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. 2022 Apr;97(2):766-801.
doi: 10.1111/brv.12822. Epub 2021 Dec 10.

Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians

Gordon Grigg  1 , Julia Nowack  2 , José Eduardo Pereira Wilken Bicudo  3 , Naresh Chandra Bal  4 , Holly N Woodward  5 , Roger S Seymour  6
Affiliations

Whole-body endothermy: ancient, homologous and widespread among the ancestors of mammals, birds and crocodylians

Gordon Grigg et al. Biol Rev Camb Philos Soc. 2022 Apr.

Abstract

The whole-body (tachymetabolic) endothermy seen in modern birds and mammals is long held to have evolved independently in each group, a reasonable assumption when it was believed that its earliest appearances in birds and mammals arose many millions of years apart. That assumption is consistent with current acceptance that the non-shivering thermogenesis (NST) component of regulatory body heat originates differently in each group: from skeletal muscle in birds and from brown adipose tissue (BAT) in mammals. However, BAT is absent in monotremes, marsupials, and many eutherians, all whole-body endotherms. Indeed, recent research implies that BAT-driven NST originated more recently and that the biochemical processes driving muscle NST in birds, many modern mammals and the ancestors of both may be similar, deriving from controlled 'slippage' of Ca2+ from the sarcoplasmic reticulum Ca2+ -ATPase (SERCA) in skeletal muscle, similar to a process seen in some fishes. This similarity prompted our realisation that the capacity for whole-body endothermy could even have pre-dated the divergence of Amniota into Synapsida and Sauropsida, leading us to hypothesise the homology of whole-body endothermy in birds and mammals, in contrast to the current assumption of their independent (convergent) evolution. To explore the extent of similarity between muscle NST in mammals and birds we undertook a detailed review of these processes and their control in each group. We found considerable but not complete similarity between them: in extant mammals the 'slippage' is controlled by the protein sarcolipin (SLN), in birds the SLN is slightly different structurally and its role in NST is not yet proved. However, considering the multi-millions of years since the separation of synapsids and diapsids, we consider that the similarity between NST production in birds and mammals is consistent with their whole-body endothermy being homologous. If so, we should expect to find evidence for it much earlier and more widespread among extinct amniotes than is currently recognised. Accordingly, we conducted an extensive survey of the palaeontological literature using established proxies. Fossil bone histology reveals evidence of sustained rapid growth rates indicating tachymetabolism. Large body size and erect stature indicate high systemic arterial blood pressures and four-chambered hearts, characteristic of tachymetabolism. Large nutrient foramina in long bones are indicative of high bone perfusion for rapid somatic growth and for repair of microfractures caused by intense locomotion. Obligate bipedality appeared early and only in whole-body endotherms. Isotopic profiles of fossil material indicate endothermic levels of body temperature. These proxies led us to compelling evidence for the widespread occurrence of whole-body endothermy among numerous extinct synapsids and sauropsids, and very early in each clade's family tree. These results are consistent with and support our hypothesis that tachymetabolic endothermy is plesiomorphic in Amniota. A hypothetical structure for the heart of the earliest endothermic amniotes is proposed. We conclude that there is strong evidence for whole-body endothermy being ancient and widespread among amniotes and that the similarity of biochemical processes driving muscle NST in extant birds and mammals strengthens the case for its plesiomorphy.

Keywords: UCP1; amniote heart; brown adipose tissue; endothermy; evolution; non-shivering thermogenesis; plesiomorphy; tachymetabolism; temperature regulation.

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Figures

Fig. 1
Fig. 1
Mechanisms of muscle non‐shivering thermogenesis (NST) in mammals and birds. The sarcoplasmic reticulum Ca2+‐ATPase (SERCA) is a Ca2+ pump involved in muscle contraction and thermogenesis. During the contraction–relaxation cycle (outside the box) SERCA uses ATP to pump Ca2+ from the cytosol into the sarcoplasmic reticulum (SR), which leads to muscle relaxation; Ca2+ leaves the SR through ryanodine receptor (RyR) channels causing muscle contraction. The boxed region relates to the shift to muscle NST in mammals and birds. In mammals the shift to NST is prompted by the attachment of a protein, sarcolipin (SLN) to SERCA, increasing its ATP utilisation by causing Ca2+ ‘slippage’, i.e. Ca2+ attaches to SERCA, but instead of being transported into the SR, Ca2+ is released again at the cytosolic side, producing heat from the ATP hydrolysis without actual muscle contraction. There is evidence of strong similarity between the mechanisms of muscle NST in birds and mammals (see Section II and Table 1), although the physiological role of SLN in bird muscle NST has not yet been demonstrated. Furthermore, how SLN or its equivalent in birds is recruited is still not fully understood. In mammals, data suggest the involvement of norepinephrine; this may be the case in birds too: there is evidence from ducklings of norepinephrine levels increasing in response to injection of glucagon (Filali‐Zegzouti et al., 2005). Figure derived from Bal et al. (2021). ETC, Electron Transport Chain.
Fig. 2
Fig. 2
Differences in energy metabolism and cardiovascular oxygen supply variables between representative ectotherms (blue) and endotherms (red). All graphs provide values for ectotherms as a proportion of those for endotherms, under similar temperatures and body sizes. The potential aerobic energy source is compared as total mitochondrial surface area (A) and maximum mitochondrial respiration rate (B). Rates of energy production include basal metabolic rate (C), an example of in vitro cellular respiration rate (D), maximum total power output (aerobic and anaerobic) during intense exercise (E) and maximum aerobic power output (F). On the bottom row are cardiovascular variables associated with delivery of oxygen for aerobic metabolism. Cardiac output during exercise (G) is similar to maximum aerobic power output (F). Vascular conductance (H) is the inverse of vascular resistance and suggests that blood flows more easily through the endotherm's circulation, however, the means are not significantly different. Mean systemic arterial blood pressure (MAP) during exercise is higher in endotherms (I), in direct association with higher cardiac output. The greater work of the endotherm heart is represented by greater ventricle mass (J). Finally, greater aerobic exercise levels of endotherms are matched by greater blood flow rates to the femur shaft through the nutrient foramen (K), presumably associated with repair of exercise‐induced microfractures (secondary osteon formation). The data are based on published information. Total mitochondrial inner surface area (A) is the sum of areas in all major tissues (liver, kidney, brain, heart, lung and skeletal muscle) and values for 1 kg animals are calculated from allometric equations (Else & Hulbert, 1985). Respiration rates of isolated mitochondria (B) are from similarly sized lizards and mice with succinate substrate at 37°C (Berner, 1999). Basal metabolic rates (C) are based on averages of 1 kg fish, amphibians and reptiles as ectotherms and mammals and birds as endotherms, all adjusted to 38°C (White, Phillips & Seymour, 2006). Liver cell respiration rates per mg of protein (D) are from rats and lizards at 37°C (Hulbert & Else, 2004). Maximum total power output (E) and maximum aerobic power output (F) are based on 1 kg crocodiles compared to mammals in general (Seymour, 2013). Cardiac output (G), systemic vascular conductance (H), mean systemic arterial blood pressure (MAP) (I) and relative left ventricle mass (J) are calculated for 1 kg animals from allometric equations (Hillman & Hedrick, 2015). Femur blood flow indices (K) in 1 kg mammals and non‐varanid reptiles are calculated from allometric equations (Seymour et al., 2012).
Fig. 3
Fig. 3
Relative sizes of some of the largest known members of Permian and Triassic sauropsids and synapsids, compared to a human and a 1 m scale. The vertical distances from the estimated heart position to the top of the body (H–H) are indicated. All of these animals, except for the captorhinid (Moradisaurus), must have had mean systemic arterial blood pressures (MAPs) higher than the 89 mm Hg (11.87 kPa) required to support a vertical blood column of 50 cm (P g  = 39 mm Hg, 5.20 kPa) with an adequate perfusion pressure against the vascular system's resistance (P r  = 50 mm Hg, 6.67 kPa). The total pressures are well within the range exhibited by extant tachymetabolic endotherms. Conversely, the largest captorhinid needed to support only a short vertical column of blood above the heart. It is important to realise, however, that a short H–H distance cannot be used as evidence of bradymetabolic ectothermy; small tachymetabolic endotherms typically have a high MAP but low H–H values.
Fig. 4
Fig. 4
Occurrences of tachymetabolic endothermy in amniote taxa, shown in red, as judged on the basis of criteria discussed in Section IV. Those for which the evidence is inconclusive are shown with a question mark. For taxa shown in black we found either no evidence for endothermy or no relevant information. The figure is indicative rather than comprehensive. The evidence on which the diagnosis for each taxon or taxonomic group is based is provided in Appendix S1. The identification of a clade as having tachymetabolic endothermy is not meant to imply necessarily that that tachymetabolism is characteristic of the whole group. We counted a strong indication of endothermy in one genus, for example, as an occurrence in that taxonomic group, even if an apparently ectothermic genus was also found. Assuming the proxies we used are valid, the results are congruent with our hypothesis that the capacity to express whole‐body endothermy arose very early in amniotes and that this capacity, seen in extant birds and mammals, is plesiomorphic. The results are also consistent with recent findings that all birds and many mammals possess similar biochemical machinery driving skeletal muscle NST, proposed as the ancient and still current source for NST in many, perhaps most extant mammals and all birds (supplemented by BAT in some eutherian mammals). Schematic phylogeny from multiple sources. Artwork by David Kirshner.
Fig. 5
Fig. 5
The hypothetical structure of the heart and outflow tracts of the earliest whole‐body (tachymetabolic) endothermic amniotes, shown schematically with the heart twisted as normal in relation to its outflow tracts (A) and untwisted in (B) to allow easier comparison with the thumbnail sketches (right) of four extant amniotes. All are represented as if viewed from below. Interventricular septa are drawn to represent their muscular and membranous sections. For the crocodylian (E) note the unusual location of the left aorta (LAo) exiting the right ventricle (RV) next to the exit leading to the pulmonary arteries (LPA and RPA), the foramen of Panizza depicted as a small gap in the common wall between the right and left aortae (RAo and LAo), and the cog‐tooth valve which contracts to initiate pulmonary bypass shunting. CA, coeliac artery; DAo, dorsal aorta; LAt, left atrium; LV, left ventricle; RAt, right atrium. Artwork by David Kirshner.
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References

    1. Affek, H. P. (2012). Clumped isotope paleothermometry: principles, applications, and challenges. The Paleontological Society Papers 18, 101–114.
    1. Allan, G. H. , Cassey, P. , Snelling, E. P. , Maloney, S. K. & Seymour, R. S. (2014). Blood flow for bone remodelling correlates with locomotion in living and extinct birds. Journal of Experimental Biology 217, 2956–2962. - PubMed
    1. * Allen, D. (2003). When Terrestrisuchus gracilis reaches puberty it becomes Saltoposuchus connectens! Journal of Vertebrate Paleontology 23, 29A.
    1. Amiot, R. , Lécuyer, C. , Buffetaut, E. , Escarguel, G. , Fluteau, F. & Martineau, F. (2006). Oxygen isotopes from biogenic apatites suggest widespread endothermy in Cretaceous dinosaurs. Earth and Planetary Science Letters 246, 41–54.
    1. Anderson, K . (2016). Multi‐omic analysis of hibernator skeletal muscle and calcium handling regulation. Retrieved from the University of Minnesota Digital Conservancy. https://hdl.handle.net/11299/181800.

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