A Comparative Study of the Evolution of Mammalian High-Frequency Hearing and Echolocation

Abstract

The lineage that gave rise to mammals split from other basal amniotes, approximately 300 million years ago. Since then, mammals have evolved many sensory novelties, including high-frequency hearing and echolocation. Sensitivity to high frequencies is particularly well developed in many echolocating mammals; for example, the upper hearing limit of several laryngeal echolocating bat species are estimated to be approximately ten times that of humans. In order to process the high frequency sounds produced during echolocation, the inner ears of laryngeal echolocating bats have undergone substantial modifications. Despite the evolutionary significance of laryngeal echolocation, it is unknown how many times it evolved within bats. Its occurrence on most, but not all, bat lineages suggests it either evolved once with secondary loss, or independently on multiple lineages. Distinguishing between these possibilities is complicated by morphological diversity and convergence. Furthermore, the genetic basis underpinning echolocation remains largely unknown. To elucidate the evolutionary history of this key trait in bats, a combined molecular and morphological approach was taken. Firstly, for two mammalian ‘hearing genes’ sequence convergence, phylogenetic signal and selection pressures were examined across echolocating and non-echolocating mammal species. Secondly, substitution rates of Conserved Non-coding Elements associated with genes regulating ear development were compared across mammals. Finally, as mammalian inner ear development is controlled by many genes, the gross structure of the bony labyrinth was studied in order to examine the combined genetic effect. Structural variation of bat cochleae and vestibular systems was examined using micro-computed tomography reconstructions, and related to ecological data. Subsequent analyses found evidence of convergence at the molecular level, in terms of amino acid substitutions, and also the morphological level, in terms of inner ear morphology. No evidence of degeneration, supporting loss-of-function in Old World fruit bats was found. Conversely, evidence of differential evolution pressures acting on the two echolocating bat lineages was found, which supports multiple origins of laryngeal echolocation in bats.