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The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population

E. I. K. Vitikainen Orcid Logo, M. Meniri Orcid Logo, H. H. Marshall Orcid Logo, F. J. Thompson Orcid Logo, R. Businge, F. Mwanguhya, S. Kyabulima, K. Mwesige, S. Ahabonya, J. L. Sanderson, G. Kalema-Zikusoka Orcid Logo, J. I. Hoffman Orcid Logo, D. Wells Orcid Logo, G. Lewis, S. L. Walker Orcid Logo, Hazel Nichols Orcid Logo, J. D. Blount Orcid Logo, M. A. Cant Orcid Logo

Philosophical Transactions of the Royal Society B: Biological Sciences, Volume: 378, Issue: 1883

Swansea University Author: Hazel Nichols Orcid Logo

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DOI (Published version): 10.1098/rstb.2022.0309

Abstract

Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring...

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Published in: Philosophical Transactions of the Royal Society B: Biological Sciences
ISSN: 0962-8436 1471-2970
Published: The Royal Society 2023
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URI: https://cronfa.swan.ac.uk/Record/cronfa63715
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spelling v2 63715 2023-06-27 The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population 43ba12986bd7754484874c73eed0ebfe 0000-0002-4455-6065 Hazel Nichols Hazel Nichols true false 2023-06-27 SBI Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring of receiving extra investment prenatally versus postnatally. We provided extra food to half of the breeding females in each group during pregnancy, leaving the other half as matched controls. This manipulation resulted in two categories of experimental offspring in synchronously born litters: (i) ‘prenatal boost’ offspring whose mothers had been fed during pregnancy, and (ii) ‘postnatal boost’ offspring whose mothers were not fed during pregnancy but who received extra alloparental care in the postnatal period. Prenatal boost offspring lived substantially longer as adults, but postnatal boost offspring had higher lifetime reproductive success (LRS) and higher glucocorticoid levels across the lifespan. Both types of experimental offspring had higher LRS than offspring from unmanipulated litters. We found no difference between the two experimental categories of offspring in adult weight, age at first reproduction, oxidative stress or telomere lengths. These findings are rare experimental evidence that prenatal and postnatal investments have distinct effects in moulding individual life history and fitness in wild mammals. Journal Article Philosophical Transactions of the Royal Society B: Biological Sciences 378 1883 The Royal Society 0962-8436 1471-2970 early life effects, cooperative breeding, social evolution, fetal programming, evolution of parental care 14 8 2023 2023-08-14 10.1098/rstb.2022.0309 http://dx.doi.org/10.1098/rstb.2022.0309 COLLEGE NANME Biosciences COLLEGE CODE SBI Swansea University Another institution paid the OA fee The research was funded by an ERC grant (grant no. 309249) and a Leverhulme International Fellowship to M.C. and a NERC standard grant (grant no. NE/N011171/1) to J.D.B. and M.A.C. The research was funded by an ERC grant (grant no. 309249) and a Leverhulme International Fellowship to M.C. and a NERC standard grant (grant no. NE/N011171/1) to J.D.B. and M.A.C. 2023-07-12T15:23:34.1289237 2023-06-27T09:30:31.3357570 Faculty of Science and Engineering School of Biosciences, Geography and Physics - Biosciences E. I. K. Vitikainen 0000-0003-3718-0941 1 M. Meniri 0000-0003-0400-3420 2 H. H. Marshall 0000-0003-2120-243x 3 F. J. Thompson 0000-0001-7581-2204 4 R. Businge 5 F. Mwanguhya 6 S. Kyabulima 7 K. Mwesige 8 S. Ahabonya 9 J. L. Sanderson 10 G. Kalema-Zikusoka 0000-0003-3473-3205 11 J. I. Hoffman 0000-0001-5895-8949 12 D. Wells 0000-0002-4531-5968 13 G. Lewis 14 S. L. Walker 0000-0003-3187-5195 15 Hazel Nichols 0000-0002-4455-6065 16 J. D. Blount 0000-0002-0016-0130 17 M. A. Cant 0000-0002-1530-3077 18 63715__27976__50b7ec5e80a44b0f99af3e7aaaa91547.pdf Vitikainen 2023 The social formation of fitness - consequences of prenatal nutrition and postnatal care.pdf 2023-06-27T09:39:26.9516034 Output 500204 application/pdf Version of Record true Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. true eng http://creativecommons.org/licenses/by/4.0/
title The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
spellingShingle The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
Hazel Nichols
title_short The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
title_full The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
title_fullStr The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
title_full_unstemmed The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
title_sort The social formation of fitness: lifetime consequences of prenatal nutrition and postnatal care in a wild mammal population
author_id_str_mv 43ba12986bd7754484874c73eed0ebfe
author_id_fullname_str_mv 43ba12986bd7754484874c73eed0ebfe_***_Hazel Nichols
author Hazel Nichols
author2 E. I. K. Vitikainen
M. Meniri
H. H. Marshall
F. J. Thompson
R. Businge
F. Mwanguhya
S. Kyabulima
K. Mwesige
S. Ahabonya
J. L. Sanderson
G. Kalema-Zikusoka
J. I. Hoffman
D. Wells
G. Lewis
S. L. Walker
Hazel Nichols
J. D. Blount
M. A. Cant
format Journal article
container_title Philosophical Transactions of the Royal Society B: Biological Sciences
container_volume 378
container_issue 1883
publishDate 2023
institution Swansea University
issn 0962-8436
1471-2970
doi_str_mv 10.1098/rstb.2022.0309
publisher The Royal Society
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Biosciences, Geography and Physics - Biosciences{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Biosciences, Geography and Physics - Biosciences
url http://dx.doi.org/10.1098/rstb.2022.0309
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description Research in medicine and evolutionary biology suggests that the sequencing of parental investment has a crucial impact on offspring life history and health. Here, we take advantage of the synchronous birth system of wild banded mongooses to test experimentally the lifetime consequences to offspring of receiving extra investment prenatally versus postnatally. We provided extra food to half of the breeding females in each group during pregnancy, leaving the other half as matched controls. This manipulation resulted in two categories of experimental offspring in synchronously born litters: (i) ‘prenatal boost’ offspring whose mothers had been fed during pregnancy, and (ii) ‘postnatal boost’ offspring whose mothers were not fed during pregnancy but who received extra alloparental care in the postnatal period. Prenatal boost offspring lived substantially longer as adults, but postnatal boost offspring had higher lifetime reproductive success (LRS) and higher glucocorticoid levels across the lifespan. Both types of experimental offspring had higher LRS than offspring from unmanipulated litters. We found no difference between the two experimental categories of offspring in adult weight, age at first reproduction, oxidative stress or telomere lengths. These findings are rare experimental evidence that prenatal and postnatal investments have distinct effects in moulding individual life history and fitness in wild mammals.
published_date 2023-08-14T15:23:29Z
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