Extensive nuclear introgression accompanied ancient mitochondrial capture in the common ancestor of two sister hare species

Abstract

Pleistocene climatic oscillations promoted contact and hybridization among hare species, leaving lasting genomic signatures. Two sister species, L. castroviejoi (broom hare, endemic to Iberia) and L. corsicanus (Italian hare, endemic to Italy), carry fixed mitogenomes from L. timidus (mountain hare), an Arctic species widespread in southern Europe before deglaciation. Whether such turnover was accompanied by nuclear introgression, and how it affects their genomes today, remains unclear. Here, we date the ancient mitochondrial replacement in the broom-Italian hare ancestor using whole mitogenomes incorporating Iron Age samples. Coalescent modelling of complete genomes infers a substantial mountain hare contribution (24%) to this ancestor ~900 Kya (~5N generations). Accordingly, phylogenetic segmentation identified genomic segments consistent with mountain-to-broom/Italian hare introgression, covering ~17.8% of the autosomes, close to ~18% expected under drift, given admixture's timing and magnitude. Genome polarisation corroborates this estimate, with 25-28% of the mountain hare genome polarising with broom and Italian hares rather than its sister Iberian hare, decreasing to 15-18% at diagnostic sites. The introgression segments concentrate fixed-introgression sites and show sharp transitions of ancestry at their borders. Highly introgressed regions are gene-dense, and regions of reduced introgression are repeat-rich, suggesting that recombination shapes the introgression landscape. They also harbour genes with mitochondrial function that mirror candidates linked to mito-nuclear coadaptation in the Iberian hare, hinting that mitonuclear interactions may influence which variants persist. Our study illustrates how combining demographic, phylogenomic and polarisation-based methods can quantify and localize extensive nuclear introgression, even in the absence of non-introgressed reference populations.