The legacy of recurrent introgression during the radiation of hares

Hybridization may often be an important source of adaptive variation, but
the extent and long-term impacts of introgression have seldom been
evaluated in the phylogenetic context of a radiation. Hares (Lepus)
represent a widespread mammalian radiation of 32 extant species
characterized by striking ecological adaptations and recurrent admixture.
To understand the relevance of introgressive hybridization during the
diversification of Lepus, we analyzed whole exome sequences (61.7 Mb) from
15 species of hares (1- 4 individuals per species), spanning the global
distribution of the genus, and two outgroups. We used a coalescent
framework to infer species relationships and divergence times, despite
extensive genealogical discordance. We found high levels of allele sharing
among species and show that this reflects extensive incomplete lineage
sorting and temporally layered hybridization. Our results revealed
recurrent introgression at all stages along the Lepus radiation, including
recent gene flow between extant species since the last glacial maximum,
but also pervasive ancient introgression occurring since near the origin
of the hare lineages. We show that ancient hybridization between northern
hemisphere species has resulted in shared variation of potential adaptive
relevance to highly seasonal environments, including genes involved in
circadian rhythm regulation, pigmentation, and thermoregulation. Our
results illustrate how the genetic legacy of ancestral hybridization may
persist across a radiation, leaving a long-lasting signature of shared
genetic variation that may contribute to adaptation within and among
species.