Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress
Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Hol...
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description | Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Holarctic Region, live in cold regions at either high altitudes or high latitudes and have a maximum distribution of species diversification confined to the Qinghai-Tibet Plateau. Variations in energy metabolism are remarkable for them living in cold environments. Leptin, an adipocyte-derived hormone, plays important roles in energy homeostasis.
To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.
Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin. |
doi_str_mv | 10.1371/journal.pone.0001472 |
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To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.
Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0001472</identifier><identifier>PMID: 18213380</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Acids ; Adaptation ; Adaptation, Physiological ; Amino Acid Sequence ; Amino acid substitution ; Amino acids ; Animals ; ATP synthase ; Bioinformatics ; Biological evolution ; Biology ; Cloning, Molecular ; Cold ; Cold regions ; Cold Temperature ; Deoxyribonucleic acid ; Disease control ; Disease prevention ; DNA ; DNA, Complementary ; Ecological adaptation ; Ecology/Evolutionary Ecology ; Ecology/Physiological Ecology ; Energy balance ; Energy metabolism ; Environmental factors ; Environmental stress ; Evolution ; Evolution & development ; Evolutionary Biology/Bioinformatics ; Evolutionary Biology/Evolutionary and Comparative Genetics ; Evolutionary Biology/Evolutionary Ecology ; Fitness ; Gene expression ; Genetic research ; High-altitude environments ; Homeostasis ; Hypoxia ; Kinases ; Laboratories ; Lagomorpha ; Leptin ; Leptin - chemistry ; Leptin - genetics ; Leptin - physiology ; Likelihood Functions ; Metabolism ; Mitochondrial DNA ; Molecular Biology/Bioinformatics ; Molecular Biology/Molecular Evolution ; Molecular evolution ; Molecular Sequence Data ; Mutation ; Natural selection ; Nucleotide sequence ; Ochotona ; Phylogenetics ; Phylogeny ; Physiological aspects ; Positive selection ; Proteins ; Regression analysis ; Reproductive fitness ; Selection, Genetic ; Sequence Homology, Amino Acid ; Spatial distribution ; Statistical methods ; Steppes ; Stresses ; Thermogenesis</subject><ispartof>PloS one, 2008-01, Vol.3 (1), p.e1472</ispartof><rights>COPYRIGHT 2008 Public Library of Science</rights><rights>2008 Yang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Yang et al. 2008</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c728t-b39eef257efdb14be39db319b0b3e8a4c6a0bde50b726aa6699d3fe3aff253823</citedby><cites>FETCH-LOGICAL-c728t-b39eef257efdb14be39db319b0b3e8a4c6a0bde50b726aa6699d3fe3aff253823</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2194619/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2194619/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2095,2914,23846,27903,27904,53769,53771,79346,79347</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18213380$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Bromage, Timothy</contributor><creatorcontrib>Yang, Jie</creatorcontrib><creatorcontrib>Wang, Zhen Long</creatorcontrib><creatorcontrib>Zhao, Xin Quan</creatorcontrib><creatorcontrib>Wang, De Peng</creatorcontrib><creatorcontrib>Qi, De Lin</creatorcontrib><creatorcontrib>Xu, Bao Hong</creatorcontrib><creatorcontrib>Ren, Yong Hong</creatorcontrib><creatorcontrib>Tian, Hui Fang</creatorcontrib><title>Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Holarctic Region, live in cold regions at either high altitudes or high latitudes and have a maximum distribution of species diversification confined to the Qinghai-Tibet Plateau. Variations in energy metabolism are remarkable for them living in cold environments. Leptin, an adipocyte-derived hormone, plays important roles in energy homeostasis.
To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.
Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.</description><subject>Acids</subject><subject>Adaptation</subject><subject>Adaptation, Physiological</subject><subject>Amino Acid Sequence</subject><subject>Amino acid substitution</subject><subject>Amino acids</subject><subject>Animals</subject><subject>ATP synthase</subject><subject>Bioinformatics</subject><subject>Biological evolution</subject><subject>Biology</subject><subject>Cloning, Molecular</subject><subject>Cold</subject><subject>Cold regions</subject><subject>Cold Temperature</subject><subject>Deoxyribonucleic acid</subject><subject>Disease control</subject><subject>Disease prevention</subject><subject>DNA</subject><subject>DNA, Complementary</subject><subject>Ecological adaptation</subject><subject>Ecology/Evolutionary Ecology</subject><subject>Ecology/Physiological Ecology</subject><subject>Energy balance</subject><subject>Energy metabolism</subject><subject>Environmental factors</subject><subject>Environmental stress</subject><subject>Evolution</subject><subject>Evolution & development</subject><subject>Evolutionary Biology/Bioinformatics</subject><subject>Evolutionary Biology/Evolutionary and Comparative Genetics</subject><subject>Evolutionary Biology/Evolutionary Ecology</subject><subject>Fitness</subject><subject>Gene expression</subject><subject>Genetic research</subject><subject>High-altitude environments</subject><subject>Homeostasis</subject><subject>Hypoxia</subject><subject>Kinases</subject><subject>Laboratories</subject><subject>Lagomorpha</subject><subject>Leptin</subject><subject>Leptin - chemistry</subject><subject>Leptin - genetics</subject><subject>Leptin - physiology</subject><subject>Likelihood Functions</subject><subject>Metabolism</subject><subject>Mitochondrial DNA</subject><subject>Molecular Biology/Bioinformatics</subject><subject>Molecular Biology/Molecular Evolution</subject><subject>Molecular evolution</subject><subject>Molecular Sequence Data</subject><subject>Mutation</subject><subject>Natural selection</subject><subject>Nucleotide sequence</subject><subject>Ochotona</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Physiological aspects</subject><subject>Positive selection</subject><subject>Proteins</subject><subject>Regression analysis</subject><subject>Reproductive fitness</subject><subject>Selection, Genetic</subject><subject>Sequence Homology, Amino Acid</subject><subject>Spatial distribution</subject><subject>Statistical methods</subject><subject>Steppes</subject><subject>Stresses</subject><subject>Thermogenesis</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2008</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNUl2LEzEUHURx19V_IDogCD605mMmM3kRlsWPwuKCX6_hZnKnnTJNukmm2H9v2o7aeRAkgYSbc869OZwse07JnPKKvl27wVvo51tncU4IoUXFHmSXVHI2E4zwh2f3i-xJCGtCSl4L8Ti7oDWjnNfkMrv_DHHw0OcBe2xi52wO1uRgYBu7Hea4c_1wLLs27zEVbZ52XGHumpWLzkLewqbr97nxiWBzvT--Nq43Odpd553doI2HFtFjCE-zRy30AZ-N51X2_cP7bzefZrd3Hxc317ezpmJ1nGkuEVtWVtgaTQuNXBrNqdREc6yhaAQQbbAkumICQAgpDW-RQ5tIvGb8Knt50t32LqjRraAop4zWtKplQixOCONgrba-24DfKwedOhacXyrwsWt6VJqyGsu2EE0lks9Sg5RMyJrwAljNq6T1buw26A2aJv04uToRnb7YbqWWbqcYlYWgh2FejQLe3Q8Y4j9Gnp9QS0hTdbZ1SaxJy-Cma1IS2i7Vr9OIQpS8LBLhzYSQMBF_xiUMIajF1y__j737McW-PsOuEPq4CmNUwhRYnICNdyF4bP94Qok6BPn3P9UhyGoMcqK9OPfzL2lMLv8Frl7w2Q</recordid><startdate>20080123</startdate><enddate>20080123</enddate><creator>Yang, 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selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress</title><author>Yang, Jie ; Wang, Zhen Long ; Zhao, Xin Quan ; Wang, De Peng ; Qi, De Lin ; Xu, Bao Hong ; Ren, Yong Hong ; Tian, Hui Fang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c728t-b39eef257efdb14be39db319b0b3e8a4c6a0bde50b726aa6699d3fe3aff253823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2008</creationdate><topic>Acids</topic><topic>Adaptation</topic><topic>Adaptation, Physiological</topic><topic>Amino Acid Sequence</topic><topic>Amino acid substitution</topic><topic>Amino acids</topic><topic>Animals</topic><topic>ATP synthase</topic><topic>Bioinformatics</topic><topic>Biological evolution</topic><topic>Biology</topic><topic>Cloning, Molecular</topic><topic>Cold</topic><topic>Cold regions</topic><topic>Cold Temperature</topic><topic>Deoxyribonucleic acid</topic><topic>Disease control</topic><topic>Disease prevention</topic><topic>DNA</topic><topic>DNA, Complementary</topic><topic>Ecological adaptation</topic><topic>Ecology/Evolutionary Ecology</topic><topic>Ecology/Physiological Ecology</topic><topic>Energy balance</topic><topic>Energy metabolism</topic><topic>Environmental factors</topic><topic>Environmental stress</topic><topic>Evolution</topic><topic>Evolution & development</topic><topic>Evolutionary Biology/Bioinformatics</topic><topic>Evolutionary Biology/Evolutionary and Comparative Genetics</topic><topic>Evolutionary Biology/Evolutionary Ecology</topic><topic>Fitness</topic><topic>Gene expression</topic><topic>Genetic research</topic><topic>High-altitude environments</topic><topic>Homeostasis</topic><topic>Hypoxia</topic><topic>Kinases</topic><topic>Laboratories</topic><topic>Lagomorpha</topic><topic>Leptin</topic><topic>Leptin - chemistry</topic><topic>Leptin - genetics</topic><topic>Leptin - physiology</topic><topic>Likelihood Functions</topic><topic>Metabolism</topic><topic>Mitochondrial DNA</topic><topic>Molecular Biology/Bioinformatics</topic><topic>Molecular Biology/Molecular Evolution</topic><topic>Molecular evolution</topic><topic>Molecular Sequence Data</topic><topic>Mutation</topic><topic>Natural selection</topic><topic>Nucleotide sequence</topic><topic>Ochotona</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Physiological aspects</topic><topic>Positive selection</topic><topic>Proteins</topic><topic>Regression analysis</topic><topic>Reproductive fitness</topic><topic>Selection, Genetic</topic><topic>Sequence Homology, Amino Acid</topic><topic>Spatial distribution</topic><topic>Statistical methods</topic><topic>Steppes</topic><topic>Stresses</topic><topic>Thermogenesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Jie</creatorcontrib><creatorcontrib>Wang, Zhen Long</creatorcontrib><creatorcontrib>Zhao, Xin 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Long</au><au>Zhao, Xin Quan</au><au>Wang, De Peng</au><au>Qi, De Lin</au><au>Xu, Bao Hong</au><au>Ren, Yong Hong</au><au>Tian, Hui Fang</au><au>Bromage, Timothy</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2008-01-23</date><risdate>2008</risdate><volume>3</volume><issue>1</issue><spage>e1472</spage><pages>e1472-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Environmental stress can accelerate the evolutionary rate of specific stress-response proteins and create new functions specialized for different environments, enhancing an organism's fitness to stressful environments. Pikas (order Lagomorpha), endemic, non-hibernating mammals in the modern Holarctic Region, live in cold regions at either high altitudes or high latitudes and have a maximum distribution of species diversification confined to the Qinghai-Tibet Plateau. Variations in energy metabolism are remarkable for them living in cold environments. Leptin, an adipocyte-derived hormone, plays important roles in energy homeostasis.
To examine the extent of leptin variations within the Ochotona family, we cloned the entire coding sequence of pika leptin from 6 species in two regions (Qinghai-Tibet Plateau and Inner Mongolia steppe in China) and the leptin sequences of plateau pikas (O. curzonia) from different altitudes on Qinghai-Tibet Plateau. We carried out both DNA and amino acid sequence analyses in molecular evolution and compared modeled spatial structures. Our results show that positive selection (PS) acts on pika leptin, while nine PS sites located within the functionally significant segment 85-119 of leptin and one unique motif appeared only in pika lineages-the ATP synthase alpha and beta subunit signature site. To reveal the environmental factors affecting sequence evolution of pika leptin, relative rate test was performed in pikas from different altitudes. Stepwise multiple regression shows that temperature is significantly and negatively correlated with the rates of non-synonymous substitution (Ka) and amino acid substitution (Aa), whereas altitude does not significantly affect synonymous substitution (Ks), Ka and Aa.
Our findings support the viewpoint that adaptive evolution may occur in pika leptin, which may play important roles in pikas' ecological adaptation to extreme environmental stress. We speculate that cold, and probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>18213380</pmid><doi>10.1371/journal.pone.0001472</doi><tpages>e1472</tpages><oa>free_for_read</oa></addata></record> |
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issn | 1932-6203 1932-6203 |
language | eng |
recordid | cdi_plos_journals_1312181789 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
subjects | Acids Adaptation Adaptation, Physiological Amino Acid Sequence Amino acid substitution Amino acids Animals ATP synthase Bioinformatics Biological evolution Biology Cloning, Molecular Cold Cold regions Cold Temperature Deoxyribonucleic acid Disease control Disease prevention DNA DNA, Complementary Ecological adaptation Ecology/Evolutionary Ecology Ecology/Physiological Ecology Energy balance Energy metabolism Environmental factors Environmental stress Evolution Evolution & development Evolutionary Biology/Bioinformatics Evolutionary Biology/Evolutionary and Comparative Genetics Evolutionary Biology/Evolutionary Ecology Fitness Gene expression Genetic research High-altitude environments Homeostasis Hypoxia Kinases Laboratories Lagomorpha Leptin Leptin - chemistry Leptin - genetics Leptin - physiology Likelihood Functions Metabolism Mitochondrial DNA Molecular Biology/Bioinformatics Molecular Biology/Molecular Evolution Molecular evolution Molecular Sequence Data Mutation Natural selection Nucleotide sequence Ochotona Phylogenetics Phylogeny Physiological aspects Positive selection Proteins Regression analysis Reproductive fitness Selection, Genetic Sequence Homology, Amino Acid Spatial distribution Statistical methods Steppes Stresses Thermogenesis |
title | Natural selection and adaptive evolution of leptin in the ochotona family driven by the cold environmental stress |
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