Genome-environment association analyses reveal geographically restricted adaptive divergence across the range of the widespread Eurasian carnivore Lynx lynx (Linnaeus, 1758)

Enrico Bazzicalupo; Mirosław Ratkiewicz; Ivan V Seryodkin; Innokentiy Okhlopkov; Naranbaatar Galsandorj; Yuriy A Yarovenko; Janis Ozolins; Alexander P Saveljev; Dime Melovski; Alexander Gavashelishvili; Krzysztof Schmidt; José A Godoy

doi:10.1111/eva.13570

Genome-environment association analyses reveal geographically restricted adaptive divergence across the range of the widespread Eurasian carnivore Lynx lynx (Linnaeus, 1758)

Evol Appl. 2023 Oct 9;16(11):1773-1788. doi: 10.1111/eva.13570. eCollection 2023 Nov.

Affiliations

¹ Department of Ecology and Evolution Estación Biológica de Doñana (CSIC) Seville Spain.
² Faculty of Biology University of Białystok Białystok Poland.
³ Laboratory of Ecology and Conservation of Animals Pacific Institute of Geography of Far East Branch of Russian Academy of Sciences Vladivostok Russia.
⁴ Institute for Biological Problems of Cryolithozone Siberian Branch of the Russian Academy of Sciences Yakutsk Russia.
⁵ Institute of Biology Mongolian Academy of Sciences Ulaanbaatar Mongolia.
⁶ Pre-Caspian Institute of Biological Resources Dagestan Federal Scientific Centre of RAS Makhachkala Russia.
⁷ Department of Hunting and Wildlife Management Latvijas Valsts mežzinātnes institūts "Silava" Salaspils Latvia.
⁸ Department of Animal Ecology Russian Research Institute of Game Management and Fur Farming Kirov Russia.
⁹ Macedonian Ecological Society (MES) Skopje North Macedonia.
¹⁰ Center of Biodiversity Studies, Institute of Ecology Ilia State University Tbilisi Georgia.
¹¹ Mammal Research Institute Polish Academy of Sciences Białowieża Poland.

Abstract

Local adaptations to the environment are an important aspect of the diversity of a species and their discovery, description and quantification has important implications for the fields of taxonomy, evolutionary and conservation biology. In this study, we scan genomes from several populations across the distributional range of the Eurasian lynx, with the objective of finding genomic windows under positive selection which may underlie local adaptations to different environments. A total of 394 genomic windows are found to be associated to local environmental conditions, and they are enriched for genes involved in metabolism, behaviour, synaptic organization and neural development. Adaptive genetic structure, reconstructed from SNPs in candidate windows, is considerably different than the neutral genetic structure of the species. A widespread adaptively homogeneous group is recovered occupying areas of harsher snow and temperature climatic conditions in the north-western, central and eastern parts of the distribution. Adaptively divergent populations are recovered in the westernmost part of the range, especially within the Baltic population, but also predicted for different patches in the western and southern part of the range, associated with different snow and temperature regimes. Adaptive differentiation driven by climate does not correlate much with the subspecies taxonomic delimitations, suggesting that subspecific divergences are mostly driven by neutral processes of genetic drift and gene flow. Our results will aid the selection of source populations for assisted gene flow or genetic rescue programs by identifying what climatic patterns to look for as predictors of pre-adaptation of individuals. Particularly, the Carpathian population is confirmed as the best source of individuals for the genetic rescue of the endangered, isolated and genetically eroded Balkan population. Additionally, reintroductions in central and western Europe, currently based mostly on Carpathian lynxes, could consider the Baltic population as an additional source to increase adaptive variation and likely improve adaptation to their milder climate.

Keywords: Eurasian lynx; Lynx lynx; conservation units; genome scans; local adaptation; subspecies.