Abstract
Adverse experiences during early life exert important effects on development, health, reproduction, and social bonds, with consequences often persisting across generations. A mother’s early life experiences can impact her offspring’s development through a number of pathways, such as maternal care, physiological signaling through glucocorticoids, or even intergenerational effects like epigenetic inheritance. Early life adversity in female yellow baboons (Papio cynocephalus) predicts elevated glucocorticoids, reduced sociality, shortened lifespan, and higher offspring mortality. If baboon mothers with more early life adversity, experience poorer condition and struggle to provide for their offspring, this could contribute to the persisting transgenerational effects of adversity. Here, we examined the effects of mothers’ early life adversity on their maternal effort, physiology, and offspring survivability in a population of olive baboons, Papio anubis. Mothers who experienced more adversity in their own early development exerted greater maternal effort (i.e., spent more time nursing and carrying) and had higher levels of glucocorticoid metabolites than mothers with less early life adversity. Offspring of mothers with more early life adversity had reduced survivability compared to offspring of mothers with less early life adversity. There was no evidence that high maternal social rank buffered the effects of early life adversity. Our data suggest early life experiences can have lasting consequences on maternal effort and physiology, which may function as proximate mechanisms for intergenerational effects of maternal experience.
Significance statement
Animals exposed to early life adversity experience both immediate and lasting consequences. If early life adversity exerts developmental constraints that affect a mother’s ability to provide for her offspring, this could explain the transgenerational effects of early life adversity. In our study of wild olive baboons, we examined how a mother’s own early life adversity predicts her maternal effort (i.e., nursing and carrying time), maternal fecal glucocorticoid levels, and offspring outcomes. We found that female baboons who experienced more early life adversity had higher glucocorticoid levels during pregnancy and lactation, exerted more maternal effort, and produced offspring with higher mortality risk than females with less early life adversity. Our results suggest that female baboons with more early life adversity experience developmental constraints and struggle to invest in offspring, which likely contributes to persisting effects of early life adversity across generations.
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Data availability
The datasets generated and analyzed for the current study are available in the supplementary materials.
Code availability
Model code is available at: https://github.com/skpatter/Maternal_early_life_adversity.
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Acknowledgements
We thank the Office of the President of the Republic of Kenya and the Kenya Wildlife Service for permission to conduct this field research. We thank Kate Abderholden, Megan Best, Megan Cole, Moira Donovan, Alexandra Duchesneau, Jessica Gunson, Molly McEntee, Laura Peña, Eila Roberts, and Leah Worthington for their contributions to data collection. We thank the staff of the Uaso Ngiro Baboon Project, particularly Jeremiah Lendira, James King’au, Joshua Lendira, and Frances Molo for their help and companionship in the field; David Muiruri for invaluable assistance with logistics and data management; and the African Conservation Centre for facilitating the UNBP project and assisting us with our work. We thank Jacinta Beehner, Sofia Carrera, Elizabeth Tinsley Johnson, Rupert Palme, Eila Roberts, and Sharmi Sen for guidance with hormonal analysis in the field and laboratory. We thank Joel Bray, Ian Gilby, Caitlin Hawley, Kevin Langergraber, Kevin Lee, Sarah Mathew, Tom Morgan, Shannon Roivas, India Schneider-Crease, Veronika Städele, the editor, and two anonymous reviewers for comments and helpful suggestions on earlier versions of this manuscript.
Funding
Research was supported with funds to SKP from the National Science Foundation (BCS-1732172); the Leakey Foundation, Arizona State University; and with funds to JBS from Arizona State University. SKP was supported by the National Science Foundation Graduate Research Fellowship under grant no. 1841051.
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The study conformed to US and Kenyan laws and was approved by the National Commission for Science and Technology of Kenya and the Kenya Wildlife Service. All animal protocols adhered to the guidelines set forth by the Animal Behaviour Society/Association for the Study of Animal Behaviour. The project was approved by the Arizona State University Institutional Care and Use Committee.
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Patterson, S.K., Hinde, K., Bond, A.B. et al. Effects of early life adversity on maternal effort and glucocorticoids in wild olive baboons. Behav Ecol Sociobiol 75, 114 (2021). https://doi.org/10.1007/s00265-021-03056-7
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DOI: https://doi.org/10.1007/s00265-021-03056-7