Parallel Evolution of Auditory Genes for Echolocation in Bats and Toothed Whales

Yong-Yi Shen,Ya-Ping Zhang,Robert W Murphy,Lu Liang,Gui-Sheng Li,Jianzhi Zhang

doi:10.1371/journal.pgen.1002788

Abstract

The ability of bats and toothed whales to echolocate is a remarkable case of convergent evolution. Previous genetic studies have documented parallel evolution of nucleotide sequences in Prestin and KCNQ4, both of which are associated with voltage motility during the cochlear amplification of signals. Echolocation involves complex mechanisms. The most important factors include cochlear amplification, nerve transmission, and signal re-coding. Herein, we screen three genes that play different roles in this auditory system. Cadherin 23 (Cdh23) and its ligand, protocadherin 15 (Pcdh15), are essential for bundling motility in the sensory hair. Otoferlin (Otof) responds to nerve signal transmission in the auditory inner hair cell. Signals of parallel evolution occur in all three genes in the three groups of echolocators—two groups of bats (Yangochiroptera and Rhinolophoidea) plus the dolphin. Significant signals of positive selection also occur in Cdh23 in the Rhinolophoidea and dolphin, and Pcdh15 in Yangochiroptera. In addition, adult echolocating bats have higher levels of Otof expression in the auditory cortex than do their embryos and non-echolocation bats. Cdh23 and Pcdh15 encode the upper and lower parts of tip-links, and both genes show signals of convergent evolution and positive selection in echolocators, implying that they may co-evolve to optimize cochlear amplification. Convergent evolution and expression patterns of Otof suggest the potential role of nerve and brain in echolocation. Our synthesis of gene sequence and gene expression analyses reveals that positive selection, parallel evolution, and perhaps co-evolution and gene expression affect multiple hearing genes that play different roles in audition, including voltage and bundle motility in cochlear amplification, nerve transmission, and brain function.

Highlights

The ability of echolocation using ultrahigh frequency sounds occurs in two groups of bats (Yangochiroptera and Rhinolophoidea) and in toothed whales including dolphins [1,2,3]
Proteins encoded by the genes Cadherin 23 (Cdh23) and protocadherin 15 (Pcdh15) are essential to hair bundle motility [12,13,14], and their malfunctions in humans cause deafness in newborns and progressive retinitis pigmentosa (Usher syndrome type I) [15]
The gene trees for Cdh23 based on nucleotide sequences (Figure 1A) were basically the same as the well-accepted species tree (Figure 1C) [26,27,28] in all methods of tree-building

Summary

Introduction

The ability of echolocation using ultrahigh frequency sounds occurs in two groups of bats (Yangochiroptera and Rhinolophoidea) and in toothed whales including dolphins [1,2,3]. Previous molecular studies on echolocation have mainly focused on the Organ of Corti In this organ, the motor protein prestin plays a key role in voltage motility [6,7,8]. Genetic mutations in the gene encoding otoferlin (Otof) cause a clinical, autosomal recessive nonsyndromic form of prelingual and sensorineural deafness [19,20,21]. This protein that may act as the major Ca2+ sensor that triggers membrane fusion at the ribbon synapse of the auditory inner hair cell [22]. The above functions are involved in the conversion of sound signals into electrical impulses in the inner ear, the expression of Otof occurs in neurons and nerve fibers in the brain [23]

Methods

Results

Discussion

Conclusion