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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Veröffentlicht in:PloS one 2008-01, Vol.3 (1), p.e1472
Hauptverfasser: Yang, Jie, Wang, Zhen Long, Zhao, Xin Quan, Wang, De Peng, Qi, De Lin, Xu, Bao Hong, Ren, Yong Hong, Tian, Hui Fang
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Wang, Zhen Long
Zhao, Xin Quan
Wang, De Peng
Qi, De Lin
Xu, Bao Hong
Ren, Yong Hong
Tian, Hui Fang
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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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. 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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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identifier ISSN: 1932-6203
ispartof PloS one, 2008-01, Vol.3 (1), p.e1472
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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