Comprehensive phylogenetic reconstructions support ancestral omnivory in the ecologically diverse bat family Phyllostomidae

Abstract

Adaptive radiations often occur with an early burst of ecological diversification, which requires not only various available niches but also a generalist ancestor with wide ecological niche breadths. However, ancestral generalism remains hard to test in empirical cases. The New World leaf-nosed bats (family Phyllostomidae) represent an unparalleled mammalian adaptive radiation with diverse dietary niches including arthropods, blood, terrestrial vertebrates, nectar, and fruits. However, when and how often phyllostomid bats transitioned from insectivory to fruit or nectar feeding remains unclear. Here we tested the hypotheses of ancestral insectivory versus ancestral omnivory in Phyllostomidae (141 species) using improved trait reconstructions based on multi-response phylogenetic threshold models, while explicitly accounting for phylogenetic uncertainty. Our results indicate that complementary fruit feeding has fully evolved at the early burst of the phyllostomid radiation and started to evolve in the most recent common ancestor of the family, supporting the ancestral omnivory hypothesis. In addition, fruit feeding probably evolved before nectar eating in Phyllostomidae, in contrast to the claims of previous studies. Extending this analysis to all bat families (621 species) reveals independent evolution of ancestral fruit feeding in four families, namely the Pteropodidae (Old World fruit bats) and three families from the Noctilionoidea superfamily. Despite the ancestral omnivory of these fruit-eating families, only Phyllostomidae and Pteropodidae show high species diversity and evolved predominant and strict fruit feeding. Therefore, our results reveal that ancestral generalism (i.e., omnivory) may be a precondition of but does not necessarily lead to adaptive radiations which also require subsequent niche partitioning and speciation.