Research Article: Adaptive Evolution of Leptin in Heterothermic Bats

Date Published: November 16, 2011

Publisher: Public Library of Science

Author(s): Lihong Yuan, Xudong Zhao, Benfu Lin, Stephen J. Rossiter, Lingjiang He, Xueguo Zuo, Guimei He, Gareth Jones, Fritz Geiser, Shuyi Zhang, Brock Fenton.


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.

Partial Text

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]. Heterothermy contrasts with homeothermy, characterized by a more or less constant and high Tb largely irrespective of Ta[3]. Heterothermy in mammals has been categorized as either daily torpor or prolonged multi-day torpor (hibernation), which the duration of torpor bouts last for less than 24 h and Tb maintained around 15°C–25°C in the former whereas between 100 h to 1000 h and Tb of 0–10°C in the latter [4]. Comparative data show that heterothermy is employed for energy conservation by members of at least ten orders of mammals, including monotremes, four marsupial orders, carnivores, rodents, eulipotyphlans (insectivores), bats and primates [5], [6], [7], [8], [9].

The evolutionary history of mammalian heterothermy remains a controversial subject although it is crucial to the success of a large number of species. In bats, which colonized and are occupying vastly diverse habitats, evolution of heterothermy is especially intriguing given their biogeography and their large range of thermoregulatory abilities. A number of scenarios regarding the evolution of heterothermy in bats have been proposed [1], [14]. If bats evolved in a temperate climate, hibernation is likely to be an ancestral trait that allowed bats to adapt to low environmental temperatures and limited food resources. As these lineages colonized tropical latitudes, the ability of hibernation was lost or was modified to become daily torpor [1]. Alternatively, if bats evolved in the tropics or subtropics and had the ability of daily heterothermy [37], hibernation in temperate species or homeothermy in tropical species are derived states [1]. A third possibility is that ancestral bats were homeothermic, although this seems unlikely given that homeothermy in extant bat taxa is relatively rare. Our data support the view of Lyman [1] that heterothermy in bats is an ancestral trait and was subsequently lost in now homeothermic bats. We provide physiological, molecular and biochemical evidence supporting this interpretation.