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.
Highlights
The ability of heterothermic mammals to regulate or vary their body temperature (Tb) in response to changes in ambient temperature (Ta) and energy requirements is considered key to their evolutionary success, allowing them to survive in adverse climates and during periods when food is scarce [1,2]
Molecular phylogenetic analysis To assess the evolutionary history of Leptin in heterothermic bats, we carried out analyses of molecular evolution in a range of heterothermic and homeothermic bat lineages
Torpor in S. heathii and H. armiger at Ta 15uC was observed on both measurement days, but bats showed full or partial rewarming daily; at Ta 5uC both species hibernated without rewarming over the two days
Summary
The ability of heterothermic mammals to regulate or vary their body temperature (Tb) in response to changes in ambient temperature (Ta) and energy requirements is considered key to their evolutionary success, allowing them to survive in adverse climates and during periods when food is scarce [1,2]. Hibernating species of bats (some members of the superfamilies Emballonuroidea, Vespertilionoidea and Rhinolophoidea) are distributed in cool temperate or subtropical regions, whereas homeothermic bats are mainly tropical or subtropical [13]. Despite these differences in distribution and thermoregulatory patterns, little is known about the evolutionary history of heterothermy in bats. This is complicated further because phylogenetic reconstructions indicate that hibernation occurs in several branches across the mammalian tree [14]. Currently there is no obvious molecular marker that can be reliably associated with hibernation
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