The complex evolutionary history of the tympanic middle ear in frogs and toads (Anura).

Boris L. Blotto,Molly C. Womack,Luis A. Coloma,Kim L. Hoke,J. Sebastián Barrionuevo,Julián Faivovich,Taran Grant,Mariane Targino,Martín O. Pereyra,Diego Baldo,Juan M. Guayasamin,Jhon Jairo Ospina-Sarria

doi:10.1038/srep34130

Abstract

Most anurans possess a tympanic middle ear (TME) that transmits sound waves to the inner ear; however, numerous species lack some or all TME components. To understand the evolution of these structures, we undertook a comprehensive assessment of their occurrence across anurans and performed ancestral character state reconstructions. Our analysis indicates that the TME was completely lost at least 38 independent times in Anura. The inferred evolutionary history of the TME is exceptionally complex in true toads (Bufonidae), where it was lost in the most recent common ancestor, preceding a radiation of >150 earless species. Following that initial loss, independent regains of some or all TME structures were inferred within two minor clades and in a radiation of >400 species. The reappearance of the TME in the latter clade was followed by at least 10 losses of the entire TME. The many losses and gains of the TME in anurans is unparalleled among tetrapods. Our results show that anurans, and especially bufonid toads, are an excellent model to study the behavioural correlates of earlessness, extratympanic sound pathways, and the genetic and developmental mechanisms that underlie the morphogenesis of TME structures.

Highlights

The function of audition in frogs and toads (Anura) is primarily the perception of airborne sounds, including those involved in social communication[1]
Perception of airborne sounds is enabled by a tympanic middle ear (TME) composed minimally of a tympanic membrane, middle ear cavity, and middle ear bone (=columella, columella auris, stapes, plectrum) that conducts sound waves from the environment to the inner ear where they are transduced into electrical signals via hair cells[1,2,3,4]
Two scenarios are compatible with current evidence: the tympanic annulus and membrane might have been present in the most recent common ancestor of Anura and lost with the columella in Ascaphidae +Leiopelmatidae, or they might have arisen in Lalagobatrachia

Summary

Introduction

The function of audition in frogs and toads (Anura) is primarily the perception of airborne sounds, including those involved in social communication[1]. Turtles, and archosaurs possess a complete TME, and even the amphisbaenians, snakes, and lizards that have lost the tympanic membrane and middle ear cavity retain a columella[11], the sole exceptions being the pygopod lizard Aprasia repens[12] and possibly the snakes Atractaspis and Xenocalamus[13]. Among anurans, with at least a few species of several families lacking the entire TME, a condition referred to as “earlessness”[14]. Earlessness is especially common in the true toad family Bufonidae, in which the TME is completely lacking in more than 200 species. Several authors have noted the reduction and loss of TME structures (e.g.,16–20) or morphological variations in middle ear structure (e.g.,1,21–23) in bufonids, but the phylogenetic distribution of earlessness has never been studied either within Bufonidae or across Anura.

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