Parallel Evolution of KCNQ4 in Echolocating Bats

Liu, Zhen; Li, Shude; Wang, Wei; Xu, Dongming; Murphy, Robert W.; Shi, Peng

doi:10.1371/journal.pone.0026618

Cited by 40 publications

(41 citation statements)

References 33 publications

(52 reference statements)

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“…The evolution of echolocation and its associated high-frequency hearing makes laryngeal echolocating bats a fascinating mammal group for molecular evolutionary studies of hearing genes. Many genes associated with hearing have recently been proved to have undergone positive selection in echolocating bats and also in echolocating cetaceans [10], [11], [12], [13], [14], [15], [16], [70]. However, our results from the branch-site model A tests showed no significant evidence of positive selection in the major focal branches leading to echolocating bats, although one statistically supported positively selected site (260Q) was found in the ancestral branch of Yinpterochiroptera echolocating bats (Table 2).…”

Section: Discussionmentioning

confidence: 99%

“…Such excellent auditory performance making echolocating bats fascinating mammals for studying genes associated with hearing. Recently, many studies have revealed that some genes associated with hearing have undergone positive selection in echolocating bats and cetaceans [10], [11], [12], [13], [14], [15], [16]. Considering the important role of Myo6 in hearing, it is reasonable to hypothesize that the Myo6 may also be a target gene for positive selection in bats that use laryngeal echolocation compared with species that do not use laryngeal echolocation (the Old World fruit bats in the family Pteropodidae).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

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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.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2013

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“…The molecular evolution of Kcnq4 in bats shows several parallels with patterns seen in Prestin . Echolocating bats form a monophyletic group in the Kcnq4 nucleotide and amino acid sequence trees, and five amino acid sites are shared between echolocating bats in both suborders [Yinpterochiroptera and Yangochiroptera (Liu et al, 2011)]. Reconstruction of ancestral sequences suggests that bats in the two suborders evolved mutations at two amino acid sites in parallel.…”

Section: Echolocationmentioning

confidence: 99%

From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats

Jones¹,

Teeling²,

Rossiter³

2013

Front. Physiol.

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Great advances have been made recently in understanding the genetic basis of the sensory biology of bats. Research has focused on the molecular evolution of candidate sensory genes, genes with known functions [e.g., olfactory receptor (OR) genes] and genes identified from mutations associated with sensory deficits (e.g., blindness and deafness). For example, the FoxP2 gene, underpinning vocal behavior and sensorimotor coordination, has undergone diversification in bats, while several genes associated with audition show parallel amino acid substitutions in unrelated lineages of echolocating bats and, in some cases, in echolocating dolphins, representing a classic case of convergent molecular evolution. Vision genes encoding the photopigments rhodopsin and the long-wave sensitive opsin are functional in bats, while that encoding the short-wave sensitive opsin has lost functionality in rhinolophoid bats using high-duty cycle laryngeal echolocation, suggesting a sensory trade-off between investment in vision and echolocation. In terms of olfaction, bats appear to have a distinctive OR repertoire compared with other mammals, and a gene involved in signal transduction in the vomeronasal system has become non-functional in most bat species. Bitter taste receptors appear to have undergone a “birth-and death” evolution involving extensive gene duplication and loss, unlike genes coding for sweet and umami tastes that show conservation across most lineages but loss in vampire bats. Common vampire bats have also undergone adaptations for thermoperception, via alternative splicing resulting in the evolution of a novel heat-sensitive channel. The future for understanding the molecular basis of sensory biology is promising, with great potential for comparative genomic analyses, studies on gene regulation and expression, exploration of the role of alternative splicing in the generation of proteomic diversity, and linking genetic mechanisms to behavioral consequences.

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“…Ancestral reconstructions appeared to be reliable because both methods gave identical results, and nodal support values exceeded 99%. We then looked for parallel or convergent changes by comparing ancestral and extant protein sequences [6,8]. Parallel changes were required to have the same descendant amino acids from the same ancestral amino acids, and convergence was considered to have occurred when identical amino acids were derived from different ancestral amino acids.…”

Section: Materials and Methods (A) Species Pcr Amplification And Sequmentioning

confidence: 99%

Repeated functional convergent effects of Na _V 1.7 on acid insensitivity in hibernating mammals

et al. 2014

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Hibernating mammals need to be insensitive to acid in order to cope with conditions of high CO 2 ; however, the molecular basis of acid tolerance remains largely unknown. The African naked mole-rat (Heterocephalus glaber) and hibernating mammals share similar environments and physiological features. In the naked mole-rat, acid insensitivity has been shown to be conferred by the functional motif of the sodium ion channel Na V 1.7. There is now an opportunity to evaluate acid insensitivity in other taxa. In this study, we tested for functional convergence of Na V 1.7 in 71 species of mammals, including 22 species that hibernate. Our analyses revealed a functional convergence of amino acid sequences, which occurred at least six times independently in mammals that hibernate. Evolutionary analyses determined that the convergence results from both parallel and divergent evolution of residues in the functional motif. Our findings not only identify the functional molecules responsible for acid insensitivity in hibernating mammals, but also open new avenues to elucidate the molecular underpinnings of acid insensitivity in mammals.

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Parallel Evolution of KCNQ4 in Echolocating Bats

Cited by 40 publications

References 33 publications

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)

From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats

Repeated functional convergent effects of Na _V 1.7 on acid insensitivity in hibernating mammals

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Parallel Evolution of KCNQ4 in Echolocating Bats

Cited by 40 publications

References 33 publications

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)

From the ultrasonic to the infrared: molecular evolution and the sensory biology of bats

Repeated functional convergent effects of Na V 1.7 on acid insensitivity in hibernating mammals

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Repeated functional convergent effects of Na _V 1.7 on acid insensitivity in hibernating mammals