012) Products—gridded DEMs. http://archive.ilmb.gov.bc.ca/crgb/products/imagery/gridded.htm

  • Culver M (1999) Molecular genetic variation, population structure, and natural history of free-ranging pumas (Puma concolor). Dissertation, University of Maryland, College Park

  • Culver M, Johnson WE, Pecon-Slattery J, O’Brien SJ (2000) Genomic ancestry of the American puma (Puma concolor). J Hered 91:186–197

    Article  CAS  PubMed  Google Scholar 

  • Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499

    Article  PubMed  Google Scholar 

  • Dickson BG, Beier P (2002) Home-range and habitat selection by adult cougars in southern California. J Wildl Manag 66:1235–1245

    Article  Google Scholar 

  • Dickson BG, Beier P (2007) Quantifying the influence of topographic position on cougar (Puma concolor) movement in southern California, USA. J Zool 271:270–277

    Google Scholar 

  • Dickson BG, Jenness JS, Beier P (2005) Influence of vegetation, topography, and roads on cougar movement in southern California. J Wildl Manag 69:264–276

    Article  Google Scholar 

  • Elbroch LM, Wittmer HU (2012) Puma spatial ecology in open habitats with aggregate prey. Mamm Biol 77:377–384

    Google Scholar 

  • Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813

    Article  CAS  PubMed  Google Scholar 

  • Ernest HB, Boyce WM, Bleich VC, May B, Stiver SJ, Torres SG (2003) Genetic structure of mountain lion (Puma concolor) populations in California. Conserv Genet 4:353–366

    Article  CAS  Google Scholar 

  • Fox J, Weisberg S (2011) An R Companion to Applied Regression, 2nd edn. Sage, Thousand Oaks

    Google Scholar 

  • Gabriel KR, Sokal RR (1969) A new statistical approach to geographic variation analysis. Syst Zool 18:259–278

    Article  Google Scholar 

  • Garroway CJ, Bowman J, Wilson PJ (2011) Using a genetic network to parameterize a landscape resistance surface for fishers, Martes pennanti. Mol Ecol 20:3978–3988

    Article  PubMed  Google Scholar 

  • Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19

    Article  Google Scholar 

  • Graves TA, Wasserman TN, Ribeiro MC, Landguth EL, Spear SF, Balkenhol N, Higgins CB, Fortin MJ, Cushman SA, Waits LP (2012) The influence of landscape characteristics and home-range size on the quantification of landscape-genetics relationships. Landsc Ecol 27:253–266

    Article  Google Scholar 

  • Guillot G, Estoup A, Mortier F, Cosson JF (2005) A spatial statistical model for landscape genetics. Genetics 170:1261–1280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holbrook JD, DeYoung RW, Janecka JE, Tewes ME, Honeycutt RL, Young JH (2012) Genetic diversity, population structure, and movements of mountain lions (Puma concolor) in Texas. J Mammal 93:989–1000

    Article  Google Scholar 

  • Hornocker M, Negri S (2010) Cougar: ecology and conservation. University of Chicago Press, Chicago

    Google Scholar 

  • Jombart T, Devillard S, Dufour AB, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103

    Article  CAS  PubMed  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Kertson BN, Spencer RD, Marzluff JM, Hepinstall-Cymerman J, Grue CE (2011) Cougar space use and movements in the wildland-urban landscape of western Washington. Ecol Appl 21:2866–2881

    Article  Google Scholar 

  • Koen EL, Garroway CJ, Wilson PJ, Bowman J (2010) The effect of map boundary on estimates of landscape resistance to animal movement. PLoS ONE 5:e11785

    Article  PubMed  PubMed Central  Google Scholar 

  • Legendre P, Fortin MJ (2010) Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data. Mol Ecol Resour 10:831–844

    Article  PubMed  Google Scholar 

  • Legendre P, Lapointe FJ, Casgrain P (1994) Modeling brain evolution from behavior: a permutational regression approach. Evolution 48:1487–1499

    Article  Google Scholar 

  • Logan KA, Irwin LL (1985) Mountain lion habitats in the Big Horn Mountains, Wyoming. Wild Soc Bull 13:257–262

    Google Scholar 

  • Logan KA, Sweanor LL (2010) Behavior and social organization of a solitary carnivore. In: Hornocker M, Negri S (eds) Cougar ecology and conservation. University of Chicago Press, Chicago, pp 105–117

    Google Scholar 

  • Loxterman JL (2010) Fine scale population genetic structure of pumas in the Intermountain West. Conserv Genet 12:1049–1059

    Article  Google Scholar 

  • Maletzke BT (2010) Effects of anthropogenic disturbance on landscape ecology of cougars. Dissertation, Washington State University, Pullman

  • Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197

    Article  Google Scholar 

  • Marquardt DW (1970) Generalized inverses, ridge regression and biased linear estimation. Technometrics 12:591–612

    Article  Google Scholar 

  • McRae BH (2006) Isolation by resistance. Evolution 60:1551–1561

    Article  PubMed  Google Scholar 

  • McRae BH, Shah VB (2011) Circuitscape User Guide. The University of California, Santa Barbara

    Google Scholar 

  • McRae BH, Beier P, Dewald LE, Huynh LY, Keim P (2005) Habitat barriers limit gene flow and illuminate historical events in a wide-ranging carnivore, the American puma. Mol Ecol 14:1965–1977

    Article  CAS  PubMed  Google Scholar 

  • McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  • Menotti-Raymond MA, O’Brien SJ (1995) Evolutionary conservation of ten microsatellite loci in four species of Felidae. J Hered 86:319–322

    CAS  PubMed  Google Scholar 

  • Menotti-Raymond MA, David VA, Lyons LA, Schaffer AA, Tomlin JF, Hutton MK, O’Brien SJ (1999) A genetic linkage map of microsatellites in the domestic cat (Felis catus). Genomics 57:9–23

    Article  CAS  PubMed  Google Scholar 

  • Miotto RA, Cervini M, Figueiredo MG, Begotti RA, Galetti PM Jr (2011) Genetic diversity and population structure of pumas (Puma concolor) in southeastern Brazil: implications for conservation in a human-dominated landscape. Conserv Genet 12:1447–1455

    Article  Google Scholar 

  • Musial TS (2009) Evolutionary and landscape genetic structure of Puma concolor in Oregon. Portland State University, Portland, Oregon, Thesis

    Google Scholar 

  • Naidu, A (2015) Where mountain lions traverse: Insights from landscape genetics in southwestern United States and northwestern Mexico. Dissertation, University of Arizona, Tucson

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Newby J (2011) Puma Dispersal Ecology in the Central Rocky Mountains. University of Montana, Missoula, Montana, Thesis

    Google Scholar 

  • Park SDE (2001) Trypanotolerance in west African cattle and the population genetic effects of selection. Dissertation, University of Dublin

  • Parks LC, Wallin DO, Cushman SA, McRae BH (2015) Landscape-level analysis of mountain goat population connectivity in Washington and southern British Columbia. Conserv Genet 16:1195–1207

    Article  Google Scholar 

  • Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e2074–e2093

    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 

  • Pimm SL, Dollar L, Bass OL Jr (2006) The genetic rescue of the Florida panther. Anim Conserv 9:115–122

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Ridgeway G (2013) gbm: generalized boosted regression models. R package version 2.0-8. http://CRAN.R-project.org/package=gbm

  • Riley SPD, Pollinger JP, Sauvajot RM, York EC, Bromley C, Fuller TK, Wayne RK (2006) FAST-TRACK: a southern California freeway is a physical and social barrier to gene flow in carnivores. Mol Ecol 15:1733–1741

    Article  CAS  PubMed  Google Scholar 

  • Robinson HS, Wielgus RB, Cooley HS, Cooley SW (2008) Sink populations in carnivore management: cougar demography and immigration in a hunted population. Ecol Appl 18:1028–1037

    Article  PubMed  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 

  • Seidensticker JC IV, Hornocker MG, Wiles WV, Mesnick JP (1973) Mountain lion social organization in the Idaho Primitive Area. Wildlife Monogr 35:3–60

    Google Scholar 

  • Shirk AJ, Wallin DO, Cushman SA, Rice CG, Warheit KI (2010) Inferring landscape effects on gene flow: a new model selection framework. Mol Ecol 19:3603–3619

    Article  CAS  PubMed  Google Scholar 

  • Sinclair EA, Swenson EL, Wolfe ML, Choate DC, Bates B, Crandall KA (2001) Gene flow estimates in Utah’s cougars imply management beyond Utah. Anim Conserv 4:257–264

    Article  Google Scholar 

  • Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142

    Article  CAS  PubMed  Google Scholar 

  • Sweanor LL, Logan KA, Hornocker MG (2000) Cougar dispersal patterns, metapopulation dynamics, and conservation. Conserv Biol 14:798–808

    Article  Google Scholar 

  • Taylor S, Buergelt C, Roelke-Parker M, Homer B, Rotstein D (2002) Causes of mortality of free-ranging Florida panthers. J Wildlife Dis 38:107–114

    Article  Google Scholar 

  • United States Geological Survey (USGS) (2012) Seamless Data Warehouse. http://seamless.usgs.gov/index.php/. Retrieved 28 Mar 2012

  • van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Resour 4:535–538

    Article  Google Scholar 

  • Walker CW, Harveson LA, Pittman MT, Tewes ME, Honeycutt RL (2000) Microsatellite variation in two populations of mountain lions (Puma concolor) in Texas. Southwest Nat 45:196–203

    Article  Google Scholar 

  • Washington Department of Fish and Widlife (WDFW) (2011) 2011 Game status and trend report. Wildlife Program, Washington Department of Fish and Wildlife, Olympia

  • Washington State Department of Transportation (WSDOT) (2012) Washington State Department of Transportation geodata catalog. http://www.wsdot.wa.gov/Mapsdata/geodatacatalog/. Retrieved 12 Apr 2012

  • Washington Wildlife Habitat Connectivity Working Group (WHCWG) (2010) Washington connected landscapes project: statewide analysis. Washington Department of Fish and Wildlife and Washington Department of Transportation, Olympia. http://waconnected.org/statewide-analysis/

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

    Article  Google Scholar 

Download references

Acknowledgments

We thank Washington Department of Fish and Wildlife (WDFW) staff for diligently collecting samples from all known cougar mortalities for use in this project. Also, thanks to Cathy Lacey and Brian Harris with British Columbia Ministry of Forests, Lands and Natural Resource Operations and compulsory inspectors for assistance in BC. All genotyping was performed by WDFW’s Molecular Genetics Laboratory in Olympia, Washington. We would also like to thank Spencer Houck and Heidi Rodenhizer for assistance with GIS processing. Finally, we thank the following hound handlers for volunteering their time and expertise on research projects: R. Eich, B. Heath, K. Lester, D Likens, T. MacArthur, K. Reber, S. Reynaud, C. Sanchez, B. Smith, C. Smith, M. Thorniley, B. Thorniley, and B. Trudell and M. White. Washington State General and Wildlife Funds were used in part to fund the production of the genetic data. Funding for this project was provided by WDFW, Seattle City Light, Washington Chapter of the Wildlife Society, North Cascades Audubon Society, and Huxley College of the Environment.

Author information

Authors and Affiliations

  1. Oregon Department of Fish and Wildlife, 1401 Gekeler Lane, La Grande, OR, 97850, USA

    Matthew J. Warren

  2. Department of Environmental Sciences, Huxley College of the Environment, Western Washington University, 516 High Street, Bellingham, WA, 98225-9181, USA

    David O. Wallin

  3. Washington Department of Fish and Wildlife, 3515 State Highway 97A, Wenatchee, WA, 98801, USA

    Richard A. Beausoleil

  4. Washington Department of Fish and Wildlife, 600 Capitol Way N., Olympia, WA, 98501, USA

    Kenneth I. Warheit

Authors
  1. Matthew J. Warren
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David O. Wallin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard A. Beausoleil
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kenneth I. Warheit
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew J. Warren.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Warren, M.J., Wallin, D.O., Beausoleil, R.A. et al. Forest cover mediates genetic connectivity of northwestern cougars. Conserv Genet 17, 1011–1024 (2016). https://doi.org/10.1007/s10592-016-0840-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0840-7

Keywords

Search

Navigation