Abstract

BackgroundEnvironmental 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.Methodology/Principal FindingsTo 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 α and β 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.Conclusions/SignificanceOur 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.

Highlights

  • The environment is an important driver for organismic natural selection

  • A 646-bp fragment in pikas and a 565-bp fragment from both Lepus oiostolus and Oryctolagus cuniculus, which contained the complete coding region, were cloned, respectively. These sequences were submitted to GenBank and were assigned the following accession numbers: DQ983189 (Ochotona curzoniae); EF091861 (Ochtona nubrica); EF091863 (Ochotona cansus cansus 1); EF091864 (Ochotona cansus cansus 2); EF091862 (Ochotona annecten); EF091860 (Ochotona daurica bedfordi); DQ983190 (Lepus oiostolus), and DQ983191 (Oryctolagus cuniculus)

  • The deduced amino acid sequences were composed of 167 amino acids and encoded an apparent signal peptide sequence of 21 amino acids with the signal cleavage site between a non-polar (Ala)-21 and Val-22

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Summary

Introduction

The environment is an important driver for organismic natural selection. Environmental changes or climatic fluctuations can make organisms evolve rapidly into different morphologic or taxonomic groups or create new functions specialized in different individual living environments [1]. Organismic evolution is the process by which an organism must repetitiously overcome new conditions and create a new set of unique metabolic reactions to a particular environmental stress This adaptive response to changing environmental conditions results in an acceleration of evolutionary rate of the lineage and the functional evolution of specific stress-response proteins, which favors organismic fitness to a new environment. 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. Probably not hypoxia, may be the primary environmental factor for driving adaptive evolution of pika leptin

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