Experimental demonstration of prenatal programming of mitochondrial aerobic metabolism lasting until adulthood

Stier, A. , Monaghan, P. and Metcalfe, N. B. (2022) Experimental demonstration of prenatal programming of mitochondrial aerobic metabolism lasting until adulthood. Proceedings of the Royal Society of London Series B: Biological Sciences, 289(1970), 20212679. (doi: 10.1098/rspb.2021.2679) (PMID:35232239)

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Abstract

It is increasingly being postulated that among-individual variation in mitochondrial function underlies variation in individual performance (e.g. growth rate) and state of health. It has been suggested (but not adequately tested) that environmental conditions experienced before birth could programme postnatal mitochondrial function, with persistent effects potentially lasting into adulthood. We tested this hypothesis in an avian model by experimentally manipulating prenatal conditions (incubation temperature and stability) and then measuring mitochondrial aerobic metabolism in blood cells from the same individuals during the middle of the growth period and at adulthood. Mitochondrial aerobic metabolism changed markedly across life stages, and parts of these age-related changes were influenced by the prenatal temperature conditions. A high incubation temperature induced a consistent and long-lasting increase in mitochondrial aerobic metabolism. Postnatal mitochondrial aerobic metabolism was positively associated with oxidative damage on DNA but not telomere length. While we detected significant within-individual consistency in mitochondrial aerobic metabolism across life stages, the prenatal temperature regime only accounted for a relatively small proportion (less than 20%) of the consistent among-individual differences we observed. Our results demonstrate that prenatal conditions can programme consistent and long-lasting differences in mitochondrial function, which could potentially underlie among-individual variation in performance and health state.

Item Type:Articles
Additional Information:Funding: The project was funded by a Marie Sklodowska-Curie Postdoctoral Fellowship (grant no. 658085) to A.S., and A.S. was supported by a ‘Turku Collegium for Science and Medicine' Fellowship and a Marie Sklodowska-Curie Postdoctoral Fellowship (grant no. 894963) at the time of writing. P.M. was supported by ERC Advanced Grant no. 101020037 and N.B.M. by ERC Advanced Grant nos. 322784 and 834653.
Keywords:General Agricultural and Biological Sciences, General Environmental Science, General Immunology and Microbiology, General Biochemistry, Genetics and Molecular Biology, General Medicine
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Metcalfe, Professor Neil and Stier, Dr Antoine and Monaghan, Professor Pat
Authors: Stier, A., Monaghan, P., and Metcalfe, N. B.
College/School:College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
Journal Name:Proceedings of the Royal Society of London Series B: Biological Sciences
Publisher:The Royal Society
ISSN:0962-8452
ISSN (Online):1471-2954
Published Online:02 March 2022
Copyright Holders:Copyright © 2022 The Author(s)
First Published:First published in Proceedings of the Royal Society of London Series B: Biological Sciences 289(1970): 20212679
Publisher Policy:Reproduced in accordance with the publisher copyright policy
Data DOI:10.6084/m9.figshare.16708483.v1

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
312093InteragePatricia MonaghanEuropean Commission (EC)101020037Institute of Biodiversity, Animal Health and Comparative Medicine
305090MITOWILDNeil MetcalfeEuropean Commission (EC)834653Institute of Biodiversity, Animal Health and Comparative Medicine