The evolution of bat vestibular systems in the face of potential antagonistic selection pressures for flight and echolocation.

Kalina T J Davies,Paul J J Bates,Stephen J Rossiter,James A Cotton,Ibnu Maryanto,Kornelius Kupczik

doi:10.1371/journal.pone.0061998

Kalina T J Davies, Paul J J Bates + Show 4 more

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https://doi.org/10.1371/journal.pone.0061998

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Abstract

The vestibular system maintains the body’s sense of balance and, therefore, was probably subject to strong selection during evolutionary transitions in locomotion. Among mammals, bats possess unique traits that place unusual demands on their vestibular systems. First, bats are capable of powered flight, which in birds is associated with enlarged semicircular canals. Second, many bats have enlarged cochleae associated with echolocation, and both cochleae and semicircular canals share a space within the petrosal bone. To determine how bat vestibular systems have evolved in the face of these pressures, we used micro-CT scans to compare canal morphology across species with contrasting flight and echolocation capabilities. We found no increase in canal radius in bats associated with the acquisition of powered flight, but canal radius did correlate with body mass in bat species from the suborder Yangochiroptera, and also in non-echolocating Old World fruit bats from the suborder Yinpterochiroptera. No such trend was seen in members of the Yinpterochiroptera that use laryngeal echolocation, although canal radius was associated with wing-tip roundedness in this group. We also found that the vestibular system scaled with cochlea size, although the relationship differed in species that use constant frequency echolocation. Across all bats, the shape of the anterior and lateral canals was associated with large cochlea size and small body size respectively, suggesting differential spatial constraints on each canal depending on its orientation within the skull. Thus in many echolocating bats, it seems that the combination of small body size and enlarged cochlea together act as a principal force on the vestibular system. The two main groups of echolocating bats displayed different canal morphologies, in terms of size and shape in relation to body mass and cochlear size, thus suggesting independent evolutionary pathways and offering tentative support for multiple acquisitions of echolocation.

Highlights

During their adaptive radiation to occupy new environments, mammals have faced multiple simultaneous selection pressures that have shaped their ecology, locomotion and sensory modality
We investigated the allometric scaling of R versus body mass after accounting for the potentially confounding effects of phylogeny
Models that included either flight or laryngeal echolocation did not result in improved model fit

Summary

Introduction

During their adaptive radiation to occupy new environments, mammals have faced multiple simultaneous selection pressures that have shaped their ecology, locomotion and sensory modality. Many of these pressures are likely to have been antagonistic, such that changes conferring fitness advantages in one aspect may at the same time be disadvantageous in another. We tested for evidence of potential evolutionary constraints on the vertebrate vestibular system, which incorporates three approximately orthogonally oriented semicircular canals (anterior, posterior and lateral) that are responsible for monitoring angular acceleration of the head, and maintaining the body’s sense of balance [6]. As the flocculus sits within the canals, expansion of this brain region can be associated with an increase in semicircular canal size [11,12]

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