A unifying, eco‐physiological framework for animal dormancy

Abstract

1. Various animals across the tree of life express some form of programmed dormancy (e.g. hibernation, diapause) to maximize fitness in highly seasonal environments. The integrated phenotype of animals undergoing programmed dormancy is strikingly similar among diverse groups; however, research on programmed dormancy has historically been phylogenetically siloed. A broad comparative approach could clarify new angles for answering fundamental questions about programmed dormancy evolution. 2. To advance this approach, we present a cross-taxonomic framework describing dimensions that distinguish animal dormancies and provide a set of core traits that animals regulate as they progress through the eco-physiological phases of deep, programmed dormancy. 3. We use this universal framework to explore the ultimate drivers and evolutionary consequences of dormancy across the tree of life. Deep, programmed dormancy appears to be a predictable and repeated adaptation to highly seasonal environments that draws on a conserved suite of ancestral traits. We highlight evidence for molecular convergence in signalling pathways coordinating environmental sensing and energy metabolism in the insect and mammal lineages, separated by 700 million years of evolution and representing independent colonizations of highly seasonal environments. 4. Lastly, we discuss the utility of this new framework and highlight opportunities and challenges for researchers to continue advancing our understanding of dormancy through a broad, comparative lens.

Snow modulates winter energy use and cold exposure across an elevation gradient in a montane ectotherm

“…One key difference between these approaches is that mechanistic niche models initiate and terminate "winter" according to the microclimate conditions rather than calendar date (Fitzpatrick et al, 2019(Fitzpatrick et al, , 2020, whereas we used fixed thresholds based on natural history observations, effectively assuming that phenology is independent of site-to-site microclimate variation. Spring emergence can be either environmentally cued or endogenously determined in animals that undergo programmed dormancy (Wilsterman et al, 2020), suggesting that both approaches may capture ecologically relevant responses. If beetles are emerging from dormancy as soon as energy use increases in the spring, the energetic costs of winter will be overestimated in our analysis at some sites and years, due to the inclusion of the spring increase in energy use.…”

“…Snow buffers the soil from cold air temperatures in winter, providing a thermally stable microhabitat for the vast array of terrestrial ectotherms (and hibernating endotherms) that overwinter in dormancy in the subnivium (below‐snow habitat) or soil (Pauli et al, 2013; Slatyer et al, 2021; Wilsterman et al, 2020; Zhang, 2005). Across the Western United States, anthropogenic climate change is causing increased frequency of drought, which is leading to more frequent winters with low snowpack (Huning & AghaKouchak, 2020; Mote et al, 2018; Stewart et al, 2004).…”

Different ways to play it cool: Transcriptomic analysis sheds light on different activity patterns of three amphipod species under long‐term cold exposure

“…According to the dynamic energy budget model, organisms allocate available energy primarily to growth, activity, reproduction, and basal maintenance (Sokolova et al, 2012). In order to survive in the cold during hibernation, energy is entirely allocated to basal maintenance (Wilsterman et al, 2021). Accordingly, we found a high proportion of suppressed genes related to activity, growth, and reproduction in cold‐exposed G. lacustris .…”

Temperature and development drive variation in oral morphology among tailed frog (Ascaphusspp.) populations

“…Understanding the evolution of traits is an enduring and influential research theme in ecology (Knott et al, 2019). The need for interdisciplinary and multi-scale approaches to uncover complex ecological interactions (Thompson et al, 2001;Reiners et al, 2017;McCallen et al, 2019) has led to the development of integrative frameworks that can help account for interacting intrinsic and extrinsic drivers of phenotypic variation (e.g., Sultan, 2007;Sanger and Rajakumar, 2019;Skúlason et al, 2019;Wilsterman et al, 2020). In this study, we used a framework combining approaches from ecology, evolution, and development (eco-evo-devo framework; Skúlason et al, 2019) to uncover drivers of labial tooth number variation in two species of tailed frog, Ascaphus montanus and A. truei.…”