The Evolution of Endothermy and Its Diversity in Mammals and Birds

Abstract

Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.

Relationships between integumental characteristics and thermoregulation in South American camelids

“…In mammals, endothermic homoeothermy generally results from a combination of high resting, aerobically supported heat production rates (about five-to tenfold that of reptiles) in all soft tissues and sufficient insulation to retard excessive heat loss (Ruben, 1995;Grigg et al, 2004).…”

“…It is assumed that mammalian hair evolved about 200 million years ago (Ruben, 1995;Meng and Wyss, 1997;Grigg et al, 2004). The recent identification of reptilian genes -E-mail: mgerken@gwdg.de encoding hair keratin-like proteins revealed a new insight into the evolutionary origin of hair (Eckhart et al, 2008).…”

“…Several functions have been attributed to hair fibre including barrier to cutaneous water loss, mechanical protection against abrasion of the skin, camouflage or display through hair pigmentation and an important role for endothermy (Grigg et al, 2004). Hair fibre in mammals has some apparent advantages for thermoregulation over scales as found in ectotherm reptiles as it allows a more flexible adaptation of the body surface to environmental conditions.…”

Association between obesity and reduced body temperature in dogs

“…As homeothermy can account for 2/3 or more of energy expenditure in mammals and birds, 6,7 a small reduction in body temperature could yield great energy savings, thus favoring energy storage and the consequent development of obesity. In other words, by lowering body temperature, the organism might achieve a state of enhanced metabolic efficiency that could lead to obesity.…”

A simple molecular mathematical model of mammalian hibernation

“…Mechanisms of regulating hibernation could vary greatly among mammals -certainly the patterns of body temperatures do (Grigg et al, 2004;Hut et al, 2002a). Our model is derived primarily from species of the order Rodentia, particularly ground squirrels and chipmunks.…”