The development of sustained, long-term endothermy was one of the major transitions in the evolution of vertebrates. Thermogenesis in endotherms does not only occur via shivering or activity, but also via nonshivering thermogenesis (NST). Mammalian NST is mediated by the uncoupling protein 1 in the brown adipose tissue (BAT) and possibly involves an additional mechanism of NST in skeletal muscle. This alternative mechanism is based on Ca2+-slippage by a sarcoplasmatic reticulum Ca2+-ATPase (SERCA) and is controlled by the protein sarcolipin. The existence of muscle based NST has been discussed for a long time and is likely present in all mammals. However, its importance for thermoregulation was demonstrated only recently in mice. Interestingly, birds, which have evolved from a different reptilian lineage than mammals and lack UCP1-mediated NST, also exhibit muscle based NST under the involvement of SERCA, though likely without the participation of sarcolipin. In this review we summarize the current knowledge on muscle NST and discuss the efficiency of muscle NST and BAT in the context of the hypothesis that muscle NST could have been the earliest mechanism of heat generation during cold exposure in vertebrates that ultimately enabled the evolution of endothermy. We suggest that the evolution of BAT in addition to muscle NST was related to heterothermy being predominant among early endothermic mammals. Furthermore, we argue that, in contrast to small mammals, muscle NST is sufficient to maintain high body temperature in birds, which have enhanced capacities to fuel muscle NST by high rates of fatty acid import.

Increased winter survival by reducing energy expenditure in adult animals is often viewed as the primary function of torpor. However, torpor has many other functions that ultimately increase the survival of heterothermic mammals and birds. In this review, we summarize new findings revealing that animals use torpor to cope with the conditions during and after natural disasters, including fires, storms, and heat waves. Furthermore, we suggest that torpor, which also prolongs longevity and was likely crucial for survival of mammals during the time of the dinosaur extinctions, will be advantageous in a changing world. Climate change is assumed to lead to an increase in the occurrence and intensity of climatic disasters, such as those listed above and also abnormal floods, droughts, and extreme temperatures. The opportunistic use of torpor, found in many heterothermic species, will likely enhance survival of these challenges, because these species can reduce energy and foraging requirements. However, many strictly seasonal hibernators will likely face the negative consequences of the predicted increase in temperature, such as range contraction. Overall, available data suggest that opportunistic heterotherms with their flexible energy requirements have an adaptive advantage over homeotherms in response to unpredictable conditions.

The whole‐body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non‐shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole‐body endotherms. Indeed, recent research implies that BAT‐driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled ‘slippage’ of Ca ²⁺ from the sarcoplasmic reticulum Ca ²⁺ ‐ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole‐body endothermy could even have pre‐dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole‐body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the ‘slippage’ is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi‐millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole‐body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four‐chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole‐body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole‐body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole‐body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.

Mammalian heterotherms, species that employ short or long periods of torpor, are found in many different climatic regions. Although the underlying physiological mechanisms of heterothermy in species from lower latitudes (i.e., the tropics and southern hemisphere) appear analogous to those of temperate and arctic heterotherms, the ultimate triggers and resulting patterns of energy expenditure and body temperature are often noticeably different. Phenotypic flexibility in the patterns of thermoregulation in non-Holarctic species can be extensive (depending on body condition, environmental parameters and species competition) and the factors responsible for inducing heterothermy are more variable in non-Holarctic species. As well as being a regular adaptation to seasonality, heterothermy can also be employed as a response to unpredictability in environmental parameters and as a response to emergency situations. Non-Holarctic heterotherms also challenge the notion that regular inter-bout arousals during hibernation are obligatory and suggest all that is necessary to maintain proper functioning during hibernation is an occasional passive return to—or maintenance of—a relatively high body temperature. The study of non-Holarctic heterotherms has led to the conclusion that heterothermy must be defined on the basis of mechanistic, physiological parameters, and not solely by body temperature; yet we are still limited in our abilities to record such mechanistic parameters in the field. It is now believed that homeothermy in mammals evolved in hot climates via an ancestral heterothermic state. Similar to extant warm-climate heterotherms, early mammals could have relied mainly on passive body temperature regulation with a capacity for short- to longer-term up-regulation of metabolism when needed. Hibernation, as seen in temperate and arctic species may then be a derived state of this ancestral heterothermy, and the study of torpor in warm climates can provide potential models for the energetics of early mammals.

Although storms provide an extreme environmental challenge to organisms and are predicted to increase in frequency and intensity due to climate change, there are no quantitative observations on the behaviour and physiology of animals during natural disasters. We provide the first data on activity and thermal biology of a free-ranging, arboreal mammal during a storm with heavy rain and category 1 cyclone wind speeds. We studied a population of sugar gliders (Petaurus breviceps), a species vulnerable to bad weather due to their small body size and mode of locomotion, in a subtropical habitat during spring when storms are common. Although torpor is generally rare in this species, sugar gliders remained inactive or reduced foraging times during the storm and further minimized energy demands by entering deep torpor. All animals survived the storm and reverted to normal foraging activity during the following night(s). It thus appears that heterothermic mammals have a crucial adaptive advantage over homeothermic species as they can outlast challenging weather events, such as storms and floods, by reducing metabolism and thus energetic needs.

We experimentally tested the costs of deep torpor at low temperatures by comparing telomere dynamics in two species of rodents hibernating at either 3 or 14°C. Our data show that hibernators kept at the warmer temperature had higher arousal frequencies, but maintained longer telomeres than individuals hibernating at the colder temperature. We suggest that the high-energy demand of frequent arousals is counteracted by a lower temperature differential between torpid and euthermic body temperature and that telomere length is restored during arousals when the body temperature is returned to normothermic values. Taken together, our study shows that hibernation at low body temperatures comes with costs on a cellular level and that hibernators need to actively counterbalance the shortening of telomeres.