Hibernation in bats (Mammalia: Chiroptera) did not evolve through positive selection of leptin

Abstract

Temperature regulation is an indispensable physiological activity critical for animal survival. However, relatively little is known about the origin of thermoregulatory regimes in a phylogenetic context, or the genetic mechanisms driving the evolution of these regimes. Using bats as a study system, we examined the evolution of three thermoregulatory regimes (hibernation, daily heterothermy, and homeothermy) in relation to the evolution of leptin, a protein implicated in regulation of torpor bouts in mammals, including bats. A threshold model was used to test for a correlation between lineages with positively selected lep, the gene encoding leptin, and the thermoregulatory regimes of those lineages. Although evidence for episodic positive selection of lep was found, positive selection was not correlated with lineages of heterothermic bats, a finding that contradicts results from previous studies. Evidence from our ancestral state reconstructions suggests that the most recent common ancestor of bats used daily heterothermy and that the presence of hibernation is highly unlikely at this node. Hibernation likely evolved independently at least four times in bats—once in the common ancestor of Vespertilionidae and Molossidae, once in the clade containing Rhinolophidae and Rhinopomatidae, and again independently in the lineages leading to Taphozous melanopogon and Mystacina tuberculata. Our reconstructions revealed that thermoregulatory regimes never transitioned directly from hibernation to homeothermy, or the reverse, in the evolutionary history of bats. This, in addition to recent evidence that heterothermy is best described along a continuum, suggests that thermoregulatory regimes in mammals are best represented as an ordered continuous trait (homeothermy ← → daily torpor ← → hibernation) rather than as the three discrete regimes that evolve in an unordered fashion. These results have important implications for methodological approaches in future physiological and evolutionary research.

How weather triggers the emergence of bats from their subterranean hibernacula

“…The timing of arousal after hibernation is part of a bat’s circannual rhythm, which has been demonstrated for many hibernating animal species and is of particular importance in perennial organisms 65 , 66 . Although the underlying mechanisms for circannual rhythms are still not well understood 67 , our study sheds new light on the interplay of weather and residual triggers for the synchronization of species specific emergence from their hibernacula.…”

Unexpected expression of heat-activated transient receptor potential (TRP) channels in winter torpid bats and cold-activated TRP channels in summer active bats

“…Bats (order Chiroptera) are the only mammals that can fly ( Teeling et al, 2005 ). They are endothermic heterotherms ( Lazzeroni et al, 2018 ) and usually maintain their body temperature around 37 °C. They can enter torpor at ambient temperatures ranging from −10 °C to 21 °C ( Webb et al, 2011 ).…”

Sequencing the Genome of Indian Flying Fox, Natural Reservoir of Nipah Virus, Using Hybrid Assembly and Conservative Secondary Scaffolding

“…Although bats make up more than 20% of existing mammals with 1,400 species ( Lazzeroni et al, 2018 ), only 38 bat genome assemblies are currently available in the NCBI Genbank database. Several different sequencing strategies have been used in the past years to sequence bat genomes, including (i) high coverage long-read sequencing strategy, e.g., 83x of PacBIO Eonycteris spelaea ( Wen et al, 2018 ), (ii) Illumina sequencing (e.g., 93x for paired-end libraries and 67x of mate-pair libraries) for P. alecto ( Zhang et al, 2013 ) and also (iii) hybrid sequencing, e.g., 145x of Illumina short reads and 24x of PacBio long-reads for Rousettus aegyptecus ( Pavlovich et al, 2018 ).…”