The evolutionary pathways for local adaptation in mountain hares

Abstract

Understanding the evolution of local adaptations is a central aim of evolutionary biology and key for the identification of unique populations and lineages of conservation relevance. By combining RAD sequencing and whole‐genome sequencing, we identify genetic signatures of local adaptation in mountain hares (Lepus timidus) from isolated and distinctive habitats of its wide distribution: Ireland, the Alps and Fennoscandia. Demographic modelling suggested that the split of these mountain hares occurred around 20 thousand years ago, providing the opportunity to study adaptive evolution over a short timescale. Using genome‐wide scans, we identified signatures of extreme differentiation among hares from distinct geographic areas that overlap with area‐specific selective sweeps, suggesting targets for local adaptation. Several identified candidate genes are associated with traits related to the uniqueness of the different environments inhabited by the three groups of mountain hares, including coat colour, ability to live at high altitudes and variation in body size. In Irish mountain hares, a variant of ASIP, a gene previously implicated in introgression‐driven winter coat colour variation in mountain and snowshoe hares (L. americanus), may underlie brown winter coats, reinforcing the repeated nature of evolution at ASIP moulding adaptive seasonal colouration. Comparative genomic analyses across several hare species suggested that mountain hares’ adaptive variants appear predominantly species‐specific. However, using coalescent simulations, we also show instances where the candidate adaptive variants have been introduced via introgressive hybridization. Our study shows that standing adaptive variation, including that introgressed from other species, was a crucial component of the post‐glacial dynamics of species.

Mountain- and brown hare genetic polymorphisms to survey local adaptations and conservation status of the heath hare (Lepus timidus sylvaticus, Nilsson 1831)

“…2A,B) is clearly visible in the phylogenies and in ancestry complot analysis (Fig. 2C), which support that the subspecies represent biological entities beyond a single gene winter pelage colour difference 39 . Furthermore, these private alleles could be used to examine the diversification of hares and their subspecies through the use of SNP panels.…”

“…Although, the sample size for this analysis is too small in itself to provide any conclusions, we were able to identify a number of variants within and around genes (Fig. 3) with known effects on pigmentation 10,39 . If integrated with a larger dataset, we trust that the genomic data provided here will provide a valuable resource for population genetics, conservation biology and evolutionary studies on hares.…”

Bidirectional hybridisation and introgression between introduced European brown hare, Lepus europaeus and the endemic Irish hare, L. timidus hibernicus

“…The Irish hare is genetically distinct from its closest geographic neighbours possessing a comparatively high number of unique mitochondrial haplotypes (Hughes et al 2006;Hamill et al 2006). The genetic composition of its population is consistent with the long-term accumulation of genetic differences due to local adaptation to snowless conditions (Giska et al 2022) resulting from its persistence in ice free refuges during successive glacial advances in, or around, Ireland (Montgomery et al 2014). Thus, hybridisation and introgression with introduced the European brown hare has at least the potential to threaten the Irish hare's genetic integrity as an island endemic.…”

“…Introgression in hares may be selected for and is adaptive: for example, camouflage in snowshoe hares Lepus americanus (Jones et al 2018), coat colour variants (Giska et al 2019(Giska et al , 2022; structural and physicochemical properties of proteins encoded by the OXHPOS complex in Arctic lineages of Northern American hares (Melo-Ferreira et al 2014b); and genes associated with spermatogenesis, immunity and mitochondrial metabolism in northern populations of L. granatensis (Seixas et al 2018). Thus, hares are excellent models for research on the interplay of biogeography and evolution where there are marked discontinuities in global change due to climate change and anthropogenic introductions (Acevedo et al 2012;Marques 2017b;Reid et al 2021).…”

“…L.t. hibernicus possesses a high level of genetic diversity being isolated in Ireland for a longer period of time and adapted to a wider range of lowland and upland conditions than L. timidus subspecies in Scandinavia and the Alps (Hughes et al 2006;Giska et al 2022). As such, L. t. hibernicus may be a stronger ecological competitor for L. europaeus than its continental relatives.…”