Hybridization load introduced by Alpine ibex hybrid swarms

Abstract

Species conservation efforts can be threatened by deleterious mutation accumulation following population contractions. In addition to de novo mutations, a significant source of genetic load could be deleterious variants introduced into a population through hybridization. Hence, even successfully restored species may face deleterious mutation swamping due to hybridization with an abundant and closely related species. The outcomes of such hybridization events are poorly understood given the complex interplay of introduced adaptive and maladaptive variation. Here, we analyze this potential risk for Alpine ibex (Capra ibex), a flagship species of large mammal restoration in the Alps. Near-extinction two centuries ago resulted in exceptionally low genome-wide diversity and increased inbreeding, which facilitated the purging of severe deleterious mutations but accumulation of less severe ones. We produced a highly contiguous chromosome-level genome assembly of the Alpine ibex capturing structural divergence from its closest domestic species, the domestic goat (Capra hircus) known to hybridize with Alpine ibex Genome sequencing of eight recent ibex-goat hybrids and backcrosses from two hybrid swarms in Northern Italy revealed highly diverse recombinants and an average of 30 masked, predicted loss-of-function (LOF) mutations per hybrid compared to 10 in non-hybrid Alpine ibex. This exposes Alpine ibex to further backcrosses, exposing their vulnerable gene pool to an influx of hybridization load. Individual-based genomic simulations suggest that such LOF load would return to pre- hybridization levels with a lag of over 100 generations after gene flow subsides. Hybridization could also disrupt local adaptation in the recipient species. Our work provides a direct estimate of hybridization load and, by this, informs on the complexity of managing endangered gene pools in the face of hybridization.