Climate Variability and the Energetic Pathways of Evolution: The Origin of Endothermy in Mammals and Birds

• Published in: Physiological and biochemical zoology Vol. 77; no. 6; pp. 959 - 981
• Main Author: Portner, Hans O
• Format: Journal Article
• Language: English
• Published: United States The University of Chicago Press 01-11-2004
• Subjects: Adaptation, Physiological; Air; Animals; Aves; Biological Evolution; Birds; Birds - physiology; Body temperature; Cell Membrane - physiology; Climate; Climate models; Environment; Evolution; Heat tolerance; Invertebrates - physiology; Mammals; Mammals - physiology; Metabolism; Metazoa; Mitochondria - physiology; Oxygen; Reptiles - physiology; Thermogenesis - genetics; Thermogenesis - physiology
• ISSN: 1522-2152; 1537-5293
• DOI: 10.1086/423742

Large‐scale climate oscillations in earth’s history have influenced the directions of evolution, last but not least, through mass extinction events. This analysis tries to identify some unifying forces behind the course of evolution that favored an increase in organismic complexity and performance, paralleled by an increase in energy turnover, and finally led to endothermy. The analysis builds on the recent concept of oxygen‐limited thermal tolerance and on the hypothesis that unifying principles exist in the temperature‐dependent biochemical design of the eukaryotic cell in animals. The comparison of extant water‐breathing and air‐breathing animal species from various climates provides a cause‐and‐effect understanding of the trade‐offs and constraints in thermal adaptation and their energetic consequences. It is hypothesized that the high costs of functional adaptation to fluctuating temperatures, especially in the cold (cold eurythermy), cause an increase in energy turnover and, at the same time, mobility and agility. These costs are associated with elevated mitochondrial capacities at minimized levels of activation enthalpies for proton leakage. Cold eurythermy is seen as a precondition for the survival of evolutionary crises elicited by repeated cooling events during extreme climate fluctuations. The costs of cold eurythermy appear as the single most important reason why metazoan evolution led to life forms with high energy turnover. They also explain why dinosaurs were able to live in subpolar climates. Finally, they give insight into the pathways, benefits, and trade‐offs involved in the evolution of constant, elevated body temperature maintained by endothermy. Eurythermy, which encompasses cold tolerance, is thus hypothesized to be the “missing link” between ectothermy and endothermy. Body temperatures between 32° and 42°C in mammals and birds then result from trade‐offs between the limiting capacities of ventilation and circulation and the evolutionary trend to maximize performance at the warm end of the thermal tolerance window.