Evolution of Cranial Morphology and the Functional Consequences of Echolocation in Bats

Abstract

Chiroptera (bats) is the second most species-rich mammalian order and has extraordinary diversity in cranial shape and function. This diversity includes three echolocation modalities and numerous dietary specializations, which have been linked to ecological, behavioral, and sensory adaptations. Previous analyses have suggested that the positioning of the rostrum relative to the basicranium (upturned or downturned snout) is linked to the evolution of echolocation modes. I tested this hypothesis directly by quantifying rostral flexion via 3D geometric morphometrics and using phylogenetic comparative methods to detect macroevolutionary patterns across 235 species of bats. I found that >30% of variation in skull shape is linked to rostral flexion. Disparity though time analysis indicates that the rostral angle of modern lineages was established early in the evolution of most clades, and that echolocator modes have different adaptive optima. Finally, I analyzed biomechanical consequences associated with extreme upturned rostra. I found that unilateral bites have an increase of stress associated with a decrease in rostral flexion (upturned snout) then an increase in flexion (downturned rostrum). This provides evidence for variation in dietary opportunity between different echolocating groups. Overall, I find that rostral flexion is a key element of cranial diversity of bats that played a strong role early in the adaptation of this trait and has broad ranging consequences for the biomechanical properties of the skull. Evolution to different echolocation modes likely significantly constrained subsequent diversification of the skull, helping to explain part of the overall diversity of skull form in this remarkable clade.