Adaptation to the High-Arctic island environment despite long-term reduced genetic variation in Svalbard reindeer

Nicolas Dussex; Ole K Tørresen; Tom van der Valk; Mathilde Le Moullec; Vebjørn Veiberg; Ave Tooming-Klunderud; Morten Skage; Benedicte Garmann-Aarhus; Jonathan Wood; Jacob A Rasmussen; Åshild Ø Pedersen; Sarah L F Martin; Knut H Røed; Kjetill S Jakobsen; Love Dalén; Brage B Hansen; Michael D Martin

doi:10.1016/j.isci.2023.107811

Adaptation to the High-Arctic island environment despite long-term reduced genetic variation in Svalbard reindeer

iScience. 2023 Sep 3;26(10):107811. doi: 10.1016/j.isci.2023.107811. eCollection 2023 Oct 20.

Authors

Nicolas Dussex¹, Ole K Tørresen², Tom van der Valk^{3

4}, Mathilde Le Moullec⁵, Vebjørn Veiberg⁶, Ave Tooming-Klunderud², Morten Skage², Benedicte Garmann-Aarhus^{2

7}, Jonathan Wood⁸, Jacob A Rasmussen^{1

9}, Åshild Ø Pedersen¹⁰, Sarah L F Martin¹, Knut H Røed¹¹, Kjetill S Jakobsen², Love Dalén^{3

4

12}, Brage B Hansen^{5

6}, Michael D Martin^{1

5}

Affiliations

¹ Department of Natural History, University Museum, Norwegian University of Science and Technology (NTNU), Erling Skakkes gate 47A, Trondheim, Norway.
² Centre for Ecological and Evolutionary Synthesis (CEES), Department of Biosciences, University of Oslo, PO Box 1066 Blindern, N-0316 Oslo, Norway.
³ Centre for PalaeoGenetics, Svante Arrhenius väg 20C, SE 106 91 Stockholm, Sweden.
⁴ Department of Bioinformatics and Genetics, Swedish Museum of Natural History, SE 104 05 Stockholm, Sweden.
⁵ Centre for Biodiversity Dynamics, Department of Biology, Norwegian University of Science and Technology (NTNU), NO 7491 Trondheim, Norway.
⁶ Department of Terrestrial Ecology, Norwegian Institute for Nature Research (NINA), NO 7034 Trondheim, Trondheim, Norway.
⁷ Natural History Museum, University of Oslo, NO 0318 Oslo, Norway.
⁸ Tree of Life, Wellcome Sanger Institute, Wellcome Genome Campus, Hinxton CB10 1SA Cambridge, UK.
⁹ Globe Institute, University of Copenhagen, 2100 Copenhagen, Denmark.
¹⁰ Norwegian Polar Institute, Fram Centre, NO 9296 Tromsø, Norway.
¹¹ Department of Preclinical Sciences and Pathology, Norwegian University of Life Sciences, P.O. Box 5003, 1432 Ås, Norway.
¹² Department of Zoology, Stockholm University, SE-106 91 Stockholm, Sweden.

Abstract

Typically much smaller in number than their mainland counterparts, island populations are ideal systems to investigate genetic threats to small populations. The Svalbard reindeer (Rangifer tarandus platyrhynchus) is an endemic subspecies that colonized the Svalbard archipelago ca. 6,000-8,000 years ago and now shows numerous physiological and morphological adaptations to its arctic habitat. Here, we report a de-novo chromosome-level assembly for Svalbard reindeer and analyze 133 reindeer genomes spanning Svalbard and most of the species' Holarctic range, to examine the genomic consequences of long-term isolation and small population size in this insular subspecies. Empirical data, demographic reconstructions, and forward simulations show that long-term isolation and high inbreeding levels may have facilitated the reduction of highly deleterious-and to a lesser extent, moderately deleterious-variation. Our study indicates that long-term reduced genetic diversity did not preclude local adaptation to the High Arctic, suggesting that even severely bottlenecked populations can retain evolutionary potential.

Keywords: Animal species; Genomics; Sequence analysis.