Hearing Sensitivity of Primates: Recurrent and Episodic Positive Selection in Hair Cells and Stereocilia Protein-Coding Genes.

Andreia Moreira,Myriam Croze,Hervé Luga,Franklin Delehelle,Patricia Balaresque,Catherine Mollereau,Sylvain Cussat-Blanc

doi:10.1093/gbe/evab133

Abstract

The large spectrum of hearing sensitivity observed in primates results from the impact of environmental and behavioral pressures to optimize sound perception and localization. Although evidence of positive selection in auditory genes has been detected in mammals including in Hominoids, selection has never been investigated in other primates. We analyzed 123 genes highly expressed in the inner ear of 27 primate species and tested to what extent positive selection may have shaped these genes in the order Primates tree. We combined both site and branch-site tests to obtain a comprehensive picture of the positively selected genes (PSGs) involved in hearing sensitivity, and drew a detailed description of the most affected branches in the tree. We chose a conservative approach, and thus focused on confounding factors potentially affecting PSG signals (alignment, GC-biased gene conversion, duplications, heterogeneous sequencing qualities). Using site tests, we showed that around 12% of these genes are PSGs, an α selection value consistent with average human genome estimates (10–15%). Using branch-site tests, we showed that the primate tree is heterogeneously affected by positive selection, with the black snub-nosed monkey, the bushbaby, and the orangutan, being the most impacted branches. A large proportion of these genes is inclined to shape hair cells and stereocilia, which are involved in the mechanotransduction process, known to influence frequency perception. Adaptive selection, and more specifically recurrent adaptive evolution, could have acted in parallel on a set of genes (ADGRV1, USH2A, PCDH15, PTPRQ, and ATP8A2) involved in stereocilia growth and the whole complex of bundle links connecting them, in species across different habitats, including high altitude and nocturnal environments.

Highlights

Audition constitutes a key gate between organisms and their acoustic environments
Using branch-site tests, we investigated which branches of the primate tree were the most susceptible to selection regarding this set of genes
Our results show that adaptive selection acts on inner ear expressed genes, and on genes coding for stereocilia structures inside hair bundles

Summary

Introduction

Audition constitutes a key gate between organisms and their acoustic environments. Hearing sensitivity varies between placental mammal species, influenced by a species’ body size, middle and inner ear features, and continuous adaptation to their acoustic biotope (Vater et al., 2004; Bernardi et al, 2019; Köppl and Manley, 2018). Primates diverged from the rest of the mammals around 67.8 mya (Springer et al, 2012) and colonized very contrasting acoustic biotopes, from rainforest to savanna. Their adaptation to these new biotopes and associated sound propagation modalities (Brown and Waser, 2017) has likely had repercussions on their hearing sensitivity, optimizing sensitivity for their lifestyles (including circadian rhythms, i.e., nocturnal, diurnal or cathemeral) and for inter-individual communication (Ramsier and Rauschecker, 2017), in a process similar to what has been reported in subterranean mammal species (Heffner, 2004; Charlton et al, 2019). The middle and inner ear are thought to have co-evolved to improve highfrequency sensitivity (Coleman and Boyer, 2012; Köppl and Manley, 2018; Manley, 2017)

Objectives

Methods

Results

Conclusion