Abstract:
During the Miocene, Hyaenidae was a highly diverse family of Carnivora that has since been severely reduced to four
species: the bone-cracking spotted, striped, and brown hyenas, and the specialized insectivorous aardwolf. Previous
studies investigated the evolutionary histories of the spotted and brown hyenas, but little is known about the remaining
two species. Moreover, the genomic underpinnings of scavenging and insectivory, defining traits of the extant species,
remain elusive. Here, we generated an aardwolf genome and analyzed it together with the remaining three species to
reveal their evolutionary relationships, genomic underpinnings of their scavenging and insectivorous lifestyles, and their
respective genetic diversities and demographic histories. High levels of phylogenetic discordance suggest gene flow
between the aardwolf lineage and the ancestral brown/striped hyena lineage. Genes related to immunity and digestion
in the bone-cracking hyenas and craniofacial development in the aardwolf showed the strongest signals of selection,
suggesting putative key adaptations to carrion and termite feeding, respectively. A family-wide expansion in olfactory
receptor genes suggests that an acute sense of smell was a key early adaptation. Finally, we report very low levels of
genetic diversity within the brown and striped hyenas despite no signs of inbreeding, putatively linked to their similarly
slow decline in effective population size over the last 2 million years. High levels of genetic diversity and more stable
population sizes through time are seen in the spotted hyena and aardwolf. Taken together, our findings highlight how
ecological specialization can impact the evolutionary history, demographics, and adaptive genetic changes of an evolutionary
lineage.
