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Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas

Abstract

Within any hierarchical society, an individual's social rank can have profound effects on its health and reproductive success1,2, and rank-related variation in these traits is often mediated by variation in endocrine function2. Maternal effects mediated by prenatal hormone exposure are potentially important for non-genetic inheritance of phenotypic traits related to social rank3, and thus for shaping individual variation in behaviour and social structure. Here we show that androgen concentrations in wild female spotted hyaenas (Crocuta crocuta) are higher during late gestation in dominant females than in subordinate females. Furthermore, both male and female cubs born to mothers with high concentrations of androgens in late pregnancy exhibit higher rates of aggression and mounting behaviour than cubs born to mothers with lower androgen concentrations. Both behaviours are strongly affected in other mammals by organizational effects of androgens4, and both have important effects on fitness in hyaenas. Therefore, our results suggest that rank-related maternal effects of prenatal androgen exposure can adaptively influence offspring phenotype in mammals, as has previously been shown to occur in birds. They also suggest an organizational mechanism for the development of female dominance and aggressiveness in spotted hyaenas, traits that may offset the costs of extreme virilization.

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Figure 1: Maternal hormones during gestation in wild spotted hyaenas.
Figure 2: The relationship between faecal androgens and social rank in pregnant female spotted hyaenas during the second half of gestation.
Figure 3: Maternal androgens and cub behaviour.

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Acknowledgements

We thank the Office of the President of Kenya for permission to conduct field research. We also thank the Kenya Wildlife Service, the Narok County Council and the Senior Warden of the Masai Mara National Reserve for their cooperation. The following individuals provided assistance in the field: E. Boydston, M. Durham, A. Engh, L. G. Frank, P. Garrett, I. Graham, T. Harty, K. Kapheim, J. Kolowski, K. Nelson, G. Ording, L. Smale, M. Szykman, J. Tanner, K. Theis, R. Van Horn, S. Wahaj, H. Watts and K. Weibel. P. Bills and P. Van Meter provided technical assistance. This research was supported by NSF grants to K.E.H. and J.A.F., and fellowships from Michigan State University and the International Foundation for Ethical Research to S.M.D. Author Contributions Laboratory work, including development and validation of faecal hormone assays, was performed by S.M.D. and J.A.F. Field work was conducted by S.M.D. and K.E.H. The original idea for the study was conceived by K.E.H. S.M.D. conducted the statistical analyses and drafted the manuscript, which was further developed by all three authors.

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Correspondence to S. M. Dloniak.

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Dloniak, S., French, J. & Holekamp, K. Rank-related maternal effects of androgens on behaviour in wild spotted hyaenas. Nature 440, 1190–1193 (2006). https://doi.org/10.1038/nature04540

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