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Litter characteristics and helping context during early life shape the responsiveness of the stress axis in a wild cooperative breeder

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Abstract

Stress responses have evolved to quickly and appropriately deal with environmental stressors in order to secure or restore homeostasis. Since the regulation of stress hormones plays a key adaptive role, the regulatory processes controlling stress hormones levels may be under high selective pressure. The social environment during early life (parents and litter characteristics) strongly affects ontogeny of the hypothalamic–pituitary–adrenal (HPA) axis. In cooperative breeders, offspring are also confronted with helpers but whether and how variation in the helping context can affect HPA axis responsiveness of offspring remains unanswered. Combining dexamethasone suppression and adrenocorticotropic hormone stimulation tests, we investigated the link between the social environment and the characteristics of the HPA axis at the early stages of life in wild Alpine marmots (Marmota marmota). We show that when raised in the presence of helpers, marmot pups exhibit a greater capacity not only to mount, but also to turn off a stress response. The capacity to mount a stress response was also higher as the pups were raised in large litters. Determining impacts of such social modulation of the HPA axis functioning on individual fitness would make an important contribution to our understanding of the evolution of cooperative breeding.

Significance statement

In recent decades, concepts of stress ecology have become essential for understanding the evolution of social behaviour and the diversity of individual trajectories in complex societies. However, very little is known about how the social environment shapes an individual’s physiological ability to respond to stressors in the wild. Here, we set up hormone challenge protocols in Alpine marmot pups to investigate the relationship between early life social context and functional characteristics of the stress axis in a wild cooperative breeder. We found that the regulatory activity of the stress axis is boosted in marmot pups raised in the presence of helpers. This regulatory activity is further enhanced when the pups are raised in large litters. Our data open up new avenues for our understanding of the evolution of cooperative breeding.

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Acknowledgements

We thank all the students and field assistants in marmot catching. We thank the municipality of Tignes for the use of the Santel chalet and the authorities of the Vanoise National Park for granting us permission to work in La Grande Sassière Nature Reserve. We are very grateful to the reviewers for their insightful comments and suggestions.

Funding

This work was supported by the French Agence Nationale pour la Recherche (ANR-13-JSV7-0005).

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Correspondence to Benjamin Rey.

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Fieldwork work was undertaken after the issuance of permit number AP n82010/121 by the Prefecture of Savoie. All applicable national and institutional guidelines for the use of animals were followed. All the procedures were approved by the ethical committee of the University Claude Bernard Lyon 1 (ethic approval numbers n8BH2012-92 V1 and 2017012500169084 v1).

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The authors declare no competing interests.

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Communicated by A. I Schulte-Hostedde

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Cohas, A., Bichet, C., Garcia, R. et al. Litter characteristics and helping context during early life shape the responsiveness of the stress axis in a wild cooperative breeder. Behav Ecol Sociobiol 75, 171 (2021). https://doi.org/10.1007/s00265-021-03108-y

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  • DOI: https://doi.org/10.1007/s00265-021-03108-y

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