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.

MicroRNAs (miRNAs) regulate many physiological processes through post-transcriptional control of gene expression and are a major part of the small noncoding RNAs (snRNA). As hibernators can survive at low body temperatures (Tb) for many months without suffering tissue damage, understanding the mechanisms that enable them to do so are of medical interest. Because the brain integrates peripheral physiology and white adipose tissue (WAT) is the primary energy source during hibernation, we hypothesized that both of these organs play a crucial role in hibernation, and thus, their activity would be relatively increased during hibernation. We carried out the first genomic analysis of small RNAs, specifically miRNAs, in the brain and WAT of a hibernating bat (Myotis ricketti) by comparing deeply torpid with euthermic individual bats using high-throughput sequencing (Solexa) and qPCR validation of expression levels. A total of 196 miRNAs (including 77 novel bat-specific miRNAs) were identified, and of these, 49 miRNAs showed significant differences in expression during hibernation, including 33 in the brain and 25 in WAT (P≤0.01 &│logFC│≥1). Stem-loop qPCR confirmed the miRNA expression patterns identified by Solexa sequencing. Moreover, 31 miRNAs showed tissue- or state-specific expression, and six miRNAs with counts >100 were specifically expressed in the brain. Putative target gene prediction combined with KEGG pathway and GO annotation showed that many essential processes of both organs are significantly correlated with differentially expressed miRNAs during bat hibernation. This is especially evident with down-regulated miRNAs, indicating that many physiological pathways are altered during hibernation. Thus, our novel findings of miRNAs and Interspersed Elements in a hibernating bat suggest that brain and WAT are active with respect to the miRNA expression activity during hibernation.

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Adipose tissue is an important endocrine organ and energy supplier. Its physiological effect on the regulation of the energy balance is considered an important factor underlying the evolution of mammals. To test whether the genes controlling lipid metabolism have undergone adaptive molecular change in the evolution of mammals, in this study, we used the orthologous gene sequences of 12 important lipid metabolism proteins (leptin, OB-RL, RXRA, RXRB, RXRG, PPARA, PPARB/D, PPARG, PNLIP, ADIPOQ, LPL and UCP1) from NCBI's databases. We found evidence that 4 of the corresponding genes (leptin, ADIPOQ, PNLIP and PPARA) have undergone positive selection in their evolutionary history and that most adaptive changes occurred during the evolution of the super-clades Laurasiatheria (placentals) and suborders within Euarchontoglires (primates and rodents). Comparisons across sets of genes showed that in a third of cases, bursts of positive selection, more than would be expected by chance, occurred on corresponding branches. We propose that the positive selection drives adaptive changes in some lipid metabolism genes in or within Laurasiatheria and Euarchontoglires clades. Along with evidence from earlier studies, our results show that co-evolution among interacting lipid metabolism proteins has taken place. protein evolution; lipid metabolism; Darwinian selection, positive selection Citation:Lin B F, Yuan L H, Chen J P. Selection pressure drives the co-evolution of several lipid metabolism genes in mammals. Chin Sci Bull, 2012, 57: 877885,

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