The impact of bottlenecks and inbreeding on the genome of the endangered Pyrenean desman

Abstract

The Pyrenean desman (Galemys pyrenaicus) is a small semiaquatic mammal endemic to the Iberian Peninsula. Despite its limited range, this species presents a strong genetic structure due to past isolation in glacial refugia and subsequent bottlenecks. Additionally, some populations are highly fragmented today as a consequence of river barriers, causing substantial levels of inbreeding. These features make the Pyrenean desman a unique model in which to study the genomic footprints of differentiation, bottlenecks and extreme isolation in an endangered species. The complete genome of the Pyrenean desman was assembled using a Bloom filter-based approach. An analysis of the 1.83 Gb reference genome and the sequencing of five additional individuals from different evolutionary units allowed us to detect its main genomic characteristics. The population differentiation of the species was reflected in highly distinctive demographic trajectories. A severe population bottleneck during the postglacial recolonization of the eastern Pyrenees created the lowest genomic heterozygosity ever recorded in a mammal. Moreover, isolation and inbreeding gave rise to a high proportion of runs of homozygosity (ROH). Despite these extremely low levels of genetic diversity, two key multigene families from an eco-evolutionary perspective that need to be genetically variable, the major histocompatibility complex and olfactory receptor genes, showed heterozygosity excess in the majority of individuals. Furthermore, these two classes of genes were significantly less abundant than expected within ROH. These results allow us to characterize important genomic health indicators for each individual, information that may be crucial for the conservation and management of the species.