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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The data that support the findings of this study are included in the R package vullioud2018 available on GitHub (https://github.com/hyenaproject/vullioud2018).
Alonzo, S. H. Social and coevolutionary feedbacks between mating and parental investment. Trends Ecol. Evol. 25, 99–108 (2010).
Clutton-Brock, T. H. & Huchard, E. Social competition and selection in males and females. Phil. Trans. R. Soc. B 368, 20130074 (2013).
Ah-King, M. & Ahnesjö, I. The ‘sex role’ concept: an overview and evaluation. Evol. Biol. 40, 461–470 (2013).
Darwin, C. The Descent of Man, and Selection in Relation to Sex (Murray, London, 1871).
Andersson, M. B. Sexual Selection (Princeton Univ. Press, Princeton, 1994).
Clutton-Brock, T. H. Mammal Societies (John Wiley, Chichester, 2016).
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).
Hemelrijk, C. K., Wantia, J. & Isler, K. Female dominance over males in primates: self-organisation and sexual dimorphism. PLoS ONE 3, e2678 (2008).
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).
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).
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).
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).
Bissonnette, A. et al. Coalitions in theory and reality: a review of pertinent variables and processes. Behaviour 152, 1–56 (2015).
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).
Frank, L. G. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Anim. Behav. 151, 1510–1527 (1986).
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).
Gould, S. J. Hyena myths and realities. Nat. Hist. 90, 16–24 (1981).
Swanson, E. M. et al. Ontogeny of sexual size dimorphism in the spotted hyena (Crocuta crocuta). J. Mammal. 94, 1298–1310 (2013).
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).
Höner, O. P. et al. Female mate-choice drives the evolution of male-biased dispersal in a social mammal. Nature 448, 798–801 (2007).
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).
Smith, J. E. et al. Evolutionary forces favoring intragroup coalitions among spotted hyenas and other animals. Behav. Ecol. 21, 284–303 (2010).
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).
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).
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).
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).
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).
MacLeod, K. J. & Lukas, D. Revisiting non-offspring nursing: allonursing evolves when the costs are low. Biol. Lett. 10, 20140378 (2014).
Digby, L. in Infanticide by Males and its Implications (eds van Schaik, C. P. & Janson, C. H.) 423–446 (Cambridge Univ. Press, Cambridge, 2000).
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).
East, M. L. et al. Maternal effects on offspring social status in spotted hyenas. Behav. Ecol. 20, 478–483 (2009).
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).
Gowaty, P. A. & Hubbell, S. P. Reproductive decisions under ecological constraints: it’s about time. Proc. Natl Acad. Sci. USA 106, 10017–10024 (2009).
Lehtonen, J., Parker, G. A. & Schärer, L. Why anisogamy drives ancestral sex roles. Evolution 70, 1129–1135 (2016).
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).
Holekamp, K. E. & Smale, L. Dominance acquisition during mammalian social development: the ‘inheritance’ of maternal rank. Am. Zool. 31, 306–317 (1991).
Mills, M. G. L. Kalahari Hyenas: Comparative Behavioral Ecology of Two Species (Chapman & Hall, London, 1994).
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).
Kruuk, H. The Spotted Hyena: A Study of Predation and Social Behavior (Univ. Chicago Press, Chicago, 1972).
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).
Höner, O. P. et al. The fitness of dispersing spotted hyaena sons is influenced by maternal social status. Nat. Commun. 1, 60 (2010).
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).
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).
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).
Frank, L. G., Glickman, S. E. & Licht, P. Fatal sibling aggression, precocial development, and androgens in neonatal spotted hyenas. Science 252, 702–704 (1991).
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).
Wilhelm, K. et al. Characterization of spotted hyena, Crocuta crocuta microsatellite loci. Mol. Ecol. Notes 3, 360–362 (2003).
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).
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).
Kolowski, J. M. & Holekamp, K. E. Ecological and anthropogenic influences on space use by spotted hyaenas. J. Zool. 277, 23–36 (2009).
Ilany, A. & Akçay, E. Social inheritance can explain the structure of animal social networks. Nat. Commun. 7, 12084 (2016).
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).
Wood, S. N. Generalized Additive Models: An Introduction with R (CRC Press, Boca Raton, 2017).
Frank, L. G., Glickman, S. E. & Powch, I. Sexual dimorphism in the spotted hyaena (Crocuta crocuta). J. Zool. 221, 308–313 (1990).
R Development Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2018).
Rousset, F. & Ferdy, J.-B. Testing environmental and genetic effects in the presence of spatial autocorrelation. Ecography 37, 781–790 (2014).
Breslow, N. E. & Clayton, D. G. Approximate inference in generalized linear mixed models. J. Am. Stat. Assoc. 88, 9–25 (1993).
Agresti, A. & Coull, B. A. Approximate is better than ‘exact’ for interval estimation of binomial proportions. Am. Stat. 52, 119–126 (1998).
Wolff, J. O. & MacDonald, D. W. Promiscuous females protect their offspring. Trends Ecol. Evol. 19, 127–134 (2004).
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.
The authors declare no competing interests.
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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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