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

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          Abstract

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

          Steroid hormones may enter cells by diffusion through the plasma membrane. However, we demonstrate here that some steroid hormones are taken up by receptor-mediated endocytosis of steroid-carrier complexes. We show that 25-(OH) vitamin D3 in complex with its plasma carrier, the vitamin D-binding protein, is filtered through the glomerulus and reabsorbed in the proximal tubules by the endocytic receptor megalin. Endocytosis is required to preserve 25-(OH) vitamin D3 and to deliver to the cells the precursor for generation of 1,25-(OH)2 vitamin D3, a regulator of the calcium metabolism. Megalin-/- mice are unable to retrieve the steroid from the glomerular filtrate and develop vitamin D deficiency and bone disease.
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            A random effects branch-site model for detecting episodic diversifying selection.

            Adaptive evolution frequently occurs in episodic bursts, localized to a few sites in a gene, and to a small number of lineages in a phylogenetic tree. A popular class of "branch-site" evolutionary models provides a statistical framework to search for evidence of such episodic selection. For computational tractability, current branch-site models unrealistically assume that all branches in the tree can be partitioned a priori into two rigid classes--"foreground" branches that are allowed to undergo diversifying selective bursts and "background" branches that are negatively selected or neutral. We demonstrate that this assumption leads to unacceptably high rates of false positives or false negatives when the evolutionary process along background branches strongly deviates from modeling assumptions. To address this problem, we extend Felsenstein's pruning algorithm to allow efficient likelihood computations for models in which variation over branches (and not just sites) is described in the random effects likelihood framework. This enables us to model the process at every branch-site combination as a mixture of three Markov substitution models--our model treats the selective class of every branch at a particular site as an unobserved state that is chosen independently of that at any other branch. When benchmarked on a previously published set of simulated sequences, our method consistently matched or outperformed existing branch-site tests in terms of power and error rates. Using three empirical data sets, previously analyzed for episodic selection, we discuss how modeling assumptions can influence inference in practical situations.
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              The evolution of echolocation in bats.

              Recent molecular phylogenies have changed our perspective on the evolution of echolocation in bats. These phylogenies suggest that certain bats with sophisticated echolocation (e.g. horseshoe bats) share a common ancestry with non-echolocating bats (e.g. Old World fruit bats). One interpretation of these trees presumes that laryngeal echolocation (calls produced in the larynx) probably evolved in the ancestor of all extant bats. Echolocation might have subsequently been lost in Old World fruit bats, only to evolve secondarily (by tongue clicking) in this family. Remarkable acoustic features such as Doppler shift compensation, whispering echolocation and nasal emission of sound each show multiple convergent origins in bats. The extensive adaptive radiation in echolocation call design is shaped largely by ecology, showing how perceptual challenges imposed by the environment can often override phylogenetic constraints.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                19 April 2013
                : 8
                : 4
                : e62307
                Affiliations
                [1 ]Institute of Molecular Ecology and Evolution, Institutes for Advanced Interdisciplinary Research, East China Normal University, Shanghai, China
                [2 ]School of Biological Sciences, University of Bristol, Bristol, United Kingdom
                [3 ]School of Biological and Chemical Sciences, Queen Mary University of London, London, United Kingdom
                University of Western Ontario, Canada
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BS XH SZ. Performed the experiments: BS XH. Analyzed the data: BS XH. Contributed reagents/materials/analysis tools: SZ. Wrote the paper: BS GJ SJR SZ.

                Article
                PONE-D-12-34869
                10.1371/journal.pone.0062307
                3631194
                23620821
                ef891dbd-26a8-494e-9f25-d2863ebb8e42
                Copyright @ 2013

                This 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.

                History
                : 9 November 2012
                : 19 March 2013
                Page count
                Pages: 11
                Funding
                This work was supported by grants awarded by the Key Construction Program of the National “985” Project and “211” Project to SZ, the Royal Society Research Fellowship and a Biotechnology and Biological Sciences Research Council (BBSRC) Chinese Partnering award to SJR, the Biotechnology and Biological Sciences Research Council (BBSRC) Chinese Partnering award to GJ, and the PhD Candidate Fund of East China Normal University for overseas Studies, International Conference and Domestic Scholarly Visits to BS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Evolutionary Ecology
                Evolutionary Biology
                Evolutionary Processes
                Adaptation
                Evolutionary Selection
                Natural Selection
                Evolutionary Systematics
                Taxonomy
                Animal Taxonomy
                Phylogenetics
                Organismal Evolution
                Animal Evolution
                Forms of Evolution
                Model Organisms
                Animal Models
                Zoology
                Animal Phylogenetics
                Animal Taxonomy

                Uncategorized
                Uncategorized

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