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Adaptive evolution of Leptin in heterothermic bats.

ABSTRACT: Heterothermy (hibernation and daily torpor) is a key strategy that animals use to survive in harsh conditions and is widely employed by bats, which are found in diverse habitats and climates. Bats comprise more than 20% of all mammals and although heterothermy occurs in divergent lineages of bats, suggesting it might be an ancestral condition, its evolutionary history is complicated by complex phylogeographic patterns. Here, we use Leptin, which regulates lipid metabolism and is crucial for thermogenesis of hibernators, as molecular marker and combine physiological, molecular and biochemical analyses to explore the possible evolutionary history of heterothermy in bat. The two tropical fruit bats examined here were homeothermic; in contrast, the two tropical insectivorous bats were clearly heterothermic. Molecular evolutionary analyses of the Leptin gene revealed positive selection in the ancestors of all bats, which was maintained or further enhanced the lineages comprising mostly heterothermic species. In contrast, we found evidence of relaxed selection in homeothermic species. Biochemical assays of bat Leptin on the activity on adipocyte degradation revealed that Leptin in heterothermic bats was more lipolytic than in homeothermic bats. This shows that evolutionary sequence changes in this protein are indeed functional and support the interpretation of our physiological results and the molecular evolutionary analyses. Our combined data strongly support the hypothesis that heterothermy is the ancestral state of bats and that this involved adaptive changes in Leptin. Subsequent loss of heterothermy in some tropical lineages of bats likely was associated with range and dietary shifts.

SUBMITTER: Yuan L

PROVIDER: S-EPMC3217946 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Adaptive evolution of Leptin in heterothermic bats.

Yuan Lihong L Zhao Xudong X Lin Benfu B Rossiter Stephen J SJ He Lingjiang L Zuo Xueguo X He Guimei G Jones Gareth G Geiser Fritz F Zhang Shuyi S

PloS one 20111116 11

Heterothermy (hibernation and daily torpor) is a key strategy that animals use to survive in harsh conditions and is widely employed by bats, which are found in diverse habitats and climates. Bats comprise more than 20% of all mammals and although heterothermy occurs in divergent lineages of bats, suggesting it might be an ancestral condition, its evolutionary history is complicated by complex phylogeographic patterns. Here, we use Leptin, which regulates lipid metabolism and is crucial for ther ...[more]

PMID: 22110614

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Project description:BackgroundExpansions of gene families are predictive for ongoing genetic adaptation to environmental cues. We describe such an expansion of the carcinoembryonic antigen (CEA) gene family in certain bat families. Members of the CEA family in humans and mice are exploited as cellular receptors by a number of pathogens, possibly due to their function in immunity and reproduction. The CEA family is composed of CEA-related cell adhesion molecules (CEACAMs) and secreted pregnancy-specific glycoproteins (PSGs). PSGs are almost exclusively expressed by trophoblast cells at the maternal-fetal interface. The reason why PSGs exist only in a minority of mammals is still unknown.ResultsAnalysis of the CEA gene family in bats revealed that in certain bat families, belonging to the subgroup Yangochiroptera but not the Yinpterochiroptera subgroup an expansion of the CEA gene family took place, resulting in approximately one hundred CEA family genes in some species of the Vespertilionidae. The majority of these genes encode secreted PSG-like proteins (further referred to as PSG). Remarkably, we found strong evidence that the ligand-binding domain (IgV-like domain) of PSG is under diversifying positive selection indicating that bat PSGs may interact with structurally highly variable ligands. Such ligands might represent bacterial or viral pathogen adhesins. We have identified two distinct clusters of PSGs in three Myotis species. The two PSG cluster differ in the amino acids under positive selection. One cluster was only expanded in members of the Vespertilionidae while the other was found to be expanded in addition in members of the Miniopteridae and Mormoopidae. Thus one round of PSG expansion may have occurred in an ancestry of all three families and a second only in Vespertilionidae. Although maternal ligands of PSGs may exist selective challenges by two distinct pathogens seem to be likely responsible for the expansion of PSGs in Vespertilionidae.ConclusionsThe rapid expansion of PSGs in certain bat species together with selection for diversification suggest that bat PSGs could be part of a pathogen defense system by serving as decoy receptors and/or regulators of feto-maternal interactions.

Dataset Information

Adaptive evolution of Leptin in heterothermic bats.

Publications

Adaptive evolution of Leptin in heterothermic bats.

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