Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats

Jessica H Arbour,Abigail A Curtis,Sharlene E Santana

doi:10.1038/s41467-019-09951-y

Abstract

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. Rather, models of discrete shifts between adaptive zones may better explain macroevolutionary dynamics across radiations. To investigate which of these processes underlie exceptional levels of morphological diversity during ecological diversification, we use modern phylogenetic tools and 3D geometric morphometric datasets to examine adaptive zone shifts in bat skull shape. Here we report that, while disparity was established early, bat skull evolution is best described by multiple adaptive zone shifts. Shifts are partially decoupled between the cranium and mandible, with cranial evolution more strongly driven by echolocation than diet. Phyllostomidae, a trophic adaptive radiation, exhibits more adaptive zone shifts than all other families combined. This pattern was potentially driven by ecological opportunity and facilitated by a shift to intermediate cranial shapes compared to oral-emitters and other nasal emitters.

Highlights

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed
Systematic analyses of trait evolution rarely find significant evolutionary rate heterogeneity consistent with an adaptive radiation scenario at larger taxonomic scales, with most major clades apparently evolving under strong selection[11]
In an extensive study of birds (>2000 species), Cooney et al.[9] showed evolutionary rate heterogeneity in bill morphology that was predominantly restricted to branches with distinct shifts to novel, highly specialized bill shapes, whereas evolutionary rates in bill shape remained fairly consistent across other bird clades

Summary

Introduction

Morphological diversity may arise rapidly as a result of adaptation to novel ecological opportunities, but early bursts of trait evolution are rarely observed. We predict that (1) adaptive zones corresponding to major sensory modes will differ in cranial morphology (e.g., the orientation of the rostrum between oral and nasal echolocators30), and (2) increased ecological diversification in Phyllostomidae is tied to increased adaptive shifts in skull shape evolution, with respect to shape changes that are linked to bite performance and the mechanical demands of different diets (e.g., rostral length and cranium height)[36,37].

Results

Conclusion