The voltage-gated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats

YANG, LIU*; NAIJIAN, HAN*; FRANCHINI LUCIA F.*; HUIHUI XU; PISCIOTTANO FRANCISCO; ANA BELEN ELGOYHEN; KOILMANI EMMANUVEL RAJAN; SHUYI ZHANG

MOLECULAR BIOLOGY AND EVOLUTION

OXFORD UNIV PRESS

Lugar: Oxford; Año: 2011 p. 1 - 10

0737-4038

Bats are the only mammals that use highly developed laryngeal echolocation, a sensory mechanism that is based on the ability to emit laryngeal sounds and interpret the returning echoes to identify objects. Although this capability allows bats to orientate and hunt in complete darkness, endowing them with great survival advantages, the genetic bases underlying the evolution of bat echolocation are still largely unknown. Echolocation requires high frequency hearing that in mammals is largely dependent on outer hair cell somatic electromotility. Then, understanding the molecular evolution of outer hair cell genes might help to unravel the evolutionary history of echolocation. In this work we analyzed the molecular evolution of two key outer hair cell genes: the voltage-gated potassium channel gene KCNQ4 and CHRNA10, the gene encoding the α10 nicotinic acetylcholine receptor subunit. We reconstructed the phylogeny of bats based on KCNQ4 and CHRNA10 protein and nucleotide sequences. A phylogenetic tree built using KCNQ4 amino acid sequences showed that two paraphyletic clades of laryngeal echolocating bats grouped together, with eight shared substitutions among particular lineages. In addition, our analyses indicate that two of these parallel substitutions, M388I and P406S, were probably fixed under positive selection and could have had a strong functional impact on KCNQ4. Moreover, our results indicate that KCNQ4 evolved under positive selection in the lineage leading to mammals, suggesting that this gene might have been important for the evolution of mammalian hearing. On the other hand, our results indicate that CHRNA10, a gene that evolved positively in the mammalian lineage, is under strong purifying selection in bats. Thus, the CHRNA10 amino acid tree did not show echolocating bat monophyly and reproduced the bat species tree. These results indicate that only genes involved in particular hearing functions or pathways could be responsible for the evolution of echolocation. The present work continues to delineate the genetic bases of echolocation and ultrasonic hearing in bats.