Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

Patrick J. Tkaczynski; Fabrizio Mafessoni; Cédric Girard-Buttoz; Liran Samuni; Corinne Y. Ackermann; Pawel Fedurek; Cristina Gomes; Catherine Hobaiter; Therese Löhrich; Virgile Manin; Anna Preis; Prince D. Valé; Erin G. Wessling; Livia Wittiger; Zinta Zommers; Klaus Zuberbuehler; Linda Vigilant; Tobias Deschner; Roman M. Wittig; Catherine Crockford

doi:10.1038/s42003-023-04909-9

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

Patrick J. Tkaczynski^*, Fabrizio Mafessoni^*, Cédric Girard-Buttoz, Liran Samuni, Corinne Y. Ackermann, Pawel Fedurek, Cristina Gomes, Catherine Hobaiter, Therese Löhrich, Virgile Manin, Anna Preis, Prince D. Valé, Erin G. Wessling, Livia Wittiger, Zinta Zommers, Klaus Zuberbuehler, Linda Vigilant, Tobias Deschner, Roman M. Wittig, Catherine Crockford

^*Corresponding author for this work

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Abstract

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Original language	English
Article number	565
Number of pages	14
Journal	Communications Biology
Volume	6
Issue number	1
DOIs	https://doi.org/10.1038/s42003-023-04909-9
Publication status	Published - 26 May 2023

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Tkaczynski, P. J., Mafessoni, F., Girard-Buttoz, C., Samuni, L., Ackermann, C. Y., Fedurek, P., Gomes, C., Hobaiter, C., Löhrich, T., Manin, V., Preis, A., Valé, P. D., Wessling, E. G., Wittiger, L., Zommers, Z., Zuberbuehler, K., Vigilant, L., Deschner, T., Wittig, R. M., & Crockford, C. (2023). Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees. Communications Biology, 6(1), Article 565. https://doi.org/10.1038/s42003-023-04909-9

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title = "Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees",

abstract = "Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.",

author = "Tkaczynski, {Patrick J.} and Fabrizio Mafessoni and C{\'e}dric Girard-Buttoz and Liran Samuni and Ackermann, {Corinne Y.} and Pawel Fedurek and Cristina Gomes and Catherine Hobaiter and Therese L{\"o}hrich and Virgile Manin and Anna Preis and Val{\'e}, {Prince D.} and Wessling, {Erin G.} and Livia Wittiger and Zinta Zommers and Klaus Zuberbuehler and Linda Vigilant and Tobias Deschner and Wittig, {Roman M.} and Catherine Crockford",

note = "Funding: This study was funded by the Max Planck Society and the European Research Council (ERC) under the European Union{\textquoteright}s Horizon 2020 research and innovation program awarded to C.C. (grant agreement no. 679787). L.S. was supported by the Minerva Foundation, C.Y.A. and A.P. received funding from the LSB Leakey Foundation, C.Y.A. also received funding from Subvention Egalit{\'e} (University of Neuch{\^a}tel, Switzerland) and Fonds des Donations (University of Neuch{\^a}tel, Switzerland). C.G. was supported by the Wenner-Gren Foundation. VM was supported by a grant of Deutsche Forschungsgemeinschaft (DFG) granted to R.M.W. (WI 2637/3-1). Core funding for the Ta{\"i} Chimpanzee Project was provided by the Max Planck Society since 1997 and for Budongo Conservation Field Station by the Royal Zoological Society of Scotland since 2008. Open Access funding enabled and organized by Projekt DEAL.",

year = "2023",

month = may,

day = "26",

doi = "10.1038/s42003-023-04909-9",

language = "English",

volume = "6",

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issn = "2399-3642",

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Tkaczynski, PJ, Mafessoni, F, Girard-Buttoz, C, Samuni, L, Ackermann, CY, Fedurek, P, Gomes, C, Hobaiter, C, Löhrich, T, Manin, V, Preis, A, Valé, PD, Wessling, EG, Wittiger, L, Zommers, Z, Zuberbuehler, K, Vigilant, L, Deschner, T, Wittig, RM & Crockford, C 2023, 'Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees', Communications Biology, vol. 6, no. 1, 565. https://doi.org/10.1038/s42003-023-04909-9

TY - JOUR

T1 - Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

AU - Tkaczynski, Patrick J.

AU - Mafessoni, Fabrizio

AU - Girard-Buttoz, Cédric

AU - Samuni, Liran

AU - Ackermann, Corinne Y.

AU - Fedurek, Pawel

AU - Gomes, Cristina

AU - Hobaiter, Catherine

AU - Löhrich, Therese

AU - Manin, Virgile

AU - Preis, Anna

AU - Valé, Prince D.

AU - Wessling, Erin G.

AU - Wittiger, Livia

AU - Zommers, Zinta

AU - Zuberbuehler, Klaus

AU - Vigilant, Linda

AU - Deschner, Tobias

AU - Wittig, Roman M.

AU - Crockford, Catherine

N1 - Funding: This study was funded by the Max Planck Society and the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program awarded to C.C. (grant agreement no. 679787). L.S. was supported by the Minerva Foundation, C.Y.A. and A.P. received funding from the LSB Leakey Foundation, C.Y.A. also received funding from Subvention Egalité (University of Neuchâtel, Switzerland) and Fonds des Donations (University of Neuchâtel, Switzerland). C.G. was supported by the Wenner-Gren Foundation. VM was supported by a grant of Deutsche Forschungsgemeinschaft (DFG) granted to R.M.W. (WI 2637/3-1). Core funding for the Taï Chimpanzee Project was provided by the Max Planck Society since 1997 and for Budongo Conservation Field Station by the Royal Zoological Society of Scotland since 2008. Open Access funding enabled and organized by Projekt DEAL.

PY - 2023/5/26

Y1 - 2023/5/26

N2 - Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

AB - Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

U2 - 10.1038/s42003-023-04909-9

DO - 10.1038/s42003-023-04909-9

M3 - Article

SN - 2399-3642

VL - 6

JO - Communications Biology

JF - Communications Biology

IS - 1

M1 - 565

ER -

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees

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