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      Genetic Adaptations of an Island Pit-Viper to a Unique Sedentary Life with Extreme Seasonal Food Availability

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          Abstract

          The Shedao pit-viper ( Gloydius shedaoensis) exhibits an extreme sedentary lifestyle. The island species exclusively feeds on migratory birds during migratory seasons and experiences prolonged hibernation and aestivation period each year (up to eight months). The sedentary strategy reduces energy expenditure, but may trigger a series of adverse effects and the snakes have likely evolved genetic modifications to alleviate these effects. To investigate the genetic adaptations, we sequenced and compared the transcriptomes of the Shedao pit-viper and its closest mainland relative, the black eyebrow pit-viper ( G. intermedius). The Shedao pit-viper revealed a low rate of molecular evolution compared to its mainland relative, which is possibly associated with metabolic suppression. Signals of positive selection were detected in two genes related to antithrombin ( SERPINC1) and muscle atrophy ( AARS). Those genes exert significant functions in thrombosis, inhibiting oxidation and prolonged fasting. Convergent and parallel substitutions of amino acid with two other sedentary vertebrates, which often suggest adaptation, were found in a fatty acid beta-oxidation related gene ( ACATA1) and a circadian link gene ( KLF10), which regulate lipogenesis, gluconeogenesis, and glycolysis. Furthermore, a circadian clock gene ( CRY2) exhibited two amino acid substitutions specific to the Shedao pit-viper and one variant was predicted to affect protein function. Modifications of these genes and their related functions may have contributed to the survival of this island snake species with a sedentary lifestyle and extreme seasonal food availability. Our study demonstrated several important clues for future research on physiological and other phenotypic adaptation.

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          Most cited references 34

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            Bayesian estimation of species divergence times under a molecular clock using multiple fossil calibrations with soft bounds.

            We implement a Bayesian Markov chain Monte Carlo algorithm for estimating species divergence times that uses heterogeneous data from multiple gene loci and accommodates multiple fossil calibration nodes. A birth-death process with species sampling is used to specify a prior for divergence times, which allows easy assessment of the effects of that prior on posterior time estimates. We propose a new approach for specifying calibration points on the phylogeny, which allows the use of arbitrary and flexible statistical distributions to describe uncertainties in fossil dates. In particular, we use soft bounds, so that the probability that the true divergence time is outside the bounds is small but nonzero. A strict molecular clock is assumed in the current implementation, although this assumption may be relaxed. We apply our new algorithm to two data sets concerning divergences of several primate species, to examine the effects of the substitution model and of the prior for divergence times on Bayesian time estimation. We also conduct computer simulation to examine the differences between soft and hard bounds. We demonstrate that divergence time estimation is intrinsically hampered by uncertainties in fossil calibrations, and the error in Bayesian time estimates will not go to zero with increased amounts of sequence data. Our analyses of both real and simulated data demonstrate potentially large differences between divergence time estimates obtained using soft versus hard bounds and a general superiority of soft bounds. Our main findings are as follows. (1) When the fossils are consistent with each other and with the molecular data, and the posterior time estimates are well within the prior bounds, soft and hard bounds produce similar results. (2) When the fossils are in conflict with each other or with the molecules, soft and hard bounds behave very differently; soft bounds allow sequence data to correct poor calibrations, while poor hard bounds are impossible to overcome by any amount of data. (3) Soft bounds eliminate the need for "safe" but unrealistically high upper bounds, which may bias posterior time estimates. (4) Soft bounds allow more reliable assessment of estimation errors, while hard bounds generate misleadingly high precisions when fossils and molecules are in conflict.
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              CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity.

              Light is a major environmental signal for circadian rhythms. We have identified and analyzed cry, a novel Drosophila cryptochrome gene. All characterized family members are directly photosensitive and include plant blue light photoreceptors. We show that cry transcription is under circadian regulation, influenced by the Drosophila clock genes period, timeless, Clock, and cycle. We also show that cry protein levels are dramatically affected by light exposure. Importantly, circadian photosensitivity is increased in a cry-overexpressing strain. These physiological and genetic data therefore link a specific photoreceptor molecule to circadian rhythmicity. Taken together with the data in the accompanying paper, we propose that CRY is a major Drosophila photoreceptor dedicated to the resetting of circadian rhythms.
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                Author and article information

                Journal
                G3 (Bethesda)
                Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes, Genomes, Genetics
                G3: Genes|Genomes|Genetics
                Genetics Society of America
                2160-1836
                17 March 2020
                May 2020
                : 10
                : 5
                : 1639-1646
                Affiliations
                [* ]Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China
                []Nature Conservation of Snake Island and Laotieshan Mountain, Dalian 116041, China
                []Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
                [§ ]Key Laboratory of Vertebrate Evolution and Human Origins of Chinese Academy of Sciences, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Science, Beijing 100044, China
                [** ]University of Chinese Academy of Sciences, Beijing 100049, China
                [†† ]College of life sciences and food engineering, Yibin University, Yibin 644007, China
                Author notes
                [1 ]Corresponding author: Chengdu Institute of Biology, Chinese Academy of Sciences, Number 9, Seciton 4, Ren-min Nan Road, Chengdu, Sichuan 610041, P.R. China. E-mail: qiyin@ 123456cib.ac.cn
                Article
                GGG_401101
                10.1534/g3.120.401101
                7202027
                32184370
                Copyright © 2020 Lu et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Page count
                Figures: 2, Tables: 2, Equations: 0, References: 63, Pages: 8
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                Investigations

                Genetics

                genetic adaptations, transcriptome, extreme sedentary life, gloydius shedaoensis

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