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Published June 16, 2022 | Supplemental Material
Journal Article Open

Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur

Abstract

Birds and mammals independently evolved the highest metabolic rates among living animals. Their metabolism generates heat that enables active thermoregulation, shaping the ecological niches they can occupy and their adaptability to environmental change. The metabolic performance of birds, which exceeds that of mammals, is thought to have evolved along their stem lineage. However, there is no proxy that enables the direct reconstruction of metabolic rates from fossils. Here we use in situ Raman and Fourier-transform infrared spectroscopy to quantify the in vivo accumulation of metabolic lipoxidation signals in modern and fossil amniote bones. We observe no correlation between atmospheric oxygen concentrations and metabolic rates. Inferred ancestral states reveal that the metabolic rates consistent with endothermy evolved independently in mammals and plesiosaurs, and are ancestral to ornithodirans, with increasing rates along the avian lineage. High metabolic rates were acquired in pterosaurs, ornithischians, sauropods and theropods well before the advent of energetically costly adaptations, such as flight in birds. Although they had higher metabolic rates ancestrally, ornithischians reduced their metabolic abilities towards ectothermy. The physiological activities of such ectotherms were dependent on environmental and behavioural thermoregulation, in contrast to the active lifestyles of endotherms1. Giant sauropods and theropods were not gigantothermic, but true endotherms. Endothermy in many Late Cretaceous taxa, in addition to crown mammals and birds, suggests that attributes other than metabolism determined their fate during the terminal Cretaceous mass extinction.

Additional Information

© The Author(s), under exclusive licence to Springer Nature Limited 2022. Received 09 July 2020; Accepted 19 April 2022; Published 25 May 2022. V. Rhue, K. Zyskowski and G. Watkins-Colwell facilitated specimen selection; T. Wu and M. Ghosh provided guidance for ATR FT-IR spectroscopy at the Yale West Campus Analytical Core. J.W. was supported by a Dissertation Improvement Grant from the Yale Institute for Biospheric Studies and a Graduate Student Research Grant from the Geological Society of America. I.M. was funded by a predoctoral grant from the Universidad Complutense de Madrid (CT27/16-CT28/16) and partially supported by project PGC2018-094955-A-I00 funded by the Spanish Ministerio de Ciencia, Innovación y Universidades. P.M.H. was funded by a Sloan Research Fellowship. Data availability: The Supplementary Information and Supplementary Data 1 and 2 contain all methods and source data: specimen information, method details, extracted S- and N-crosslink Raman intensities, formulae and conversions used to calculate the metabolic rates, details of regressions, data used for principal component and discriminant analyses, published body masses or body-mass estimates, correlation analyses, assessments of the prediction performance of various used regression models, assessments of potential data biases, labelled plots of all the analyses performed, data for the ancestral reconstruction. ATR FT-IR spectra are plotted in Extended Data Figs. 4, 5 and 6. Code availability: R code for phylogeny time-scaling and ancestral state reconstruction is available at GitHub (https://github.com/IrisMenendez/Dinosaur_metabolism). Contributions: J.W., J.M.C. and D.E.G.B. designed the project. M.F., J.A.G. and M.A.N. helped with specimen selection and sample materials preparation. J.W. designed the analytical strategy, performed Raman and FT-IR spectroscopy, processed and analysed the data and prepared the figures. J.W., P.M.H. and I.M. discussed statistical analyses. I.M. ran the time-calibrated ancestral state reconstruction. All authors discussed the data. J.W. and D.E.G.B. wrote the manuscript with input from all authors. The authors declare no competing interests. Peer review information: Nature thanks Kliti Grice, Marcin Kozanecki, Nick Stone and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Attached Files

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Additional details

Created:
August 22, 2023
Modified:
October 24, 2023