Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 6

Oxygen Isotopes Suggest Elevated Thermometabolism Within Multiple Permo-Triassic Therapsid Clades

Affiliations

Oxygen Isotopes Suggest Elevated Thermometabolism Within Multiple Permo-Triassic Therapsid Clades

Kévin Rey et al. Elife.

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.

Keywords: ecology; endothermy; none; permo-triassic; stable isotopes; therapsids.

Conflict of interest statement

The authors declare that no competing interests exist.

Figures

Figure 1.
Figure 1.. δ18Op differences between Permian therapsids and other tetrapods.
Differences in δ18Op values between therapsids and stereospondyls (white symbols) and between therapsids and parareptiles (black symbols) from the same localities are plotted against their corresponding palaeolatitude. A theoretical framework based on modern temperature gradient (0.6 ± 0.1°C/°Lat; see Appendix 1) and phosphate-water-temperature oxygen isotope fractionation (Lécuyer et al., 2013) predicts various δ18Op value differences. The lighter orange and red areas correspond to the uncertainty of the temperature gradient. Dap.: Daptocephalus; Tap.: Tapinocephalus. DOI: http://dx.doi.org/10.7554/eLife.28589.003
Figure 2.
Figure 2.. δ18Op differences between Early to Middle Triassic therapsids and other tetrapods.
Differences in δ18Op values between therapsids and stereospondyls (white symbols) and between therapsids and archosauriforms (black symbols) from the same localities are plotted against their corresponding palaeolatitude. A theoretical framework based on a lower-than-today thermal gradient (0.4 ± 0.1°C/°Lat; see Appendix 1) and phosphate-water-temperature oxygen isotope fractionation (Lécuyer et al., 2013) predicts various δ18Op value differences. The lighter orange and red areas correspond to the uncertainty of the temperature gradient. DOI: http://dx.doi.org/10.7554/eLife.28589.004
Figure 3.
Figure 3.. δ18Op differences between Middle to latest Triassic therapsids and other tetrapods.
Differences in δ18Op values between therapsids and stereospondyls (white symbols) and between therapsids and archosauriforms (black symbols) from the same localities are plotted against their corresponding palaeolatitude. A theoretical framework based on a lower-than-today thermal gradient (0.5 ± 0.1°C/°Lat; see Appendix 1) and phosphate-water-temperature oxygen isotope fractionation (Lécuyer et al., 2013) predicts various δ18Op value differences. The lighter orange and red areas correspond to the uncertainty of the temperature gradient. DOI: http://dx.doi.org/10.7554/eLife.28589.005
Figure 4.
Figure 4.. Phylogeny of sampled therapsids.
Phylogeny of the sampled therapsids plotted alongside a stratigraphic scale, based on proposed therapsid phylogenies (Ruben and Jones, 2000; Hillenius and Ruben, 2004; Gebauer, 2007; Cisneros et al., 2012; Liu, 2013; Ruta et al., 2013) and their biostratigraphic ranges (Kammerer et al., 2011; Kemp, 2012; Ruta et al., 2013; Huttenlocker, 2014; Day et al., 2015; Viglietti et al., 2016). The thickest parts of the bold lines represent the age range uncertainty of the localities where the samples come from. Species identified as endotherm-like are written in bold and red. Node numbers refer to clades quoted in the text: 1: Neotherapsida; 2: Dicynodontoidea; 3: Lystrosauridae; 4: Kannemeyeriiformes; 5: Epicynodontia; 6: Eucynodontia. DOI: http://dx.doi.org/10.7554/eLife.28589.006
Figure 5.
Figure 5.. Isotopic preservation assessment.
δ18Oc18Op differences between teeth and bones plotted against the structural carbonate content (wt%) of apatite. Samples that have δ18Oc18Op differences higher than 14.7‰ are considered doubtful as regards potential diagenetic alteration (see text). For carbonate contents (wt%) higher than 13.4%, the δ18Oc values are considered to be inherited from inorganic diagenetic processes. A high difference between δ18Oc and δ18Op is interpreted as the result of a microbially-mediated alteration of the apatite phosphate or too high δ18Oc values resulting from the addition of inorganic carbonate or isotopic exchange with an external source of inorganic carbon. The grey crosses refer to previously published South African bone and tooth samples (Rey et al., 2016). DOI: http://dx.doi.org/10.7554/eLife.28589.007
Appendix 1—figure 1.
Appendix 1—figure 1.. Expected latitudinal variation of the δ18Op difference between vertebrate taxa of various physiologies and ecologies.
Based on modern relationships between climate and phosphate-water-temperature oxygen isotope fractionation (Lécuyer et al., 2013) the following δ18Op values differences are predicted: (1) corresponds to a terrestrial endotherm compared to a terrestrial ectotherm; (2) corresponds to a terrestrial endotherm compared to a semi-aquatic ectotherm; The vertical range (3) corresponds to terrestrial animals having similar thermometabolism; (4) corresponds to the difference between a terrestrial and a semi-aquatic animals having a similar thermometabolism. DOI: http://dx.doi.org/10.7554/eLife.28589.009

Similar articles

See all similar articles

Cited by 5 PubMed Central articles

References

    1. Abdala F, Jashashvili T, Rubidge BS, Heever J. New Material of Microgomphodon oligocynus (Eutherapsida, Therocephalia) and the Taxonomy of Southern African Bauriidae. In: Kammerer C. F, Angielczyk K. D, Fröbisch J, editors. Early Evolutionary History of the Synapsida, Vertebrate Paleobiology and Paleoanthropology. Netherlands: Springer; 2014. pp. 209–231.
    1. Abdala F, Ribeiro AM. Distribution and diversity patterns of Triassic cynodonts (Therapsida, Cynodontia) in Gondwana. Palaeogeography, Palaeoclimatology, Palaeoecology. 2010;286:202–217. doi: 10.1016/j.palaeo.2010.01.011. - DOI
    1. Amiot R, Buffetaut E, Lecuyer C, Wang X, Boudad L, Ding Z, Fourel F, Hutt S, Martineau F, Medeiros MA, Mo J, Simon L, Suteethorn V, Sweetman S, Tong H, Zhang F, Zhou Z. Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology. 2010;38:139–142. doi: 10.1130/G30402.1. - DOI
    1. Amiot R, Lécuyer C, Buffetaut E, Escarguel G, Fluteau F, Martineau F. Oxygen isotopes from biogenic apatites suggest widespread endothermy in cretaceous dinosaurs. Earth and Planetary Science Letters. 2006;246:41–54. doi: 10.1016/j.epsl.2006.04.018. - DOI
    1. Amiot R, Lécuyer C, Buffetaut E, Fluteau F, Legendre S, Martineau F. Latitudinal temperature gradient during the Cretaceous Upper Campanian–Middle Maastrichtian: δ18O record of continental vertebrates. Earth and Planetary Science Letters. 2004;226:255–272. doi: 10.1016/j.epsl.2004.07.015. - DOI

Publication types

Substances

Grant support

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Feedback