Comprising more than 1,400 species, bats possess adaptations unique among mammals including powered flight, unexpected longevity, and extraordinary immunity. Some of the molecular mechanisms underlying these unique adaptations includes DNA repair, metabolism and immunity. However, analyses have been limited to a few divergent lineages, reducing the scope of inferences on gene family evolution across the Order Chiroptera. We conducted an exhaustive comparative genomic study of 37 bat species, one generated in this study, encompassing a large number of lineages, with a particular emphasis on multi-gene family evolution across immune and metabolic genes. In agreement with previous analyses, we found lineage-specific expansions of the APOBEC3 and MHC-I gene families, and loss of the proinflammatory PYHIN gene family. We inferred more than 1,000 gene losses unique to bats, including genes involved in the regulation of inflammasome pathways such as epithelial defense receptors, the natural killer gene complex and the interferon-gamma induced pathway. Gene set enrichment analyses revealed genes lost in bats are involved in defense response against pathogen-associated molecular patterns and damage-associated molecular patterns. Gene family evolution and selection analyses indicate bats have evolved fundamental functional differences compared to other mammals in both innate and adaptive immune system, with the potential to enhance anti-viral immune response while dampening inflammatory signaling. In addition, metabolic genes have experienced repeated expansions related to convergent shifts to plant-based diets. Our analyses support the hypothesis that, in tandem with flight, ancestral bats had evolved a unique set of immune adaptations whose functional implications remain to be explored.

Book Review.

The role of mechanical morphologies in the exploitation of novel niche space is well characterized, however, the role of sensory structures in unlocking new niches is less clear. Here we investigate the relationship between the evolution of sensory structures and diet during the radiation of noctilionoid bats. With a broad range of foraging ecologies and a well- supported phylogeny, noctilionoids constitute an ideal group for studying this relationship. We used diffusible iodine-based contrast enhanced computed tomography (diceCT) scans of 44 noctilionoid species to analyze relationships between the relative volumes of three sensory structures (olfactory bulbs, orbits, and cochleae) and diet. We found a positive relationship between frugivory and both olfactory and orbit size. However, we also found a negative relationship between nectarivory and cochlea size. Ancestral state estimates suggest that larger orbits and olfactory bulbs were present in the common ancestor of family Phyllostomidae, but not in other noctilionoid. This constellation of traits indicates a shift toward omnivory at the base of Phyllostomidae, predating their radiation into an exceptionally broad range of dietary niches. This is consistent with a scenario in which changes in sensory systems associated with foraging and feeding set the stage for subsequent morphological modification and diversification.