Ice-age climate adaptations trap the alpine marmot in a state of low genetic diversity
Toni I. Gossmann
(1, 2)
,
Achchuthan Shanmugasundram
(3, 4)
,
Stefan Börno
(5)
,
Ludovic Duvaux
(6, 7)
,
Christophe Lemaire
(7)
,
Heiner Kuhl
(5, 8)
,
Sven Klages
(5)
,
Lee D. Roberts
(9, 10)
,
Sophia Schade
(5)
,
Johanna M. Gostner
(11)
,
Falk Hildebrand
(12, 13)
,
Jakob Vowinckel
(9)
,
Coraline Bichet
(14)
,
Michael Mülleder
(9, 15)
,
Enrica Calvani
(3, 9)
,
Aleksej Zelezniak
(3, 16)
,
Julian L. Griffin
(9)
,
Peer Bork
(12, 17)
,
Dominique Allainé
(18)
,
Aurélie Cohas
(18)
,
John J. Welch
(19)
,
Bernd Timmermann
(5)
,
Markus Ralser
(5)
1
Department of Animal and Plant Sciences
2 Universität Bielefeld = Bielefeld University
3 The Francis Crick Institute [London]
4 University of Liverpool
5 MPIMG - Max Planck Institute for Molecular Genetics
6 BioGeCo - Biodiversité, Gènes & Communautés
7 IRHS - Institut de Recherche en Horticulture et Semences
8 Department of Ecophysiology and Aquaculture
9 CAM - University of Cambridge [UK]
10 University of Leeds
11 Leopold Franzens Universität Innsbruck - University of Innsbruck
12 EMBL - European Molecular Biology Laboratory
13 Earlham Institute
14 Institute of Avian Research
15 Department of Biochemistry
16 Chalmers University of Technology [Gothenburg, Sweden]
17 Max Delbrück Centre for Molecular Medicine
18 LBBE - Laboratoire de Biométrie et Biologie Evolutive - UMR 5558
19 Department of Genetics
2 Universität Bielefeld = Bielefeld University
3 The Francis Crick Institute [London]
4 University of Liverpool
5 MPIMG - Max Planck Institute for Molecular Genetics
6 BioGeCo - Biodiversité, Gènes & Communautés
7 IRHS - Institut de Recherche en Horticulture et Semences
8 Department of Ecophysiology and Aquaculture
9 CAM - University of Cambridge [UK]
10 University of Leeds
11 Leopold Franzens Universität Innsbruck - University of Innsbruck
12 EMBL - European Molecular Biology Laboratory
13 Earlham Institute
14 Institute of Avian Research
15 Department of Biochemistry
16 Chalmers University of Technology [Gothenburg, Sweden]
17 Max Delbrück Centre for Molecular Medicine
18 LBBE - Laboratoire de Biométrie et Biologie Evolutive - UMR 5558
19 Department of Genetics
Ludovic Duvaux
- Function : Author
- PersonId : 747485
- IdHAL : ludovic-duvaux
- ORCID : 0000-0003-0960-0312
- IdRef : 150007264
Christophe Lemaire
- Function : Author
- PersonId : 1203326
Coraline Bichet
- Function : Author
- PersonId : 767869
- ORCID : 0000-0003-0255-4966
Dominique Allainé
- Function : Author
- PersonId : 21838
- IdHAL : dominique-allaine
- IdRef : 033441235
Abstract
Some species responded successfully to prehistoric changes in climate [1,2], while others failed to adapt and became extinct [3]. 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 [4,5]. Since the disappearance of this habitat, the rodent persists in large numbers in the high-altitude Alpine meadow [6,7]. 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.