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Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur

Wiemann, Jasmina and Menéndez, Iris and Crawford, Jason M. and Fabbri, Matteo and Gauthier, Jacques A. and Hull, Pincelli M. and Norell, Mark A. and Briggs, Derek E. G. (2022) Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur. Nature, 606 (7914). pp. 522-526. ISSN 0028-0836. doi:10.1038/s41586-022-04770-6. https://resolver.caltech.edu/CaltechAUTHORS:20220531-924660000

[img] PDF (Details regarding specimen selection, organic matter endogeneity, a comparison of Raman metabolic rates and palaeohistological metabolic inferences, and the Supplementary Methods, Supplementary References, Supplementary Tables 1–4 and Supplementary Figs) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 1: Multivariate spectral analyses of biological signals in fossil amniote hard tissues) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 2: Intraskeletal variation of MCin vivo values (spectral crosslink-to-peptide ratios)) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 3: Modern and fossil crosslink-to-peptide (MCin vivo) ratios versus corresponding amniote body masses plotted from raw data) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 6: Net enrichment plot identifying Attenuated-reflectance Fourier-Transform Infrared (ATR FT-IR) spectral signatures that represent reaction educts (blue) and products (orange) of biomolecule fossilization in amniote bone) - Supplemental Material
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[img] Image (JPEG) (Extended Data Fig. 7: Linear regression (dotted line) of MCin vivo values and published metabolic rates in (n=25) extant amniote bones) - Supplemental Material
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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41586-022-04770-6DOIArticle
https://rdcu.be/cOGS9PublisherFree ReadCube access
https://github.com/IrisMenendez/Dinosaur_metabolismRelated ItemCode
ORCID:
AuthorORCID
Wiemann, Jasmina0000-0003-3581-1711
Menéndez, Iris0000-0003-1866-8351
Crawford, Jason M.0000-0002-7583-1242
Fabbri, Matteo0000-0002-1257-1594
Hull, Pincelli M.0000-0001-8607-4817
Norell, Mark A.0000-0002-1084-5555
Briggs, Derek E. G.0000-0003-0649-6417
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.
Funders:
Funding AgencyGrant Number
Yale Institute for Biospheric StudiesUNSPECIFIED
Geological Society of AmericaUNSPECIFIED
Universidad Complutense de MadridCT27/16-CT28/16
Ministerio de Ciencia, Innovación y Universidades (MICIU)PGC2018-094955-A-I00
Alfred P. Sloan FoundationUNSPECIFIED
Subject Keywords:Biogeochemistry; Metabolism; Palaeontology
Issue or Number:7914
DOI:10.1038/s41586-022-04770-6
Record Number:CaltechAUTHORS:20220531-924660000
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20220531-924660000
Official Citation:Wiemann, J., Menéndez, I., Crawford, J.M. et al. Fossil biomolecules reveal an avian metabolism in the ancestral dinosaur. Nature 606, 522–526 (2022). https://doi.org/10.1038/s41586-022-04770-6
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:114974
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:31 May 2022 22:40
Last Modified:28 Jun 2022 19:47

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