Oxygen isotopes suggest elevated thermometabolism within multiple Permo-Triassic therapsid clades

Abstract

The only true living endothermic vertebrates are birds and mammals, which produce and regulate their internal temperature quite independently from their surroundings. For mammal ancestors, anatomical clues suggest that endothermy originated during the Permian or Triassic. Here we investigate the origin of mammalian thermoregulation by analysing apatite stable oxygen isotope compositions (δ18Op) of some of their Permo-Triassic therapsid relatives. Comparing of the δ18Op values of therapsid bone and tooth apatites to those of co-existing non-therapsid tetrapods, demonstrates different body temperatures and thermoregulatory strategies. It is proposed that cynodonts and dicynodonts independently acquired constant elevated thermometabolism, respectively within the Eucynodontia and Lystrosauridae + Kannemeyeriiformes clades. We conclude that mammalian endothermy originated in the Epicynodontia during the middle-late Permian. Major global climatic and environmental fluctuations were the most likely selective pressures on the success of such elevated thermometabolism.DOI: http://dx.doi.org/10.7554/eLife.28589.001

Endocranial Casts of Pre-Mammalian Therapsids Reveal an Unexpected Neurological Diversity at the Deep Evolutionary Root of Mammals

“…200-180 Ma) at the evolutionary root of the Mammaliaformes clade. Finding an estimated body temperature similar to those of modern mammals in Kawingasaurus , which is recognised as the most encephalised NMT yet identified [Laass and Kaestner, 2017], also supports that endothermy likely evolved multiple times in a convergent manner in therapsids [Botha-Brink et al, 2012;Rey et al, 2017]. However, it is important to note that the evolution of endothermy in the ancestry of mammals was likely a long, incremental, complex, and highly integrated process [Kemp, 2006;Hopson, 2012], and that, as an indirect proxy to infer metabolism, an enlarged brain alone does not constitute compelling evidence for endothermy [Bennett and Ruben, 1986].…”

“…However, until now they have given inconsistent results, leading to a general lack of consensus about the point of origin of endothermy in therapsid phylogeny [Owerkowicz et al, 2015]. For instance, the fossil record of turbinates seems to indicate a late Permian origin of endothermy [Hillenius, 1994;Hillenius and Ruben, 2004; but see Laass et al, 2010], whereas geochemistry indicates convergent evolution in multiple lineages during the Triassic [Rey et al, 2017]. Histology finally indicates multiple occurrences of fibrolamellar bone from the early Permian to the Triassic and in various taxa [Botha-Brink et al, 2012;Shelton and Sanders, 2017].…”

“…Numerous proxies have been used in order to reconstruct the evolution of endothermy in mammalian ancestry, ranging from limb posture to the presence of respiratory turbinates, and from geochemistry to histological analysis of bones [Roth et al, 1986;Hillenius and Ruben, 2004;BothaBrink et al, 2012;Rey et al, 2017]. However, until now they have given inconsistent results, leading to a general lack of consensus about the point of origin of endothermy in therapsid phylogeny [Owerkowicz et al, 2015].…”

Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps

“…The isotopic ratio between 16 O, the common form of oxygen, and 18 O, is used to infer body temperature. This ratio, measured in calcium phosphate from bones and, especially, dentary enamel, is dependent on environmental and body temperatures during the formation of the sample [12,58]. We can infer the relative internal body temperatures from calcium phosphate using fractionation equations [12,[58][59][60][61].…”

“…Oldest evidence for an insulative pelage (fossilized fur impressions) has been found in the Middle Jurassic non-mammalian therapsids (Castorocauda lutrasimilis [8], Megaconus mammaliaformis [9], Agilodocodon scansorius [10]). Thermal modelling [11], the isotopic composition of mineralized remains [12] and bone palaeohistology [1,[13][14][15] have also been used to infer the thermophysiology of non-mammalian synapsids. Here, we will use this last approach.…”