The Response to Past Climate Perturbations Explains Extremely Low Genetic Diversity in the Genome of an Abundant Ice-Age Remnant, the Alpine Marmot

The Alpine Marmot (Marmota marmota) is a rodent remnant of the ‘ice-age’ climate of the Pleistocene steppe, and since the disappearance of this habitat, persists in the high altitude Alpine meadow. Sequencing its genome, we reveal that the long-term cold-climate adaptation has altered its metabolism, in particular biosynthesis and storage of fatty acids. Paradoxically, despite successful adaptation and a large population size, we detected levels of genetic variation that are among the lowest for mammals, and that purifying selection is ineffective. Reconstructing its demographic past revealed that the two apparently contradictory observations are, in fact, intimately interlinked. The climate-adaptive life history prevented genetic diversity to recover from Pleistocene perturbations. The case of the Alpine marmot demonstrates that populations of extremely low genetic diversity can be very successful and persist over thousands of years, but that a climate-adapted life history can deprive a species from the possibility to recover genetic diversity.