Auditory opportunity and visual constraint enabled the evolution of echolocation in bats

Jeneni Thiagavel,Clément Cechetto,Sharlene E Santana,Lasse Jakobsen,Eric J Warrant,John M Ratcliffe

doi:10.1038/s41467-017-02532-x

Abstract

Substantial evidence now supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation. This scenario entails a parallel sensory and biomechanical transition from a nonvolant, vision-reliant mammal to one capable of sonar and flight. Here we consider anatomical constraints and opportunities that led to a sonar rather than vision-based solution. We show that bats’ common ancestor had eyes too small to allow for successful aerial hawking of flying insects at night, but an auditory brain design sufficient to afford echolocation. Further, we find that among extant predatory bats (all of which use laryngeal echolocation), those with putatively less sophisticated biosonar have relatively larger eyes than do more sophisticated echolocators. We contend that signs of ancient trade-offs between vision and echolocation persist today, and that non-echolocating, phytophagous pteropodid bats may retain some of the necessary foundations for biosonar.

Highlights

Substantial evidence supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation
We found an additional support for the hypothesis that the ancestral bat was a predatory, echolocating bat (Bayesian posterior probabilities: animal-eating laryngeal echolocator >0.999, phytophagous laryngeal echolocator
We reconstructed ancestral states (ASs) of body and brain mass. These reconstructions suggest that the ancestral bat was ~20 g, roughly the mean size of today’s laryngeal echolocating bats, and smaller than most extant pteropodid bats (Fig. 3; Supplementary Fig. 1), with a relative brain mass >20% smaller than that of extant pteropodid species (body mass: N = 183, root AS = 18.55 g, 95% confidence interval (CI) = 7.18, 47.91; brain mass: N = 183; AS = 428.33 mg, CI = 229.59, 799.08), confirming a previous report[37]

Summary

Introduction

Substantial evidence supports the hypothesis that the common ancestor of bats was nocturnal and capable of both powered flight and laryngeal echolocation. Long before the discovery of echolocation, bats were once divided into “megabats” (members of the family Pteropodidae) and “microbats” (the remaining ~20 chiropteran families)[1,5,6,7] Today these are anachronistic terms, and the pteropodids [(~200 visiondependent species, none using laryngeal echolocation (LE)] are placed in Yinpterochiroptera (a.k.a. Pteropodiformes), which together with Yangochiroptera (a.k.a. Vespertilioniformes) comprise the two chiropteran suborders. We test three hypotheses about the relationships between visual abilities and echolocation behavior in bats across their four sensory divisions, and with respect to diet and roosting behavior, relative to ancestral states (ASs) These three hypotheses reflect mechanistic explanations for the origination and evolution of LE in bats for pursuing flying insects, and predict auditory opportunity and visual constraint[5,35]. We test the predictions that today would pteropodids possess relatively larger eyes than LE bats but that among predatory bats (all of which use LE), (i) MH bats would have relatively larger eyes than DH and CF bats and (ii) short-wavelength-sensitive (SWS) opsin genes would remain functional in MH and DH bats, but have lost functionality in CF species[36]

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Results

Conclusion