Social support drives female dominance in the spotted hyaena

Abstract

Identifying how dominance within and between the sexes is established is pivotal to understanding sexual selection and sexual conflict. In many species, members of one sex dominate those of the other in one-on-one interactions. Whether this results from a disparity in intrinsic attributes, such as strength and aggressiveness, or in extrinsic factors, such as social support, is currently unknown. We assessed the effects of both mechanisms on dominance in the spotted hyaena (Crocuta crocuta), a species where sexual size dimorphism is low and females often dominate males. We found that individuals with greater potential social support dominated one-on-one interactions in all social contexts, irrespective of their body mass and sex. Female dominance emerged from a disparity in social support in favour of females. This disparity was a direct consequence of male-biased dispersal and the disruptive effect of dispersal on social bonds. Accordingly, the degree of female dominance varied with the demographic and kin structure of the social groups, ranging from male and female co-dominance to complete female dominance. Our study shows that social support can drive sex-biased dominance and provides empirical evidence that a sex-role-defining trait can emerge without the direct effect of sex.

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Fig. 1: The effect of social support, body mass and sex on the probability that a spotted hyaena wins a dyadic interaction.
Fig. 2: The effect of dispersal and age on the cumulative relatedness of spotted hyaenas.
Fig. 3: The emergence of female dominance in spotted hyaenas and other social species.

Data availability

The data that support the findings of this study are included in the R package vullioud2018 available on GitHub (https://github.com/hyenaproject/vullioud2018).

References

  1. 1.

    Alonzo, S. H. Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol. Evol. 25, 99–108 (2010).

    Article  Google Scholar 

  2. 2.

    Clutton-Brock, T. H. & Huchard, E. Social competition and selection in males and females. Phil. Trans. R. Soc. B 368, 20130074 (2013).

    CAS  Article  Google Scholar 

  3. 3.

    Ah-King, M. & Ahnesjö, I. The ‘sex role’ concept: an overview and evaluation. Evol. Biol. 40, 461–470 (2013).

    Article  Google Scholar 

  4. 4.

    Darwin, C. The Descent of Man, and Selection in Relation to Sex (Murray, London, 1871).

  5. 5.

    Andersson, M. B. Sexual Selection (Princeton Univ. Press, Princeton, 1994).

    Google Scholar 

  6. 6.

    Clutton-Brock, T. H. Mammal Societies (John Wiley, Chichester, 2016).

  7. 7.

    von Engelhardt, N., Kappeler, P. M. & Heistermann, M. Androgen levels and female social dominance in Lemur catta. Proc. R. Soc. B 267, 1533–1539 (2000).

    CAS  Article  Google Scholar 

  8. 8.

    Hemelrijk, C. K., Wantia, J. & Isler, K. Female dominance over males in primates: self-organisation and sexual dimorphism. PLoS ONE 3, e2678 (2008).

    Article  Google Scholar 

  9. 9.

    Surbeck, M. & Hohmann, G. Intersexual dominance relationships and the influence of leverage on the outcome of conflicts in wild bonobos (Pan paniscus). Behav. Ecol. Sociobiol. 67, 1767–1780 (2013).

    Article  Google Scholar 

  10. 10.

    Chase, I. D., Tovey, C., Spangler-Martin, D. & Manfredonia, M. Individual differences versus social dynamics in the formation of animal dominance hierarchies. Proc. Natl Acad. Sci. USA 99, 5744–5749 (2002).

    CAS  Article  Google Scholar 

  11. 11.

    Stroebe, K., Nijstad, B. A. & Hemelrijk, C. K. Female dominance in human groups: effects of sex ratio and conflict level. Soc. Psychol. Personal. Sci. 8, 209–218 (2017).

    Article  Google Scholar 

  12. 12.

    Markham, C., Lonsdorf, E. V., Pusey, A. E. & Murray, C. M. Maternal rank influences the outcome of aggressive interactions between immature chimpanzees. Anim. Behav. 100, 192–198 (2015).

    Article  Google Scholar 

  13. 13.

    Bissonnette, A. et al. Coalitions in theory and reality: a review of pertinent variables and processes. Behaviour 152, 1–56 (2015).

    Article  Google Scholar 

  14. 14.

    Weiß, B. M. & Kotrschal, K. Effects of passive social support in juvenile greylag geese (Anser anser): a study from fledging to adulthood. Ethology 110, 429–444 (2004).

    Article  Google Scholar 

  15. 15.

    Frank, L. G. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Anim. Behav. 151, 1510–1527 (1986).

    Article  Google Scholar 

  16. 16.

    Watts, H. E., Tanner, J. B., Lundrigan, B. L. & Holekamp, K. E. Post-weaning maternal effects and the evolution of female dominance in the spotted hyena. Proc. R. Soc. B 276, 2291–2298 (2009).

    Article  Google Scholar 

  17. 17.

    Gould, S. J. Hyena myths and realities. Nat. Hist. 90, 16–24 (1981).

    Google Scholar 

  18. 18.

    Swanson, E. M. et al. Ontogeny of sexual size dimorphism in the spotted hyena (Crocuta crocuta). J. Mammal. 94, 1298–1310 (2013).

    Article  Google Scholar 

  19. 19.

    Smale, L., Frank, L. G. & Holekamp, K. E. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Anim. Behav. 46, 467–477 (1993).

    Article  Google Scholar 

  20. 20.

    Höner, O. P. et al. Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448, 798–801 (2007).

    Article  Google Scholar 

  21. 21.

    Davidian, E., Courtiol, A., Wachter, B., Hofer, H. & Höner, O. P. Why do some males choose to breed at home when most other males disperse?. Sci. Adv. 2, e1501236 (2016).

    Article  Google Scholar 

  22. 22.

    Smith, J. E. et al. Evolutionary forces favoring intragroup coalitions among spotted hyenas and other animals. Behav. Ecol. 21, 284–303 (2010).

    Article  Google Scholar 

  23. 23.

    East, M. L., Hofer, H. & Wickler, W. The erect ‘penis’ is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav. Ecol. Sociobiol. 33, 355–370 (1993).

    Article  Google Scholar 

  24. 24.

    Clobert, J., Le Galliard, J.-F., Cote, J., Meylan, S. & Massot, M. Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol. Lett. 12, 197–209 (2009).

    Article  Google Scholar 

  25. 25.

    Bissonnette, A., de Vries, H. & van Schaik, C. P. Coalitions in male Barbary macaques, Macaca sylvanus: strength, success and rules of thumb. Anim. Behav. 78, 329–335 (2009).

    Article  Google Scholar 

  26. 26.

    Sánchez-Tójar, A., Schroeder, J. & Farine, D. R. A practical guide for inferring reliable dominance hierarchies and estimating their uncertainty. J. Anim. Ecol. 87, 594–608 (2018).

    Article  Google Scholar 

  27. 27.

    Hofer, H. & East, M. L. Behavioral processes and costs of co-existence in female spotted hyenas: a life history perspective. Evol. Ecol. 17, 315–331 (2003).

    Article  Google Scholar 

  28. 28.

    MacLeod, K. J. & Lukas, D. Revisiting non-offspring nursing: allonursing evolves when the costs are low. Biol. Lett. 10, 20140378 (2014).

    Article  Google Scholar 

  29. 29.

    Digby, L. in Infanticide by Males and its Implications (eds van Schaik, C. P. & Janson, C. H.) 423–446 (Cambridge Univ. Press, Cambridge, 2000).

  30. 30.

    Hofer, H. & East, M. L. in Serengeti II: Dynamics, Management, and Conservation of an Ecosystem (eds Sinclair, A. R. E. & Arcese, P.) 332–363 (Univ. Chicago Press, Chicago, 1995).

  31. 31.

    East, M. L. et al. Maternal effects on offspring social status in spotted hyenas. Behav. Ecol. 20, 478–483 (2009).

    Article  Google Scholar 

  32. 32.

    Lukas, D. & Huchard, E. The evolution of infanticide by females in mammals. Preprint at https://www.biorxiv.org/content/early/2018/09/03/405688 (2018).

  33. 33.

    Gowaty, P. A. & Hubbell, S. P. Reproductive decisions under ecological constraints: it’s about time. Proc. Natl Acad. Sci. USA 106, 10017–10024 (2009).

    Article  Google Scholar 

  34. 34.

    Lehtonen, J., Parker, G. A. & Schärer, L. Why anisogamy drives ancestral sex roles. Evolution 70, 1129–1135 (2016).

    Article  Google Scholar 

  35. 35.

    Kappeler, P. M. Sex roles and adult sex ratios: insights from mammalian biology and consequences for primate behaviour. Phil. Trans. R. Soc. B 372, 20160321 (2017).

    Article  Google Scholar 

  36. 36.

    Holekamp, K. E. & Smale, L. Dominance acquisition during mammalian social development: the ‘inheritance’ of maternal rank. Am. Zool. 31, 306–317 (1991).

    Article  Google Scholar 

  37. 37.

    Mills, M. G. L. Kalahari Hyenas: Comparative Behavioral Ecology of Two Species (Chapman & Hall, London, 1994).

    Google Scholar 

  38. 38.

    East, M. L. & Hofer, H. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav. Ecol. 12, 558–568 (2001).

    Article  Google Scholar 

  39. 39.

    Kruuk, H. The Spotted Hyena: A Study of Predation and Social Behavior (Univ. Chicago Press, Chicago, 1972).

  40. 40.

    Hofer, H. & East, M. L. The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and commuters’ space use. Anim. Behav. 46, 559–574 (1993).

    Article  Google Scholar 

  41. 41.

    Höner, O. P. et al. The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nat. Commun. 1, 60 (2010).

    Article  Google Scholar 

  42. 42.

    East, M. L. & Hofer, H. Loud-calling in a female-dominated mammalian society: II. Behavioural contexts and functions of whooping of spotted hyaenas, Crocuta crocuta. Anim. Behav. 42, 651–669 (1991).

    Article  Google Scholar 

  43. 43.

    Holekamp, K. E. & Smale, L. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Anim. Behav. 46, 451–466 (1993).

    Article  Google Scholar 

  44. 44.

    Benhaiem, S., Hofer, H., Kramer-Schadt, S., Brunner, E. & East, M. L. Sibling rivalry: training effects, emergence of dominance and incomplete control. Proc. R. Soc. B 279, 3727–3735 (2012).

    Article  Google Scholar 

  45. 45.

    Frank, L. G., Glickman, S. E. & Licht, P. Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science 252, 702–704 (1991).

    CAS  Article  Google Scholar 

  46. 46.

    Smale, L., Holekamp, K. E., Weldele, M., Frank, L. G. & Glickman, S. E. Competition and cooperation between litter-mates in the spotted hyaena, Crocuta crocuta. Anim. Behav. 50, 671–682 (1995).

    Article  Google Scholar 

  47. 47.

    Wilhelm, K. et al. Characterization of spotted hyena, Crocuta crocuta microsatellite loci. Mol. Ecol. Notes 3, 360–362 (2003).

    CAS  Article  Google Scholar 

  48. 48.

    Kalinowski, S. T., Taper, M. L. & Marshall, T. C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 16, 1099–1106 (2007).

    Article  Google Scholar 

  49. 49.

    Trinkel, M., Fleischmann, P. H. & Kastberger, G. Comparison of land-use strategies of spotted hyenas (Crocuta crocuta, Erxleben) in different ecosystems. Afr. J. Ecol. 44, 537–539 (2006).

    Article  Google Scholar 

  50. 50.

    Kolowski, J. M. & Holekamp, K. E. Ecological and anthropogenic influences on space use by spotted hyaenas. J. Zool. 277, 23–36 (2009).

    Article  Google Scholar 

  51. 51.

    Ilany, A. & Akçay, E. Social inheritance can explain the structure of animal social networks. Nat. Commun. 7, 12084 (2016).

    CAS  Article  Google Scholar 

  52. 52.

    Wachter, B., Höner, O. P., East, M. L., Golla, W. & Hofer, H. Low aggression levels and unbiased sex ratios in a prey-rich environment: no evidence of siblicide in Ngorongoro spotted hyenas (Crocuta crocuta). Behav. Ecol. Sociobiol. 52, 348–356 (2002).

    Article  Google Scholar 

  53. 53.

    Wood, S. N. Generalized Additive Models: An Introduction with R (CRC Press, Boca Raton, 2017).

    Google Scholar 

  54. 54.

    Frank, L. G., Glickman, S. E. & Powch, I. Sexual dimorphism in the spotted hyaena (Crocuta crocuta). J. Zool. 221, 308–313 (1990).

    Article  Google Scholar 

  55. 55.

    R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).

  56. 56.

    Rousset, F. & Ferdy, J.-B. Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography 37, 781–790 (2014).

    Article  Google Scholar 

  57. 57.

    Breslow, N. E. & Clayton, D. G. Approximate inference in generalized linear mixed models. J. Am. Stat. Assoc. 88, 9–25 (1993).

    Google Scholar 

  58. 58.

    Agresti, A. & Coull, B. A. Approximate is better than ‘exact’ for interval estimation of binomial proportions. Am. Stat. 52, 119–126 (1998).

    Google Scholar 

  59. 59.

    Wolff, J. O. & MacDonald, D. W. Promiscuous females protect their offspring. Trends Ecol. Evol. 19, 127–134 (2004).

    Article  Google Scholar 

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Acknowledgements

We thank the Tanzania Commission for Science and Technology for permission to conduct the study, the Tanzania Wildlife Research Institute, Ngorongoro Conservation Area Authority, D. Thierer, S. Karl, M. Szameitat and P. Naman for their assistance and E. Huchard, M. Franz, O. Judson and P. Vullioud for helpful comments. The study was financed by the Leibniz Institute for Zoo and Wildlife Research, the Werner Dessauer Stiftung, the Stiftung Naturschutz and private donors.

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Conceptualization: O.P.H., A.C. and E.D. Methodology: A.C., C.V., F.R. and O.P.H. Software: C.V., A.C. and F.R. Formal analysis: C.V., A.C. and F.R. Investigation: O.P.H., E.D. and B.W. Resources: O.P.H. Data curation: O.P.H., C.V. and A.C. Writing of original draft: O.P.H., E.D., A.C. and C.V. Review and editing of draft: O.P.H., E.D, A.C., C.V., B.W. and F.R. Supervision: O.P.H. and A.C. Project administration: O.P.H. Funding acquisition: O.P.H.

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Correspondence to Oliver P. Höner.

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Vullioud, C., Davidian, E., Wachter, B. et al. Social support drives female dominance in the spotted hyaena. Nat Ecol Evol 3, 71–76 (2019). https://doi.org/10.1038/s41559-018-0718-9

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