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Ice-Age Climate Adaptations Trap the Alpine Marmot in a State of Low Genetic Diversity

2019; Elsevier BV; Volume: 29; Issue: 10 Linguagem: Inglês

10.1016/j.cub.2019.04.020

1879-0445

Toni I. Gossmann, Achchuthan Shanmugasundram, Stefan T. Börno, Ludovic Duvaux, Christophe Lemaire, Heiner Kuhl, Sven Klages, Lee D. Roberts, S. Schade, Johanna M. Gostner, Falk Hildebrand, Jakob Vowinckel, Coraline Bichet, Michael Mülleder, Enrica Calvani, Aleksej Zelezniak, Julian L. Griffin, Peer Bork, Dominique Allainé, Aurélie Cohas, John J. Welch, Bernd Timmermann, Markus Ralser,

Environmental DNA in Biodiversity Studies

Some species responded successfully to prehistoric changes in climate [1Robson K.M. Lamb C.T. Russello M.A. Low genetic diversity, restricted dispersal, and elevation-specific patterns of population decline in American pikas in an atypical environment.J. Mammal. 2015; 97: 464-472Crossref Scopus (15) Google Scholar, 2Kumar V. Kutschera V.E. Nilsson M.A. Janke A. Genetic signatures of adaptation revealed from transcriptome sequencing of Arctic and red foxes.BMC Genomics. 2015; 16: 585Crossref PubMed Scopus (18) Google Scholar], while others failed to adapt and became extinct [3Nogués-Bravo D. Rodríguez J. Hortal J. Batra P. Araújo M.B. Climate change, humans, and the extinction of the woolly mammoth.PLoS Biol. 2008; 6: e79Crossref PubMed Scopus (218) Google Scholar]. The factors that determine successful climate adaptation remain poorly understood. We constructed a reference genome and studied physiological adaptations in the Alpine marmot (Marmota marmota), a large ground-dwelling squirrel exquisitely adapted to the "ice-age" climate of the Pleistocene steppe [4Bichet C. Allainé D. Sauzet S. Cohas A. Faithful or not: direct and indirect effects of climate on extra-pair paternities in a population of Alpine marmots.Proc. Biol. Sci. 2016; 283: 20162240Crossref PubMed Scopus (13) Google Scholar, 5Tafani M. Cohas A. Bonenfant C. Gaillard J.-M. Allainé D. Decreasing litter size of marmots over time: a life history response to climate change?.Ecology. 2013; 94: 580-586Crossref PubMed Scopus (54) Google Scholar]. Since the disappearance of this habitat, the rodent persists in large numbers in the high-altitude Alpine meadow [6Couturier M. Acclimatation et acclimatement de la Marmotte des Alpes, Marmota marmota (Linné 1758), dans les Pyrénées françaises.Saugetierkdl. Mitt. 1955; 3: 105-107Google Scholar, 7Besson J.P. Introduction de la marmotte dans les Pyrénées occidentales.CR du 96ème Congrès des Sociétés Savantes, Toulouse. 1971; 3: 397-399Google Scholar]. Genome and metabolome showed evidence of adaptation consistent with cold climate, affecting white adipose tissue. Conversely, however, we found that the Alpine marmot has levels of genetic variation that are among the lowest for mammals, such that deleterious mutations are less effectively purged. Our data rule out typical explanations for low diversity, such as high levels of consanguineous mating, or a very recent bottleneck. Instead, ancient demographic reconstruction revealed that genetic diversity was lost during the climate shifts of the Pleistocene and has not recovered, despite the current high population size. We attribute this slow recovery to the marmot's adaptive life history. The case of the Alpine marmot reveals a complicated relationship between climatic changes, genetic diversity, and conservation status. It shows that species of extremely low genetic diversity can be very successful and persist over thousands of years, but also that climate-adapted life history can trap a species in a persistent state of low genetic diversity.