The origin of mammalian endothermy: a paradigm for the evolution of complex biological structure

Abstract

Several mutually incompatible theories exist about how and why endothermy evolved in mammals and birds. Some take the primary function to have been thermoregulation, selected for one adaptive purpose or another. Others take the high aerobic metabolic rate to have been primary. None of these theories is incontrovertibly supported by evidence, either from the fossil record of the synapsid amniotes or from observations and experiments on modern organisms. Furthermore, all are underpinned by the tacit assumption that endothermy must have evolved in a stepwise pattern, with an initial adaptive function followed only later by the addition of further functions. It is argued that this assumption is unrealistic and that the evolution of endothermy can be explained by the correlated progression model. Each structure and function associated with endothermy evolved a small increment at a time, in loose linkage with all the others evolving similarly. The result is that the sequence of organisms maintained functional integration throughout, and no one of the functions of endothermy was ever paramount over the others. The correlated progression model is tested by the nature of the integration between the parts as seen in living mammals, by computer simulations of the evolution of complex, multifunctional, multifactorial biological systems, and by reference to the synapsid fossil record, which is fully compatible with the model. There are several potentially important implications to be drawn from this example concerning the study of the evolution of complex structure and the new higher taxa that manifest it.

Comparative Morphology of the Internal Nasal Skeleton of Adult Marsupials Based on X-ray Computed Tomography

“…Some have suggested that ridges on the internal surfaces of the nasal cavity of therocephalians, a lineage of nonmammalian therapsids that is the sister taxon to cynodonts, served for attachment of turbinal elements (Hillenius, 1994). However, the interpretation of these ridges is debated in the literature (e.g., Kemp, 2006) and there are no preserved ossified turbinals in these specimens. Furthermore, ossified turbinals were not observed in key nonmammalian cynodont taxa (e.g., Hadrocodium wui; Macrini, 2006;Rowe et al, 2011) that are closely related to crown Mammalia.…”

Endothermy in birds: underlying molecular mechanisms

“…In chickens however, the increases in oxidative capacity (state 3 respiration rate) are accompanied by increased uncoupling of oxidative phosphorylation and increased cellular ATP demand, both of which reduce the ATP available for activity. It is unlikely, therefore, that the advantages of increased activity or any other single initial selection pressure led to modern endothermic phenotypes (Kemp, 2006). Complex organismal functions such as endothermy evolve by the gradual integration of genetic changes that affect suborganismal traits, without the need for evolutionary transitions of individual traits to contribute directly to the more complex function (Lenski et al, 2003).…”

“…In contrast to mammals (Kemp, 2006), the origin and mechanisms that led to endothermy in the Archosauria is controversial and one of the most hotly debated topics in vertebrate evolution (Gillooly et al, 2006;Seebacher, 2003;Seymour et al, 2004). At present there is no agreement even about whether ancestral archosaurs were endotherms or ectotherms (Ruben, 1995;Seymour et al, 2004), although there is little doubt that ectothermy is ancestral to endothermy (Hillenius and Ruben, 2004).…”

Body temperatures of modern and extinct vertebrates from 13 C- 18 O bond abundances in bioapatite

“…The acquisition of endothermy, the ability to maintain high and stable body temperatures through internal heat production, is a major physiological change that occurred at an unknown stage during the evolutionary transition to mammals and birds from their ancestors among the nonmammalian therapsids and nonavian dinosaurs, respectively (1). Approaches to understanding the physiology of extinct animals and the evolution of endothermy have largely focused on biophysical modeling, anatomical observations, growth rate analysis from bone histology, and behavioral studies such as estimating predator/prey ratios (1)(2)(3)(4)(5)(6)(7). The validity of each of these approaches is uncertain (for contrasting viewpoints on approaches to dinosaur thermoregulation see refs.…”