PMCID: PMC3631194This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited

A Nykjaer

AL Dance

AL Wells

B Shen

B Uberti

Bin Shen

Brock Fenton

CC Voigt

D Biemesderfer

D Novick

D Posada

D Shriner

DW Thomas

EC Teeling

EI Christensen

EM De La Cruz

ES Dierenfeld

F Buss

F Ronquist

G Gottsberger

G Jones

G Li

Gareth Jones

GL Herrera

H Birn

H Raghuram

HL Sweeney

J Breckler

J Kitamoto

J Ménétrey

J van der Westhuyzen

J Vandesompele

J Zhang

JC Buckland-Wright

JD Thompson

K Homma

K Parry-Jones

K Takeyama

K Tamura

KB Avraham

KJ Livak

KT Davies

L Aschenbrenner

LH Herbst

M Cavaleros

MB Fenton

MC Wendeln

MLG Herrera

N Ameen

N Gotoh

N Hilgert

P Heidrych

PA Peterson

R Hertzano

R Kozyraki

RA Tedman

RD Barber

RMR Barclay

RS Heffner

S Melchionda

SE Courts

Shuyi Zhang

SJ Rossiter

SK Moestrup

SL Kosakovsky Pond

SL Pond

Stephen J. Rossiter

SV van Tonder

T Datzmann

T Hasson

T Self

X Zhou

Xiuqun Han

Y Li

Y Liu

Z Liu

Z Yang

ZM Ahmed

ZM Fuzessery

PLoS ONE

English

PubMed

<div>Myosin VI (encoded by the Myo6 gene) is highly expressed in the inner and outer hair cells of the ear, retina, and polarized epithelial cells such as kidney proximal tubule cells and intestinal enterocytes. The Myo6 gene is thought to be involved in a wide range of physiological functions such as hearing, vision, and clathrin-mediated endocytosis. Bats (Chiroptera) represent one of the most fascinating mammal groups for molecular evolutionary studies of the Myo6 gene. A diversity of specialized adaptations occur among different bat lineages, such as echolocation and associated high-frequency hearing in laryngeal echolocating bats, large eyes and a strong dependence on vision in Old World fruit bats (Pteropodidae), and specialized high-carbohydrate but low-nitrogen diets in both Old World and New World fruit bats (Phyllostomidae). To investigate what role(s) the Myo6 gene might fulfill in bats, we sequenced the coding region of the Myo6 gene in 15 bat species and used molecular evolutionary analyses to detect evidence of positive selection in different bat lineages. We also conducted real-time PCR assays to explore the expression levels of Myo6 in a range of tissues from three representative bat species. Molecular evolutionary analyses revealed that the Myo6 gene, which was widely considered as a hearing gene, has undergone adaptive evolution in the Old World fruit bats which lack laryngeal echolocation and associated high-frequency hearing. Real-time PCR showed the highest expression level of the Myo6 gene in the kidney among ten tissues examined in three bat species, indicating an important role for this gene in kidney function. We suggest that Myo6 has undergone adaptive evolution in Old World fruit bats in relation to receptor-mediated endocytosis for the preservation of protein and essential nutrients.</div

Bin Shen (143992)

Xiuqun Han (173069)

Gareth Jones (34552)

Stephen J. Rossiter (34551)

Shuyi Zhang (34553)

The Francis Crick Institute

Adaptive Evolution of the Myo6 Gene in Old World Fruit Bats (Family: Pteropodidae)

Myosin VI (encoded by the Myo6 gene) is highly expressed in the inner and outer hair cells of the ear, retina, and polarized epithelial cells such as kidney proximal tubule cells and intestinal enterocytes. The Myo6 gene is thought to be involved in a wide range of physiological functions such as hearing, vision, and clathrin-mediated endocytosis. Bats (Chiroptera) represent one of the most fascinating mammal groups for molecular evolutionary studies of the Myo6 gene. A diversity of specialized adaptations occur among different bat lineages, such as echolocation and associated high-frequency hearing in laryngeal echolocating bats, large eyes and a strong dependence on vision in Old World fruit bats (Pteropodidae), and specialized high-carbohydrate but low-nitrogen diets in both Old World and New World fruit bats (Phyllostomidae). To investigate what role(s) the Myo6 gene might fulfill in bats, we sequenced the coding region of the Myo6 gene in 15 bat species and used molecular evolutionary analyses to detect evidence of positive selection in different bat lineages. We also conducted real-time PCR assays to explore the expression levels of Myo6 in a range of tissues from three representative bat species. Molecular evolutionary analyses revealed that the Myo6 gene, which was widely considered as a hearing gene, has undergone adaptive evolution in the Old World fruit bats which lack laryngeal echolocation and associated high-frequency hearing. Real-time PCR showed the highest expression level of the Myo6 gene in the kidney among ten tissues examined in three bat species, indicating an important role for this gene in kidney function. We suggest that Myo6 has undergone adaptive evolution in Old World fruit bats in relation to receptor-mediated endocytosis for the preservation of protein and essential nutrients

Stephen J Rossiter

Directory of Open Access Journals

Adaptive evolution of the myo6 gene in old world fruit bats (family: pteropodidae).

Shen, B

Han, X

Jones, G

Rossiter, SJ

Zhang, S

Queen Mary Research Online

25-Hydroxyvitamin D3 1a-hydroxylase and vitamin D synthesis.

A genetic algorithm approach to detecting lineagespecific variation in selection pressure.

A molecular phylogeny for bats illuminates biogeography and the fossil record.

A Myo6 mutation destroys coordination between the myosin heads, revealing new functions of myosin VI in the stereocilia of mammalian inner ear hair cells.

A random effects branch-site model for detecting episodic diversifying selection.

A splice-site mutation and overexpression of MYO6 cause a similar phenotype in two families with autosomal dominant hearing loss.

Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.

Altered renal proximal tubular endocytosis and histology in mice lacking myosin-VI.

Amino acid properties and consequences of substitutions.

Amino acids and sugars in nectar, and their putative evolutionary significance.

An endocytic pathway essential for renal uptake and activation of the steroid 25-(OH) vitamin D3.

Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCt method.

Augee ML

Bats: biology and behavior.

Cetaceans on a molecular fast track to ultrasonic hearing.

Characterization of unconventional MYO6, the human homologue of the gene responsible for deafness in Snell’s waltzer mice.

Compromises: sound frequencies used in echolocation by aerial-feeding bats.

Convergent sequence evolution between echolocating bats and dolphins.

Cubilin dysfunction causes abnormal metabolism of the steroid hormone 25(OH) vitamin D3.

Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice.

Deliberate insectivory by the fruit bat Rousettus aegyptiacus.

Determination of and correlation between urine protein excretion and urine protein-to-creatinine ratio values during a 24-hour period in healthy horses and ponies.

Dietary deficiency in fruit bats.

Dietary strategies of Old World fruit bats (Megachiroptera, Pteropodidae): how do they obtain sufficient protein?

Differentiation of glomerular, tubular, and normal proteinuria: determinations of urinary excretion of ß2-microglobulin, albumin, and total protein.

Diversity in rat tissue accumulation of vitamin B12 supports a distinct role for the kidney in vitamin B12 homeostasis.

Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level.

Evolution of nectarivory in phyllostomid bats (Phyllostomidae Gray, 1825, Chiroptera: Mammalia).

Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules.

Fruit intake and energy budgets of frugivorous bats.

GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues.

GARD: a genetic algorithm for recombination detection.

Houdusse A

How are the cellular functions of myosin VI regulated within the cell?

HyPhy: hypothesis testing using phylogenies.

jModelTest: phylogenetic model averaging.

Kinetic mechanism and regulation of myosin VI.

Lipid composition of the brain in the vitamin B12-deficient fruit bat (Rousettus aegyptiacus) with neurological impairment.

McCance and Widdowson’s The composition of foods.

MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0.

Megalin-dependent cubilin-mediated endocytosis is a major pathway for the apical uptake of transferrin in polarized epithelia.

Megalin-mediated endocytosis of transcobalamin-vitamin-B12 complexes suggests a role of the receptor in vitamin-B12 homeostasis.

MrBayes 3: Bayesian phylogenetic inference under mixed models.

Multiple adaptive losses of alanine-glyoxylate aminotransferase mitochondrial targeting in fruit-eating bats.

Mutations of MYO6 are associated with recessive deafness, DFNB37.

Myo6 facilitates the translocation of endocytic vesicles from cell peripheries.

MYO6, the human homologue of the gene responsible for deafness in Snell’s waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss.

Myosin VI is an actin-based motor that moves backwards.

Myosin VI is required for normal retinal function.

Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis.

Myosin VI: cellular functions and motor properties.

Myosin VI: two distinct roles in endocytosis.

Novel myosin VI isoform is abundantly expressed in retina.

Nutritional values of 14 fig species and bat feeding preferences in Panama.

Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell.

PAML 4: phylogenetic analysis by maximum likelihood.

Parallel evolution of KCNQ4 in echolocating bats.

Parallel signatures of sequence evolution among hearing genes in echolocating mammals: an emerging model of genetic convergence.

Passive sound localization of prey by the pallid bat (Antrozous p.

Phylogenomic analysis resolves the interordinal relationships and rapid diversification of the Laurasiatherian mammals.

Plasma fat-soluble vitamin and mineral concentrations in relation to diet in captive pteropodid bats.

Potential impact of recombination on sitewise approaches for detecting positive natural selection.

Prestin and high frequency hearing in mammals.

Prestin shows divergent evolution between constant frequency echolocating bats.

Receptor-mediated endocytosis in renal proximal tubule.

Regulation of myosin-VI targeting to endocytic compartments.

Role of myosin VI in the differentiation of cochlear hair cells.

Scaling of echolocation call parameters in bats.

Soluble cytokine receptors are present in normal human urine.

Sound localization in a new-world frugivorous bat, Artibeus jamaicensis: acuity, use of binaural cues, and relationship to vision.

Sound-localization acuity and its relation to vision in large and small fruit-eating bats: I. Echolocating species, Phyllostomus hastatus and Carollia perspicillata.

Sources of assimilated protein in five species of New World frugivorous bats.

Sources of assimilated proteins in Old and New World phytophagous bats.

Sources of protein in two species of phytophagous bats in a seasonal dry forest: evidence from stable-isotope analysis.

Teeling EC (2006) The evolution of echolocation in bats.

The biology of bats.

The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.

The core of the motor domain determines the direction of myosin movement.

The effect of recombination on the accuracy of phylogeny estimation.

The hearing gene Prestin reunites echolocating bats.

The hearing gene Prestin unites echolocating bats and whales.

The morphology of the gastrointestinal tract and food transit time in the fruit bats Pteropus alecto and P. poliocephalus (Megachiroptera).

The role of nitrogen from fruit pulp in the nutrition of the frugivorous bat Carollia perspicillata.

The role of olfaction and vision in the foraging behaviour of an echolocating megachiropteran fruit bat, Rousettus leschenaulti (Pteropodidae).

The structure of the myosin VI motor reveals the mechanism of directionality reversal.

The voltagegated potassium channel subfamily KQT member 4 (KCNQ4) displays parallel evolution in echolocating bats.

Uncoated endocytic vesicles require the unconventional myosin, Myo6, for rapid transport through actin barriers.

Vitamin B12 metabolism in the fruit bat (Rousettus aegyptiacus). The induction of vitamin B12 deficiency and its effect on folate levels.

Vitamin D metabolism in a frugivorous nocturnal mammal, the Egyptian fruit bat (Rousettus aegyptiacus).

Adaptive Evolution of the Myo6 Gene in Old World Fruit Bats (Family: Pteropodidae)

Adaptive Evolution of the Myo6 Gene in Old World Fruit Bats (Family: Pteropodidae)

Abstract

Similar works

Full text

Available Versions

The Francis Crick Institute

Directory of Open Access Journals

Queen Mary Research Online

Public Library of Science (PLOS)

Crossref