Comparative genomics reveals convergent adaptations in lipid metabolism and low genetic diversity in carnivorous bats

Abstract

Dietary specialization stands as a major factor in the study of adaptive evolution and the field of conservation biology among animals. Although bats show unparalleled dietary diversification among mammals, specialized carnivory remains relatively rare within this group. Consequently, our comprehension of the genetic and conservation aspects associated with this specific dietary niche in bats has largely remained uncharted. To investigate molecular adaptations and conservation genetics in carnivorous bats, we produced a new draft genome assembly for the carnivorous bat Vampyrum spectrum. Furthermore, we utilized this genome alongside another distantly related carnivorous bat Megaderma lyra, to conduct genome-wide comparative analyses with other bat species. Our findings unveil that genes linked to lipid metabolism exhibit signatures of positive selection and convergent molecular adaptation in the two divergent lineages of carnivorous bats. Intriguingly, we have uncovered that the evolution of dietary specialization in carnivorous bats is accompanied by molecular adaptations acting on genes in the peroxisome proliferator-activated receptors pathways, which are crucial in regulating plasma lipid metabolism and sustaining lipid homeostasis. Additionally, our genomic analyses also reveal low genetic diversity in both carnivorous bat species. This pattern is attributed to their continuously declining population sizes and low levels of heterozygosity, signaling their vulnerability and emphasizing the pressing need for conservation efforts. These genomic discoveries advance our understanding of genetic underpinnings of carnivory in bats and underscore substantial conservation concerns associated with carnivorous bat species.