Foraging shifts and visual preadaptation in ecologically diverse bats

Changes in behaviour may initiate shifts to new adaptive zones, with
physical adaptations for novel environments evolving later. While new
mutations are commonly considered engines of adaptive change, sensory
evolution enabling access to new resources might also arise from standing
genetic diversity, and even gene loss. We examine the relative
contribution of molecular adaptations, measured by positive and relaxed
selection, acting on eye expressed genes associated with shifts to new
adaptive zones in ecologically diverse bats from the superfamily
Noctilionoidea. Collectively, noctilionoids display remarkable ecological
breadth, from highly divergent echolocation to flight strategies linked to
specialized insectivory, the parallel evolution of diverse plant-based
diets (e.g., nectar, pollen, and fruit) from ancestral insectivory, and
–unusually for echolocating bats– often have large, well-developed eyes.
We report contrasting levels of positive selection in genes associated
with the development, maintenance, and scope of visual function, tracing
back to the origins of noctilionoids and Phyllostomidae (the bat family
with most dietary diversity), instead of during shifts to novel diets.
Generalized plant visiting was not associated with exceptional molecular
adaptation, and exploration of these novel niches took place in an
ancestral phyllostomid genetic background. In contrast, evidence for
positive selection in vision genes was found at subsequent shifts to
either nectarivory or frugivory. Thus, neotropical noctilionoids that use
visual cues for identifying food and roosts, as well as for orientation,
were effectively preadapted, with subsequent molecular adaptations in
nectar-feeding lineages and the Stenodermatinae subfamily of fig-eating
bats fine-tuning pre-existing visual adaptations for specialized purposes.