Abstract
Human-driven habitat fragmentation is increasing worldwide, and consequently many wild populations are subdivided, isolated and reduced in size. These changes in population structure reduce dispersal among subpopulations, limiting gene flow, accelerating genetic differentiation, and reducing genetic diversity and effective population sizes. Habitat fragmentation is associated with a reduced ability for populations and species to respond to changing environments, exacerbating extinction risks. The Atlantic-Gaspésie population of woodland caribou (Rangifer tarandus caribou) is isolated and genetically differentiated from other populations in Canada. It has been declining dramatically during the last century and is now considered Endangered. From a management perspective, this population is considered as a single unit of ~ 80 individuals, but GPS telemetry suggests that three subgroups use separate geographical areas and show limited dispersal. In this study, we used 16 microsatellite loci to (1) quantify and compare the genetic diversity observed within the three subgroups of the Atlantic-Gaspésie population, (2) evaluate the extent of the spatiotemporal genetic substructure among them by assessing whether the fine-scale genetic structure differs between subgroups and if it has changed over 15 years, and (3) estimate their effective population size. We found no change in genetic diversity among/within subgroups over time. We detected genetic substructure among subgroups based on their geographical locations (Logan-Albert vs. McGerrigle) and found evidence that this substructure has increased in recent years. The effective population size of this population appears to have declined by 53% over the last 15 years and is now estimated at Ne = 16 individuals. Management plans and conservation actions should consider this spatial genetic substructure to prevent further decline of this endangered population.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Apps CD, McLellan BN, Kinley TA, Flaa JP (2001) Scale-dependent habitat selection by mountain caribou, Columbia Mountains, British Columbia. J Wildl Manage 65:65–77. https://doi.org/10.2307/3803278
Archer FI, Adams PE, Schneiders BB (2017) Stratag: an r package for manipulating, summarizing and analysing population genetic data. Mol Ecol Resour 17:5–11. https://doi.org/10.1111/1755-0998.12559
Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv:14065823 [stat]
Bauduin S, McIntire E, St-Laurent M-H, Cumming S (2016) Overcoming challenges of sparse telemetry data to estimate caribou movement. Ecol Model 335:24–34. https://doi.org/10.1016/J.ECOLMODEL.2016.05.004
Bergerud AT, Mercer WE (1989) Caribou introductions in Eastern North America. Wildl Soc Bull 17:111–120
Bijlsma R, Loeschcke V (2012) Genetic erosion impedes adaptive responses to stressful environments. Evol Appl 5:117–129. https://doi.org/10.1111/j.1752-4571.2011.00214.x
Bishop MD, Kappes SM, Keele JW et al (1994) A genetic linkage map for cattle. Genetics 136:619–639
Boudreau F (1981) Écologie des étages alpin et subalpin du Mont Jacques-Cartier, parc de la Gaspésie, Québec. Université Laval, Master’s Thesis [in French]
Boudreau M (2017) Impacts de 25 ans d’aménagement forestier intensif sur l’habitat du caribou de la Gaspésie et de ses prédateurs. Université du Québec à Rimouski, Master’s Thesis [in French]
Buchanan FC, Crawford AM (1993) Ovine microsatellites at the OarFCB11, OarFCB128, OarFCB193, OarFCB266 and OarFCB304 loci. Anim Genet 24:145
Bürger R, Lynch M (1995) Evolution and extinction in a changing environmnent: a quantitative-genetic analysis. Evolution 49:151–163. https://doi.org/10.1111/j.1558-5646.1995.tb05967.x
Christopherson V (2018) Compétition pour les ressources alimentaires entre le caribou et l’orignal en Gaspésie. Université du Québec à Rimouski, Master’s Thesis [in French]
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
COSEWIC (2011) Designatable units for caribou (Rangifer tarandus) in Canada. Committee on the status of endangered wildlife in Canada, Ottawa
Courtois R, Bernatchez L, Ouellet J-P, Breton L (2003) Significance of caribou (Rangifer tarandus) ecotypes from a molecular genetics viewpoint. Conserv Genet 4:393–404. https://doi.org/10.1023/A:1024033500799
DeCesare NJ, Hebblewhite M, Robinson HS, Musiani M (2010) Endangered, apparently: the role of apparent competition in endangered species conservation. Anim Conserv 13:353–362. https://doi.org/10.1111/j.1469-1795.2009.00328.x
Do C, Waples RS, Peel D et al (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214. https://doi.org/10.1111/1755-0998.12157
ESRI (2011) ArcGIS Desktop: Release 10. Environmental Systems Research Institute, Redlands
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
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. https://doi.org/10.1111/j.1755-0998.2010.02847.x
Fountain T, Nieminen M, Sirén J et al (2016) Predictable allele frequency changes due to habitat fragmentation in the Glanville fritillary butterfly. Proc Natl Acad Sci USA 113:2678–2683. https://doi.org/10.1073/pnas.1600951113
Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327. https://doi.org/10.1146/annurev.ge.29.120195.001513
Frankham R (1995b) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107. https://doi.org/10.1017/S0016672300034455
Frankham R (1996) Relationship of genetic variation to population size in wildlife. Conserv Biol 10:1500–1508. https://doi.org/10.1046/j.1523-1739.1996.10061500.x
Frankham R, Ballou JD, Briscoe DA, Mcinness KH (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: Revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63. https://doi.org/10.1016/j.biocon.2013.12.036
Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–70. https://doi.org/10.1111/j.1469-1795.1998.tb00228.x
Fraser DJ, Bernatchez L (2001) Adaptive evolutionary conservation: towards a unified concept for defining conservation units. Mol Ecol 10:2741–2752. https://doi.org/10.1046/j.0962-1083.2001.01411.x
Frenette J (2017) Démographie et viabilité de la population de caribous de la Gaspésie-Atlantique. Université du Québec à Rimouski, Master’s Thesis [in French]
Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443. https://doi.org/10.1111/j.1365-2435.2006.01228.x
Gaudry W (2013) Impact des structures anthropiques linéaires sur la sélection d’habitat du caribou, de l’ours noir et du coyote en Gaspésie. Université du Québec à Rimouski, Master’s Thesis [in French]
Georges S, Rivard G, Lemay G (1976) Détermination de l’aire de distribution du caribou (rangifer tarandus) dans le parc de la Gaspésie et ce en fonction de l’utilisation optimale de la matière ligneuse. Ministère du tourisme, de la chasse et de la pêche. District Bas Saint-Laurent-Gaspésie [in French]
Gienapp P, Lof M, Reed TE et al (2012) Predicting demographically sustainable rates of adaptation: can great tit breeding time keep pace with climate change? Philos Trans R Soc B 368:20120289–20120289. https://doi.org/10.1098/rstb.2012.0289
Goudet J, Jombart T (2015) Hierfstat: estimation and tests of hierarchical F-statistics, R package version 0.04-22
Halverson K, Heard SB, Nason JD, Stireman JO (2008) Origins, distribution, and local co-occurrence of polyploid cytotypes in Solidago altissima (Asteraceae). Am J Bot 95:50–58. https://doi.org/10.3732/ajb.95.1.50
Hogg JT, Forbes SH, Steele BM, Luikart G (2006) Genetic rescue of an insular population of large mammals. Proc R Soc Lond B 273:1491–1499. https://doi.org/10.1098/rspb.2006.3477
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Jombart T, Ahmed I (2011) Adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. https://doi.org/10.1093/bioinformatics/btr521
Jones KC, Levine KF, Banks JD (2000) DNA-based genetic markers in black-tailed and mule deer for forensic applications. Calif Fish Game 86:115–126
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241
Kinley TA, Apps CD (2001) Mortality patterns in a subpopulation of endangered mountain caribou. Wildl Soc Bull 29:158–164
Lalonde M (2015) Inventaire aérien de la population de caribou de la Gaspésie (Rangifer tarandus caribou). Ministère des Forêts, de la Faune et des Parcs, Secteur de la faune et des parcs, Direction de la gestion de la faune de la Gaspésie—Îles-de-la-Madeleine [in French]
Lalonde M, Michaud J (2013) Inventaire aérien de la population de caribou de la Gaspésie (Rangifer tarandus caribou), Automne 2012, Ministère des Ressources naturelles du Québec [in French]
Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460
Lane JE, Kruuk LEB, Charmantier A et al (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489:554–557. https://doi.org/10.1038/nature11335
Lanfear R, Kokko H, Eyre-Walker A (2014) Population size and the rate of evolution. Trends Ecol Evol 29:33–41. https://doi.org/10.1016/J.TREE.2013.09.009
Lauzon È, Kneeshaw D, Bergeron Y (2007) Reconstruction of fire history (1680–2003) in Gaspesian mixedwood boreal forests of eastern Canada. For Ecol Manage 244:41–49. https://doi.org/10.1016/J.FORECO.2007.03.064
Lesmerises F, Johnson CJ, St-Laurent M-H (2017) Refuge or predation risk? Alternate ways to perceive hiker disturbance based on maternal state of female caribou. Ecol Evol 7:845–854. https://doi.org/10.1002/ece3.2672
Lesmerises F, Déry F, Johnson CJ, St-Laurent M-H (2018) Spatiotemporal response of mountain caribou to the intensity of backcountry skiing. Biol Conserv 217:149–156. https://doi.org/10.1016/J.BIOCON.2017.10.030
Luikart G, Cornuet J-M (1998) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237. https://doi.org/10.1111/j.1523-1739.1998.96388.x
Méndez M, Tella JL, Godoy JA (2011) Restricted gene flow and genetic drift in recently fragmented populations of an endangered steppe bird. Biol Conserv 144:2615–2622. https://doi.org/10.1016/J.BIOCON.2011.07.011
Moisan G (1956) Le caribou de Gaspé I: histoire et distribution. Nat Can 83:262–274 [in French]
Moisan G (1957) Le caribou de Gaspé III. Analyse de la population et plan d’aménagement. Nat Can 84:5–27 [in French]
Mosnier A, Ouellet J-P, Sirois L, Fournier N (2003) Habitat selection and home-range dynamics of the Gaspé caribou: a hierarchical analysis. Can J Zool 81:1174–1184. https://doi.org/10.1139/z03-065
Nadeau Fortin M-A, Sirois L, St-Laurent M-H (2016) Extensive forest management contributes to maintain suitable habitat characteristics for the endangered Atlantic-Gaspésie caribou. Can J For Res 46:933–942. https://doi.org/10.1139/cjfr-2016-0038
Ouellet J-P, Ferron J, Sirois L (1996) Space and habitat use by the threatened Gaspé caribou in southeastern Quebec. Can J Zool 74:1922–1933. https://doi.org/10.1139/z96-217
Paetkau D, Shields GF, Strobeck C (1998) Gene flow between insular, coastal and interior populations of brown bears in Alaska. Mol Ecol 7:1283–1292. https://doi.org/10.1046/j.1365-294x.1998.00440.x
Palsbøll PJ, Bérubé M, Allendorf FW (2007) Identification of management units using population genetic data. Trends Ecol Evol 22:11–16. https://doi.org/10.1016/j.tree.2006.09.003
Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447
Piry S, Luikart G, Cornuet J-M (1999) Computer note. BOTTLENECK: a computer program for detecting recent reductions in the effective size using allele frequency data. J Hered 90:502–503. https://doi.org/10.1093/jhered/90.4.502
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rivard G (1978) Étude du caribou de la Gaspésie en considérant l’habitat, Ministère du tourisme, de la chasse et de la pêche [in French]
Røed KH, Midthjell L (1998) Microsatellites in reindeer, Rangifer tarandus, and their use in other cervids. Mol Ecol 7:1773–1776. https://doi.org/10.1046/j.1365-294x.1998.00514.x
Røed KH, Ferguson MAD, Crête M, Bergerud TA (1991) Genetic variation in transferrin as a predictor for differentiation and evolution of caribou from eastern Canada. Rangifer 11:65. https://doi.org/10.7557/2.11.2.979
Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Serrouya R, Paetkau D, McLellan BN et al (2012) Population size and major valleys explain microsatellite variation better than taxonomic units for caribou in western Canada. Mol Ecol 21:2588–2601. https://doi.org/10.1111/j.1365-294X.2012.05570.x
Shafer ABA, Northrup JM, White KS et al (2012) Habitat selection predicts genetic relatedness in an alpine ungulate. Ecology 93:1317–1329. https://doi.org/10.1890/11-0815.1
Slatkin M (1977) Gene flow and genetic drift in a species subject to frequent local extinctions. Theor Popul Biol 12:253–262
Slatkin M (1985) Rare alleles as indicators of gene flow. Evolution 39:53–65. https://doi.org/10.1111/j.1558-5646.1985.tb04079.x
Soro A, Quezada-Euan JJG, Theodorou P et al (2017) The population genetics of two orchid bees suggests high dispersal, low diploid male production and only an effect of island isolation in lowering genetic diversity. Conserv Genet 18:607–619. https://doi.org/10.1007/s10592-016-0912-8
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264. https://doi.org/10.1073/pnas.0403809101
St-Laurent M-H, Dussault C, Ferron J, Gagnon R (2009) Dissecting habitat loss and fragmentation effects following logging in boreal forest: Conservation perspectives from landscape simulations. Biol Conserv 142:2240–2249. https://doi.org/10.1016/J.BIOCON.2009.04.025
Stone RT, Pulido JC, Duyk GM et al (1995) A small-insert bovine genomic library highly enriched for microsatellite repeat sequences. Mamm Genome 6:714–724
Stone I, Ouellet J-P, Sirois L et al (2008) Impacts of silvicultural treatments on arboreal lichen biomass in balsam fir stands on Québec’s Gaspé Peninsula: implications for a relict caribou herd. For Ecol Manage 255:2733–2742. https://doi.org/10.1016/J.FORECO.2008.01.040
Van Oosterhout C, Hutchison WF, Wills DPM, Shipley P (2004) micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Vézina R (1971) Inventaire du caribou dans le parc de la Gaspésie. Québec, Canada, Ministère du tourisme, de la chasse et de la pêche [in French]
Waples RS (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 10:785–796. https://doi.org/10.1111/j.1755-0998.2010.02876.x
Weckworth BV, Musiani M, Decesare NJ et al (2013) Preferred habitat and effective population size drive landscape genetic patterns in an endangered species. Proc Biol Sci 280:20131756. https://doi.org/10.1098/rspb.2013.1756
Whitlock MC, Barton NH (1997) The effective size of a subdivided population. Genetics 146:427–441
Whittington J, Hebblewhite M, DeCesare NJ et al (2011) Caribou encounters with wolves increase near roads and trails: a time-to-event approach. J Appl Ecol 48:1535–1542. https://doi.org/10.1111/j.1365-2664.2011.02043.x
Wickham H (2009) Ggplot2: elegant graphics for data analysis. Springer, Berlin
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
Worley K, Strobeck C, Arthur S et al (2004) Population genetic structure of North American thinhorn sheep (Ovis dalli). Mol Ecol 13:2545–2556. https://doi.org/10.1111/j.1365-294X.2004.02248.x
Wright S (1931) Evolution in mendelian populations. Genetics 16:97–159
Wright S (1949) The genetical structure of populations. Ann Eugen 15:323–354. https://doi.org/10.1111/j.1469-1809.1949.tb02451.x
WWF (2016) Living Planet Report 2016. Risk and resilience in a new era. WWW International, Glen
Yannic G, St-Laurent M-H, Ortego J et al (2016) Integrating ecological and genetic structure to define management units for caribou in Eastern Canada. Conserv Genet 17:437–453. https://doi.org/10.1007/s10592-015-0795-0
Acknowledgements
This work was funded by the Fonds de recherche du Québec—Nature et technologies (Grant No. 2013-FM-170586), National Research Council Canada (Grant Nos. 2013-355492 and 2010-38661), Canadian foundation for innovation (Grant No. 26442) and the Natural Sciences and Engineering Research Council of Canada, including Discovery Grants to MHSL, DG and FP and a scholarship to GT. FP holds the Canada Research Chair in Evolutionary Demography and Conservation (Grant No. 229221). We are grateful to G. Yannic and S. Côté for providing samples.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical approval
All captures, handling and sampling of animals for the purpose of this study were approved by the Animal Welfare Committee of the Ministère des Forêts, de la Faune et des Parcs du Québec (certificate # CPA FAUNE 13-08) and of the Université du Québec à Rimouski (certificate # CPA-52-13-112).
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Pelletier, F., Turgeon, G., Bourret, A. et al. Genetic structure and effective size of an endangered population of woodland caribou. Conserv Genet 20, 203–213 (2019). https://doi.org/10.1007/s10592-018-1124-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-018-1124-1