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Multiple geographic origins and high genetic differentiation of the Alpine marmots reintroduced in the Pyrenees

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Abstract

Reintroductions inherently involve a small number of founders leading reintroduced populations to be prone to genetic drift and, consequently, to inbreeding depression. Assessing the origins as the genetic diversity and structure of reintroduced populations compared to native populations are thus crucial to foresee their future. Here, we aim to clarify the origins of the Alpine marmots reintroduced in the Pyrenees and to evaluate the genetic consequences of this reintroduction after almost 30 years without monitoring. We search for the origins and compare the genetic structure and the genetic variability of three reintroduced Pyrenean and eight native Alpine populations using pairwise genetic distances, Bayesian clustering method and multivariate analyses. Our results reveal that the Alpine marmots reintroduced in the Pyrenees originated both from the Northern and the Southern Alps, and that, despite these multiple origins, none of the current Pyrenean marmots are admixed. The reintroduction led to a strong genetic differentiation and to a decrease in genetic diversity. This pattern likely results from the small number of founders and the low dispersal capacities of Alpine marmots and thus, highlight the necessity to consider both genetic characteristics and natural history when reintroducing a species.

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References

  • Allainé D (2000) Sociality, mating system and reproductive skew in marmots: evidence and hypotheses. Behav Process 51:21–34. doi:10.1016/S0376-6357(00)00116-9

    Article  Google Scholar 

  • Anonymous. 1998. IUCN Guidelines for Re-Introductions. IUCN/SSC Re-Introduction Specialist Group, Gland, Switzerland

  • Armstrong DP, Seddon PJ (2008) Directions in reintroduction biology. Trends Ecol Evol 23:20–25. doi:10.1016/j.tree.2007.10.003

    Article  PubMed  Google Scholar 

  • Arnold W, Dittami J (1997) Reproductive suppression in male alpine marmots. Anim Behav 53:53–66. doi:10.1006/anbe.1996.0277

    Article  Google Scholar 

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

    Google Scholar 

  • Borgo A (2003) Habitat requirements of the Alpine marmot Marmota marmota in re-introduction areas of the Eastern Italian Alps. Formulation and validation of habitat suitability models. Acta Theriol (Warsz) 48:557–569. doi:10.1007/BF03192501

    Article  Google Scholar 

  • Bruns U, Haiden A, Suchentrunk F (1999) Allozyme variability in autochthonous colonies of Swiss Alpine marmots (Marmota m. marmota): a confirmation of the “species-wide bottleneck hypothesis”? Folia Zool 48:11–22

    Google Scholar 

  • Canale CI, Ozgul A, Allainé D, Cohas A (2016) Differential plasticity of size and mass to environmental change in a hibernating mammal. Glob Change Biol. doi:10.1111/gcb.13286

    Google Scholar 

  • Cardoso MJ, Eldridge MDB, Oakwood M et al (2009) Effects of founder events on the genetic variation of translocated island populations: implications for conservation management of the northern quoll. Conserv Genet 10:1719–1733. doi:10.1007/s10592-008-9774-z

    Article  Google Scholar 

  • Cohas A, Yoccoz NG, Da Silva A et al (2006) Extra-pair paternity in the monogamous alpine marmot (Marmota marmota): the roles of social setting and female mate choice. Behav Ecol Sociobiol 59:597–605. doi:10.1007/s00265-005-0086-8

    Article  Google Scholar 

  • Cohas A, Yoccoz NG, Bonenfant C et al (2008) The genetic similarity between pair members influences the frequency of extrapair paternity in alpine marmots. Anim Behav 76:87–95. doi:10.1016/j.anbehav.2008.01.012

    Article  Google Scholar 

  • Couturier AJ (1955) Acclimatation et acclimatement de la Marmotte des Alpes, Marmota marmota marmota (Linne, 1758) dans les Pyrenées françaises. Saugetierkundliche Mitteilungen 3:105–108

    Google Scholar 

  • Dray S, Dufour A-B (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20

    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 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed  PubMed Central  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578. doi:10.1111/j.1471-8286.2007.01758.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrari C, Pasquaretta C, Carere C et al (2013) Testing for the presence of coping styles in a wild mammal. Anim Behav 85:1385–1396. doi:10.1016/j.anbehav.2013.03.030

    Article  Google Scholar 

  • Franklin IR, Frankham R (1998) How large must populations be to retain evolutionary potential? Anim Conserv 1:69–70. doi:10.1111/j.1469-1795.1998.tb00228.x

    Article  Google Scholar 

  • Frey-Roos F (1998) Geschlechtsspezifisches abwanderungsmuster beim alpenmurmeltier (Marmota marmota). PhD thesis, Philipps-University Marburg,Marburg

  • Galbreath KE, Hafner DJ, Zamudio KR (2009) When cold is better: climate-driven elevation shifts yield complex patterns of diversification and demography in an Alpine specialist (American Pika, Ochotona Princeps). Evolution 63:2848–2863. doi:10.1111/j.1558-5646.2009.00803.x

    Article  CAS  PubMed  Google Scholar 

  • Germano JM, Bishop PJ (2009) Suitability of amphibians and reptiles for translocation. Conserv Biol 23:7–15. doi:10.1111/j.1523-1739.2008.01123.x

    Article  PubMed  Google Scholar 

  • Gonzalez-Prat F, Puig D, Folch A (2001) Distribution of the Alpine marmot Marmota marmota (Linnaeus, 1758) in the outermost southeastern Pyren. Galemys 13:139–148

    Google Scholar 

  • Goossens B, Chikhi L, Taberlet P et al (2001) Microsatellite analysis of genetic variation among and within Alpine marmot populations in the French Alps. Mol Ecol 10:41–52. doi:10.1046/j.1365-294X.2001.01192.x

    Article  CAS  PubMed  Google Scholar 

  • Goudet J (2014) hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.04-14. http://CRAN.R-project.org/package=hierfstat

  • Hacklander K, Mostl E, Arnold W (2003) Reproductive suppression in female Alpine marmots, Marmota marmota. Anim Behav 65:1133–1140. doi:10.1006/anbe.2003.2159

    Article  Google Scholar 

  • Haig S, Ballou J, Derrickson S (1990) Management options for preserving genetic diversity reintroduction of guam rails to the wild. Conserv Biol 4:290–300. doi:10.1111/j.1523-1739.1990.tb00291.x

    Article  Google Scholar 

  • Herrero J, Garciagonzalez R, Garciaserrano A (1994) Altitudinal distribution of Alpine Marmot (Marmota marmota) in the Pyrenees, Spain/France. Arct Alp Res 26:328–331. doi:10.2307/1551793

    Article  Google Scholar 

  • Herrero J, Garcia-Gonzalez R, Garcia-Serrano A (2002) Research on alpine marmot (Marmota marmota) in the Spanish Pyrenees. In: Armitage KB, Rumiantsev VU (eds) Holarctic marmots as a factor of biodiversity. International Marmot Network, Cheboksary, pp 190–197

    Google Scholar 

  • IUCN (2015) The IUCN red list of threatened species. Version 2015-4. www.iucnredlist.org. Accessed on 19 April 2016

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  CAS  PubMed  Google Scholar 

  • Jombart T (2014) A tutorial for discriminant analysis of principal components (DAPC) using adegenet 1.4–1

  • Jombart T, Devillard S, Dufour A-B, Pontier D (2008) Revealing cryptic spatial patterns in genetic variability by a new multivariate method. Heredity 101:92–103. doi:10.1038/hdy.2008.34

    Article  CAS  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. doi:10.1186/1471-2156-11-94

    Article  PubMed  PubMed Central  Google Scholar 

  • Kruckenhauser L, Pinsker W (2004) Microsatellite variation in autochthonous and introduced populations of the Alpine marmot (Marmota marmota) along a European west-east transect. J Zool Syst Evol Res 42:19–26

    Article  Google Scholar 

  • Kruckenhauser L, Miller WJ, Preleuthner M, Pinsker W (1997) Differentiation of Alpine marmot populations traced by DNA fingerprinting. J Zool Syst Evol Res 35:143–149

    Article  Google Scholar 

  • Kruckenhauser L, Bryant AA, Griffin SC et al (2009) Patterns of within and between-colony microsatellite variation in the endangered Vancouver Island marmot (Marmota vancouverensis): implications for conservation. Conserv Genet 10:1759–1772. doi:10.1007/s10592-008-9779-7

    Article  CAS  Google Scholar 

  • Lardy S, Cohas A, Figueroa I, Allaine D (2011) Mate change in a socially monogamous mammal: evidences support the “forced divorce” hypothesis. Behav Ecol 22:120–125. doi:10.1093/beheco/arq168

    Article  Google Scholar 

  • Leberg P (1993) Strategies for population reintroduction-effects of genetic-variability on population-growth and size. Conserv Biol 7:194–199. doi:10.1046/j.1523-1739.1993.07010194.x

    Article  Google Scholar 

  • Lopez BC, Figueroa I, Pino J et al (2009) Potential distribution of the alpine marmot in Southern Pyrenees. Ethol Ecol Evol 21:225–235

    Article  Google Scholar 

  • Lopez BC, Pino J, Lopez A (2010) Explaining the successful introduction of the alpine marmot in the Pyrenees. Biol Invasions 12:3205–3217. doi:10.1007/s10530-010-9712-0

    Article  Google Scholar 

  • Mock KE, Latch EK, Rhodes OE (2004) Assessing losses of genetic diversity due to translocation: long-term case histories in Merriam’s turkey (Meleagris gallopavo merriami). Conserv Genet 5:631–645. doi:10.1007/s10592-004-1849-x

    Article  Google Scholar 

  • Moran P (1948) The interpretation of statistical maps. J R Stat Soc Ser B 10:243–251

    Google Scholar 

  • Moran P (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23. doi:10.2307/2332142

    Article  CAS  PubMed  Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic-variability in populations. Evolution 29:1–10. doi:10.2307/2407137

    Article  Google Scholar 

  • Oksanen J, Blanchet GF, Kindt R, et al (2015) vegan: Community Ecology Package

  • Perrin C, Allaine D, Leberre M (1993) Sociospatial organization and activity distribution of the Alpine Marmot marmota-marmota-preliminary-results. Ethology 93:21–30

    Article  Google Scholar 

  • Preleuthner M (1993) Das Alpenmurmeltier Marmota m. marmota, Linne´ 1758): Verbreitungsgeschichte und genetische Variation in O¨ sterreich. Ph.D. thesis, University of Vienna

  • Preleuthner M, Pinsker W (1993) Depauperated gene pools in Marmota M-Marmota are caused by an ancient bottle neck-electrophoretic analysis of wild populations from Austria and Switzerland. Acta Theriol (Warsz) 38:121–139

    Article  Google Scholar 

  • Preleuthner M, Pinsker W, Kruckenhauser L et al (1995) Alpine marmots in Austria. The present population structure as a result of the postglacial distribution history. Acta Theriol (Warsz) 40:87–100

    Article  Google Scholar 

  • Pritchard JK, Wen W (2003) Documentation for Structure software: Version2

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ramousse R, Le Berre M (1993) Management of alpine marmot populations. Oecol Mont 2:23–29

    Google Scholar 

  • Ramousse R, Le Berre M (1995) Pour un projet de charte de réintroduction de la Marmotte Alpine en France. In: Ramousse R, Le Berre M (eds) Laboratoire de Socioécologie et Conservation. International Marmot Network, Villeurbanne

    Google Scholar 

  • Ramousse R, Martinot JP, Le Berre M (1992) Twenty years of re-introduction policy of alpine marmots from the national park of La Vanoise (French Alps). In: Bassano B, Durio P; Gallo Orsi, U, Macchi E (eds.). Saint Vincent, Aosta

  • Ramousse R, Leberre M, Massemin S (1993) The paradox of reintroductions of Alpine Marmots in France. Bull Soc Zool Fr 118:287–294

    Google Scholar 

  • Rézouki C, Tafani M, Cohas A, Loison A, Gaillard JM, Allainé D, Bonenfant C (2016) Socially-mediated effects of climate change decrease survival of the hibernating Alpine marmots. J Anim Ecol 5:36–43

    Google Scholar 

  • 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 

  • Sala OE, Chapin FS, Armesto JJ et al (2000) Biodiversity-global biodiversity scenarios for the year 2100. Science 287:1770–1774. doi:10.1126/science.287.5459.1770

    Article  CAS  PubMed  Google Scholar 

  • Seddon PJ, Armstrong DP, Maloney RF (2007) Developing the science of reintroduction biology. Conserv Biol 21:303–312. doi:10.1111/j.1523-1739.2006.00627.x

    Article  PubMed  Google Scholar 

  • Sjoberg G (1996) Genetic characteristics of introduced birds and mammals. Wildl Biol 2:159–164

    Google Scholar 

  • Tafani M, Cohas A, Bonenfant C et al (2013) Decreasing litter size of marmots over time: a life history response to climate change? Ecology 94:580–586

    Article  PubMed  Google Scholar 

  • Weir B, Cockerham C (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38:1358–1370. doi:10.2307/2408641

    Article  Google Scholar 

  • Williams RN, Rhodes OE, Serfass TL (2000) Assessment of genetic variance among source and reintroduced fisher populations. J Mammal 81:895–907. doi:10.1644/1545-1542(2000)081

    Article  Google Scholar 

  • Zachos FE, Cirovic D, Kirschning J et al (2009) Genetic variability, differentiation, and founder effect in golden jackals (Canis aureus) from serbia as revealed by mitochondrial DNA and nuclear microsatellite loci. Biochem Genet 47:241–250. doi:10.1007/s10528-009-9221-y

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

In the Alps, we thank all the volunteers for helping in the field. We warmly thank the rangers of the Ecrins National Park for their precious help and advices in the field, and more particularly M. Francou, R. Papet, C. Albert, R. Estachy and B. Gaudron. We also thank the Vanoise National Park, the Alpine station Joseph Fournier and the national research infrastructure AnaEE for their logistic help. We are very grateful to T. Gayet, B. Alric, L. Crespin, N. Ferry and M.-P. Beugin for their useful advices concerning the multivariate analyses. We also thank M.A. Gillingham for carefully editing the manuscript. Financial support was received from the Agence Nationale de la Recherche (Project ANR-13-JSV7-0005), the Centre National de la Recherche Scientifique (CNRS) and the Rhône-Alpes region (Grant 15.005146.01). Fieldwork conducted was undertaken after acceptance by the Ecrins National Park, and deliverance of permits by the Préfectures of Savoie, Hautes-Alpes and Alpes de Haute Provence. A. Cohas and M. Ferrendiz-Rovira are authorized for experimentation with animals (diplomas 0ETRY20090520 and R45GRETAF110). The protocol has been approved by the ethical committee of the University of Claude Bernard Lyon 1 (n8BH2012-92 V1). In the Pyrenees, we also wish to thank all volunteers participating in the field campaigns. I. Figueroa received a grant from the Generalitat de Catalunya (011FI_B 00425) and from the Sociedad Española para la Conservación y el Estudio de Mamíferos (SECEM). We are also grateful to the Generalitat de Catalunya, the Natural Reserve of Freser-Setcases, and the Government of Andorra to help with localizations and permissions to capture marmots. I. Figueroa is authorized for experimentation with animals (UAB-FELASA, certificate number 53707). In the Gran Paradiso National Park we thank all the students who participated in the field work, all the Park rangers for their help and the Scientific Service for the coordination of the project. The research was funded by the Gran Paradiso National Park. C. Ferrari benefited from funds from the Université du Québec à Montréal (UQAM). The study complied with Canadian law regarding animal experiments (Comité institutionnel de Protection des Animaux (CIPA-UQAM), Protocole No. 615) and was authorized by ISPRA (Istituto Superiore per la Protezione e la Ricerca Ambientale, ex-INFS).

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Bichet, C., Sauzet, S., Averty, L. et al. Multiple geographic origins and high genetic differentiation of the Alpine marmots reintroduced in the Pyrenees. Conserv Genet 17, 1157–1169 (2016). https://doi.org/10.1007/s10592-016-0851-4

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