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Were the Synapsids Primitively Endotherms? a Palaeohistological Approach Using Phylogenetic Eigenvector Maps Mathieu Faure-Brac, Jorge Cubo

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Were the Synapsids Primitively Endotherms? a Palaeohistological Approach Using Phylogenetic Eigenvector Maps Mathieu Faure-Brac, Jorge Cubo Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps Mathieu Faure-Brac, Jorge Cubo To cite this version: Mathieu Faure-Brac, Jorge Cubo. Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps. Philosophical Transactions of the Royal Society B: Biological Sciences, Royal Society, The, 2020, 375 (1793), pp.20190138. 10.1098/rstb.2019.0138. hal-02447334 HAL Id: hal-02447334 https://hal.archives-ouvertes.fr/hal-02447334 Submitted on 19 Feb 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Were the synapsids primitively endotherms? Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps Mathieu G. Faure-Brac1 and Jorge Cubo1* 1Sorbonne UniversitÉ, MNHN, CNRS, Centre de Recherche en PalÉontologie ­ Paris (CR2P), Paris, France *Corresponding author: [email protected] Peer­reviewed research published in: Faure­Brac, M. G., & Cubo, J. (2020). Were the synapsids primitively endotherms? A palaeohistological approach using phylogenetic eigenvector maps. Philosophical Transactions of the Royal Society B. 2020;375(1793):20190138. DOI: https://doi.org/10.1098/rstb.2019.0138. The acquisition of mammalian endothermy is poorly constrained both phylogenetically and temporally. Here we inferred the resting metabolic rates (RMR) and the thermometabolic regimes (endothermy or ectothermy) of a sample of eight extinct synapsids using palaeohistology, phylogenetic eigenvector maps, and a sample of seventeen extant tetrapods of known RMR (quantified using respirometry). We inferred high RMR values and an endothermic metabolism for the anomodonts (Lystrosaurus sp., Oudenodon baini) and low RMR values and an ectothermic metabolism for Clepsydrops collettii, Dimetrodon sp., Edaphosaurus boanerges, Mycterosaurus sp., Ophiacodon uniformis and Sphenacodon sp. A maximum likelihood ancestral states reconstruction of resting metabolic rates performed using the values inferred using phylogenetic eigenvector maps in extinct synapsids, and the values measured using respirometry in extant tetrapods, shows that the nodes Anomodontia and Mammalia were primitively endotherms. Finally, we performed a parsimony optimisation of the presence of endothermy using the results obtained in the present study and those obtained in previous studies that used phylogenetic eigenvector maps. For this, we assigned to each extinct taxa a thermometabolic regime (ectothermy or endothermy) depending on whether the inferred values were significantly higher, lower or not −1 −0.67 significantly different from the RMR value separating ectotherms from endotherms (1.5 mL O2 .h .g ). According to this optimisation, endothermy arose independently in Archosauromorpha, in Sauropterygia, and in Therapsida. Keywords: endothermy; synapsids; quantitative paleohistology; paleophysiology 1 Were the synapsids primitively endotherms? Introduction basal metabolic rates” (21) and (B) empirical evidence: the variation of bone growth rates significantly explained One of the greatest challenges of current research in the variation of resting metabolic rates in a sample of palaeobiology is the inference of physiological features of extant amniotes (19). More recently, quantitative extinct vertebrates. Among them, endothermy is histology and phylogenetic eigenvector maps (13,22) particularly relevant because this feature is linked to a allowed to infer directly the resting metabolic rates of wide array of anatomical, physiological and behavioural extinct Archosauromorpha (1,13), Sauropterygia (15) and features. Endothermy has been defined as the presence of extinct Therapsida (14). More recently, quantitative any mechanism of non­shivering thermogenesis that histology and phylogenetic eigenvector maps (13,22) increases both body temperature and resting metabolic allowed to infer directly the resting metabolic rates of rate (1). Mammals, the only extant synapsids, are extinct Archosauromorpha (1,13), Sauropterygia (15) and endotherms (2–5). The origin of mammalian endothermy extinct Therapsida (14). is poorly constrained both phylogenetically and Olivier et al. (14) used this last approach and provided temporally, in spite of the fact that the acquisition of this evidence for an ancestral acquisition of endothermy at the ability is a key innovation (endotherms are less dependent node Eutherapsida. However, the sample composition of on climatic conditions and can occupy more ecological this study (14) did not allow to test the hypothesis of an niches (6)). Many approaches have been used to constrain acquisition of endothermy in a more inclusive node. Thus, the phylogenetic and temporal frames of this acquisition. the present study is aimed at further constraining the One of them involves identifying unequivocal anatomical temporal range and the phylogenetic frame of the correlates of endothermy such as respiratory turbinates or acquisition of endothermy in Synapsids. To do so, we will evidence for an insulative pelage (7). Respiratory infer the metabolic rates of a sample of extinct synapsids turbinates are rarely preserved in fossils but bone ridges (including Carboniferous non­neotherapsid synapsids) of turbinate attachment are first recognizable in using a recently developed bone histological variable, the therocephalians and in cynodonts (7), so they may have relative primary osteon area (RPOA) (named previously been acquired by the eutheriodonts. Oldest evidence for primary osteon density in 15), and phylogenetic an insulative pelage (fossilized fur impressions) has been eigenvector maps (PEM) (13,22). found in the Middle Jurassic nonmammalian therapsids (Castorocauda lutrasimilis (Ji, Luo, Yuan et Tabrum, Material and Methods 2006) (8); Megaconus mammaliaformis (Zhou, Wu, Material Martin et Luo, 2013) (9); Agilodocodon scansorius (Meng, Ji, Zhang, Liu, Grossnickle et Luo, 2015) (10)). We analysed femora of a total of 25 species of Thermal modelling (11), the isotopic composition of tetrapods. Seventeen of them are extant tetrapods: three mineralized remains (12) and bone palaeohistology (1,13– archosaurs (Gallus gallus (Linnaeus, 1758), Anas 15) have also been used to infer the thermophysiology of platyrhynchos (Linnaeus, 1758) and Crocodylus niloticus nonmammalian synapsids. Here we will use this last (Laurenti, 1768)), four lepidosaurs (Varanus approach. exanthematicus (Bosc, 1792), Varanus niloticus Traditionally, qualitative bone histology has been used (Linnaeus, 1758), Podarcis muralis (Laurenti, 1768) and to estimate the bone growth rate (16–18), indirectly linked Zootoca vivipara (Lichtenstein, 1823)), three turtles to the metabolic rate, i.e. the rate of energy expenditure, (Chelodina oblonga (Gray J.E., 1841), Pelodiscus and to the thermometabolism (19,20). This framework is sinensis (Wiegmann, 1835) and Trachemys scripta based on (A) theoretical grounds “the types of tissue (Thunberg in Schoepff, 1792)), six mammals (Capreolus deposited in the bones of extinct animals are the most capreolus (Linnaeus, 1758), Microcebus murinus (Miller, direct evidence of basal metabolic rates, because they 1777), Mus musculus (Linnaeus, 1758), Cavia porcellus directly reflect growth rates [...]. The sustained deposition (Linnaeus, 1758), Lepus europaeus (Pallas, 1778) and of fast­growing bone tissues, as displayed by mammals, Oryctolagus cuniculus (Linaeus, 1758)) and one amphibia birds and other dinosaurs, must reflect sustained high (Pleurodeles waltl (Michahelles, 1830)), acting as 2 Were the synapsids primitively endotherms? an outgroup for our analyses. bone growth rate (BGR) and BGR to histological features, The remaining eight species are extinct synapsids. The then histological features can be used as a proxy to infer histological thin sections of the Anomodontia metabolic rates (19,20). However, considering that (Lystrosaurus sp. (Cope, 1870) and Oudenodon bainii metabolic rate is linked to other functions, as locomotion, (Owen, 1860)) analysed were previously studied by digestion, reproduction and regulation, we need to Olivier et al. (14). They are the closest relatives of extant standardise it. For adult endothermic amniotes the basal mammals in our sample. Both of them come from late metabolic rate (BMR) has been defined as the minimum Permian and, in the case of Lystrosaurus, it can be found rate of energy expenditure measured under thermoneutral until the early Triassic. The other extinct taxa of the and postabsorptive conditions in the inactive phase of the sample are older: Clepsydrops collettii (Cope, 1875), the daily cycle (27). For adult ectothermic amniotes the oldest known synapsid, and Ophiacodon uniformis (Cope, standard metabolic rate (SMR) has been defined as the 1878) belong to the Ophiacodontidae clade; Dimetrodon minimum rate of energy expenditure measured at a given sp. (Cope, 1878) and Sphenacodon sp. (Marsh, 1878) temperature within the animal’s range of activity (28) or belong to the Sphenacodontidae clade; Mycterosaurus
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