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Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod

The dinosaur–bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as Troodon, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we ap...

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Autores principales: Tagliavento, Mattia, Davies, Amelia J., Bernecker, Miguel, Staudigel, Philip T., Dawson, Robin R., Dietzel, Martin, Götschl, Katja, Guo, Weifu, Schulp, Anne S., Therrien, François, Zelenitsky, Darla K., Gerdes, Axel, Müller, Wolfgang, Fiebig, Jens
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104568/
https://www.ncbi.nlm.nih.gov/pubmed/37011196
http://dx.doi.org/10.1073/pnas.2213987120
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author Tagliavento, Mattia
Davies, Amelia J.
Bernecker, Miguel
Staudigel, Philip T.
Dawson, Robin R.
Dietzel, Martin
Götschl, Katja
Guo, Weifu
Schulp, Anne S.
Therrien, François
Zelenitsky, Darla K.
Gerdes, Axel
Müller, Wolfgang
Fiebig, Jens
author_facet Tagliavento, Mattia
Davies, Amelia J.
Bernecker, Miguel
Staudigel, Philip T.
Dawson, Robin R.
Dietzel, Martin
Götschl, Katja
Guo, Weifu
Schulp, Anne S.
Therrien, François
Zelenitsky, Darla K.
Gerdes, Axel
Müller, Wolfgang
Fiebig, Jens
author_sort Tagliavento, Mattia
collection PubMed
description The dinosaur–bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as Troodon, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we applied dual clumped isotope (Δ(47) and Δ(48)) thermometry, a technique that resolves mineralization temperature and other nonthermal information recorded in carbonates, to eggshells from Troodon, modern reptiles, and modern birds. Troodon eggshells show variable temperatures, namely 42 and 29 ± 2 °C, supporting the hypothesis of an endothermic thermophysiology with a heterothermic strategy for this extinct taxon. Dual clumped isotope data also reveal physiological differences in the reproductive systems between Troodon, reptiles, and birds. Troodon and modern reptiles mineralize their eggshells indistinguishable from dual clumped isotope equilibrium, while birds precipitate eggshells characterized by a positive disequilibrium offset in Δ(48). Analyses of inorganic calcites suggest that the observed disequilibrium pattern in birds is linked to an amorphous calcium carbonate (ACC) precursor, a carbonate phase known to accelerate eggshell formation in birds. Lack of disequilibrium patterns in reptile and Troodon eggshells implies these vertebrates had not acquired the fast, ACC-based eggshell calcification process characteristic of birds. Observation that Troodon retained a slow reptile-like calcification suggests that it possessed two functional ovaries and was limited in the number of eggs it could produce; thus its large clutches would have been laid by several females. Dual clumped isotope analysis of eggshells of extinct vertebrates sheds light on physiological information otherwise inaccessible in the fossil record.
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spelling pubmed-101045682023-10-03 Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod Tagliavento, Mattia Davies, Amelia J. Bernecker, Miguel Staudigel, Philip T. Dawson, Robin R. Dietzel, Martin Götschl, Katja Guo, Weifu Schulp, Anne S. Therrien, François Zelenitsky, Darla K. Gerdes, Axel Müller, Wolfgang Fiebig, Jens Proc Natl Acad Sci U S A Physical Sciences The dinosaur–bird transition involved several anatomical, biomechanical, and physiological modifications of the theropod bauplan. Non-avian maniraptoran theropods, such as Troodon, are key to better understand changes in thermophysiology and reproduction occurring during this transition. Here, we applied dual clumped isotope (Δ(47) and Δ(48)) thermometry, a technique that resolves mineralization temperature and other nonthermal information recorded in carbonates, to eggshells from Troodon, modern reptiles, and modern birds. Troodon eggshells show variable temperatures, namely 42 and 29 ± 2 °C, supporting the hypothesis of an endothermic thermophysiology with a heterothermic strategy for this extinct taxon. Dual clumped isotope data also reveal physiological differences in the reproductive systems between Troodon, reptiles, and birds. Troodon and modern reptiles mineralize their eggshells indistinguishable from dual clumped isotope equilibrium, while birds precipitate eggshells characterized by a positive disequilibrium offset in Δ(48). Analyses of inorganic calcites suggest that the observed disequilibrium pattern in birds is linked to an amorphous calcium carbonate (ACC) precursor, a carbonate phase known to accelerate eggshell formation in birds. Lack of disequilibrium patterns in reptile and Troodon eggshells implies these vertebrates had not acquired the fast, ACC-based eggshell calcification process characteristic of birds. Observation that Troodon retained a slow reptile-like calcification suggests that it possessed two functional ovaries and was limited in the number of eggs it could produce; thus its large clutches would have been laid by several females. Dual clumped isotope analysis of eggshells of extinct vertebrates sheds light on physiological information otherwise inaccessible in the fossil record. National Academy of Sciences 2023-04-03 2023-04-11 /pmc/articles/PMC10104568/ /pubmed/37011196 http://dx.doi.org/10.1073/pnas.2213987120 Text en Copyright © 2023 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Physical Sciences
Tagliavento, Mattia
Davies, Amelia J.
Bernecker, Miguel
Staudigel, Philip T.
Dawson, Robin R.
Dietzel, Martin
Götschl, Katja
Guo, Weifu
Schulp, Anne S.
Therrien, François
Zelenitsky, Darla K.
Gerdes, Axel
Müller, Wolfgang
Fiebig, Jens
Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title_full Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title_fullStr Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title_full_unstemmed Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title_short Evidence for heterothermic endothermy and reptile-like eggshell mineralization in Troodon, a non-avian maniraptoran theropod
title_sort evidence for heterothermic endothermy and reptile-like eggshell mineralization in troodon, a non-avian maniraptoran theropod
topic Physical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10104568/
https://www.ncbi.nlm.nih.gov/pubmed/37011196
http://dx.doi.org/10.1073/pnas.2213987120
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