COS 133-3 - Physiological, ecological, and genomic underpinnings of daily torpor and hibernation across mammals and birds

Abstract: Numerous endotherm species have the ability to avoid challenging environmental conditions (e.g., limited food availability, heat waves) by becoming dormant for as little as a few hours (daily torpor) or for as long as several months (prolonged torpor or hibernation). Understanding the conditions under which various species may enter dormancy is important for forecasting the likely impacts of environmental changes on communities and ecosystems. Nevertheless, our current knowledge of the underlying factors that control and induce dormancy remains incomplete and phylogenetically fragmented due to both data and methodological limitations. For example, it is largely unexplored if the genes, physiology, and ecological preferences of dormancy-capable species are highly similar across diverse clades, or if they vary in a strongly clade-dependent manner. To answer this question, we classified 738 mammal and 601 bird species as hibernators, daily torpidators, or dormancy-incapable based on literature information. We then performed three sets of analyses. First, we fitted phylogenetic Markov models to examine the evolutionary transitions among the three dormancy states. Second, we collated a large literature dataset of more than 20 ecophysiological variables for each species where possible and inferred the correlations among all variables and dormancy state at the same time, accounting for phylogeny. Third, for species with available genomes, we performed scans for genes under positive selection and for gene losses to identify genes that underlie evolutionary shifts in dormancy.



Our analyses indicate that the three dormancy states are not isolated but form a continuum ranging from lack of dormancy to daily torpor to hibernation. In contrast, direct evolutionary transitions between hibernation and lack of dormancy (without daily torpor as an intermediate state) are nearly nonexistent. Across all endotherms in our dataset, species that are most likely to have the ability to enter dormancy are small nocturnal carnivores or omnivores occurring in seasonal, low-productivity environments. Other factors positively associated with dormancy include a predominantly terrestrial and fossorial lifestyle, and low mass-corrected values of basal metabolic rate and brain size. We also found that dormancy-capable species from certain clades form distinct clusters in trait space (e.g., Sciuridae, Trochilidae), even after accounting for phylogeny. Finally, we detected a number of genes that exhibit systematic associations with evolutionary shifts in dormancy states. All the aforementioned results deepen our understanding of dormancy at multiple levels and form a basis for predicting the dormancy capabilities of endotherms for which dormancy information is currently lacking.