The Molecular Evolution of Bat Chemosensory Pathways Reveals Sensory Innovation and Loss


Chemosensation detects environmental chemical cues and mediates many behaviors directly related to fitness (e.g. finding food, mates). Mammals have a secondary chemosensory system known as vomerolfaction that is primarily attributed to detecting pheromones, chemical cues that mediate many social behaviors. Vomeronasal mechanisms are conserved across mammals because of vomerolfaction’s critical roles in reproduction and social communication. Such mechanisms include the pheromone detection by vomeronasal receptors (e.g. V1Rs) and signal transduction of the Transient receptor potential cation channel 2 (Trpc2), an ion channel indispensable for vomeronasal function. Despite a nocturnal lifestyle and gregarious behaviors, most bats surprisingly lack a functioning vomeronasal system, exhibiting degraded vomeronasal morphology and pseudogenized Trpc2 and V1Rs. New World Leaf-nosed bats (Phyllostomidae) are one of the few exceptions where the vomeronasal system is well maintained. It is unclear whether phyllostomids have retained vomeronasal function through time while other bats have independently lost function or if they have regained the functional sensory system, potentially serving as a key innovation related to their diversity. To address this question, I sequenced the V1R profiles from the vomeronasal transcriptome from a diversity of phyllostomids and sequenced Trpc2 exon 2 in over 100 bats across nearly every family. Compiling the V1R data with existing mammal species, the phylogenetic history of the gene tree suggested phyllostomids V1Rs are completely orthologous with the dog and horse, providing no evidence that phyllostomids have evolved a new set of vomeronasal receptors. Additionally, many non-phyllostomids showed independent pseudogenizing mutations of Trpc2 while phyllostomids showed a signature of strong purifying selection to maintain a functional Trpc2. I simulated sequences under similar selection constraints to determine if it Trpc2 was under relaxed selection early within the phylogeny or if purifying selection has been prevalent throughout the evolutionary history of phyllostomid bats. My results showed it was unlikely that Trpc2 reactivated and supports the notion that phyllostomids have maintained vomeronasal function since the divergence with other laurasiatherians. My results also emphasize that the chemosensory system is a crucial aspect of sensory biology for some bats, a modality often underappreciated in light of other extreme bat senses.

In Ecology and Evolution. p. 138. State University of New York at Stony Brook, New York