Hot-blooded lizard illuminates endothermy origins

Abstract

Understanding the evolution of endothermy in birds and mammals is a central question in evolutionary physiology, because thermal biology intertwines with numerous ecologically important life-history traits, such as body size and shape, foraging ranges, growth rates and the production of offspring. Theories about the selective drivers for the evolution of endothermy have been debated for decades, and include: the prevention of overheating during locomotion; expanded ability to sustain exercise; the generation of heat during digestion; and parental control of the reproductive environment. The discovery that a lizard (Salvator merianae) develops endothermy when arousing from hibernation and preparing to reproduce by growing gonads, mating and depositing yolk in their eggs, recently reported by Glenn Tattersall and colleagues in Science Advances, informs this debate in a number of ways.The authors measured the environmental temperature and the body temperatures of adult male and female lizards weighing approximately 2 kg throughout the year. During the fall and winter, the lizards hibernate in underground burrows for 5–6 months. However, the researchers discovered that between days 160 and 180 of the hibernation fast, the night-time body temperature of both the males and females was raised markedly above the ambient temperature. At the end of the hibernation, the lizards resumed activity, basking during the day to supplement their own heat production and returning to the burrows at night. The team noticed that the lizards’ body temperatures remained elevated throughout the night, by up to 10°C above the burrow temperature, during the period when they were preparing to reproduce, whereas at other times of the year the nocturnal body temperatures equilibrated with the burrow. And when the authors placed fasting adults that were prepared to reproduce in a thermostatically controlled chamber for 8 days, they learned that the lizards maintained a body temperature that was higher than that of their surroundings without the benefit of heat generated by digestion or the insulation of their burrows. However, when the lizards were disturbed, their body temperature fell, perhaps because of heat loss caused by increased blood flow to the limbs, skin, tail, head or other peripheral tissues. So heat production and the ability to regulate body temperature were not associated with either feeding or activity in this lizard.The discovery that these lizards are able to maintain a body temperature that is greater than their surroundings is important in several ways. It refutes conventional wisdom, which holds that small animals that lack body insulation cannot raise body temperatures significantly, and complements previous work showing that, during reproduction, some species of python raise their body temperature up to 13°C above the surroundings when brooding eggs in insulated nests. It also shows that the ability to maintain a raised body temperature is not an oddity of one family of snake, but fits within a pattern of greater thermal stability during the reproductive period observed even in fully endothermic species, such as birds and mammals. Also, embryos are generally less tolerant of thermal fluctuations than adults, so it is not surprising to find strong selection for characteristics that confer thermal stability during development. Convergent evolution is one of the strongest lines of evidence for the significance of a characteristic; therefore, the discovery by Tattersall and colleagues of the convergent evolution of reproductive endothermy in this lizard supports the hypothesis that the same selective pressure drove the evolution of endothermy in birds and mammals.