Pervasive and recurrent hybridisation prevents inbreeding depression in Europe's most threatened seabird

Abstract

Hybridisation is a double-edged sword: while it can erode distinct evolutionary lineages, it can also introduce genetic diversity and adaptive potential into dwindling populations. In the Critically Endangered Balearic shearwater (Puffinus mauretanicus), this dilemma is exacerbated by a limited understanding of the extent and consequences of hybridisation with the Yelkouan shearwater (P. yelkouan). This knowledge gap has limited the scope of science-based conservation strategies to avoid the Balearic shearwaters imminent extinction. Here, we investigate shearwater hybridisation dynamics and their effect on genome-wide diversity in the Balearic shearwater. Divergence dating, demographic modelling and admixture analyses suggest that these two poorly-differentiated shearwater lineages experienced recurrent episodes of divergence and widespread hybridisation during glacial cycles. Selection scans reveal a 500 kb region hosting an adaptive haplotype that potentially underpins interspecific differences in migratory behaviour, and which has been repeatedly introgressed between taxa. Moreover, we show that interspecific gene flow has prevented increases in homozygosity and genetic load, and through forward simulations we illustrate how it can enhance the Balearic shearwaters resilience to future population bottlenecks. Our findings illustrate how introgression can be crucial for maintaining genetic diversity in threatened taxa, and highlight the need for considering the protection of hybridisation in conservation plans.