Ice-Age Climate Adaptations Trap the Alpine Marmot in a State of Low Genetic Diversity
Journal article, 2019
© 2019 The Author(s) 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. Despite being highly abundant and well adapted, Gossmann et al. report that the Alpine marmot is among the least genetically diverse animal species. The low diversity is found to be the consequence of consecutive, climate-related events, including long-term extreme niche adaptation, that also greatly retarded the recovery of its genetic diversity.
lipidomics
low genetic diversity
climate adaptation
ice age
reference genome
pleistocene
Alpine marmot
NUMT
large population size
migration
Author
Toni I. Gossmann
University of Sheffield
Bielefeld University
Achchuthan Shanmugasundram
University of Liverpool
The Francis Crick Institute
Stefan Börno
Max Planck Society
Ludovic Duvaux
University of Bordeaux
University of Angers
Christophe Lemaire
University of Angers
Heiner Kuhl
Max Planck Society
Leibniz Association
Sven Klages
Max Planck Society
Lee D. Roberts
University of Cambridge
University of Leeds
Sophia Schade
Max Planck Society
Johanna M. Gostner
Medical University of Innsbruck
Falk Hildebrand
Earlham Institute
European Molecular Biology Laboratory
Institute of Food Research
Jakob Vowinckel
University of Cambridge
Coraline Bichet
Institut für Vogelforschung Vogelwarte Helgoland (IfV)
Michael Mülleder
Charité University Medicine Berlin
University of Cambridge
Enrica Calvani
The Francis Crick Institute
University of Cambridge
Aleksej Zelezniak
The Francis Crick Institute
Chalmers, Biology and Biological Engineering, Systems and Synthetic Biology
Royal Institute of Technology (KTH)
Julian L. Griffin
University of Cambridge
Peer Bork
European Molecular Biology Laboratory
The Max Delbrück Center for Molecular Medicine
Molecular Medicine Partnership Unit
Dominique Allaine
Université de Lyon
Aurélie Cohas
Université de Lyon
John J. Welch
University of Cambridge
Bernd Timmermann
Max Planck Society
M. Ralser
University of Cambridge
Charité University Medicine Berlin
The Francis Crick Institute
Current Biology
0960-9822 (ISSN)
Vol. 29 10 1712-1720.e7Subject Categories (SSIF 2011)
Evolutionary Biology
Ecology
Climate Research
DOI
10.1016/j.cub.2019.04.020