Ecology

Sexual coercion in a natural mandrill population

10.24072/pcjournal.134 - Peer Community Journal, Volume 2 (2022), article no. e36.

Get full text PDF Peer reviewed and recommended by PCI

Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of intimidation, where repeated male aggression promotes future rather than immediate mating success with targeted females. Although known in humans, intimidation was recently reported in chimpanzees (Pan troglodytes) and chacma baboons (Papio ursinus), where males are regularly violent against females. Here, we investigate the nature of male coercive strategies in wild mandrills (Mandrillus sphinx), a primate living in large polygynandrous groups where severe male aggression towards females is rare and females can form coalitions against males. Yet, we found support for all three predictions of the sexual coercion hypothesis, namely that male aggression (1) specifically targets sexually receptive females, (2) inflicts costs to these females, and (3) increases male mating success in the long-term. These results hold true when considering only non-physical threats, or only severe aggression. Finally, we show that high-ranking females are most targeted by males, probably because of their higher reproductive performances, while high-ranking males are most coercive. These results indicate that sexual intimidation is widespread in sexually dimorphic and group-living mammals, and that males and females vary in their propensities to use, and to be exposed to sexual coercion, respectively.

Published online:
DOI: 10.24072/pcjournal.134
Smit, Nikolaos 1; Baniel, Alice 2, 3; Roura-Torres, Berta 4, 5; Amblard-Rambert, Paul 6; Charpentier, Marie J. E. 1; Huchard, Elise 1

1 ISEM, UMR5554 - University of Montpellier/CNRS/IRD/EPHE, Place Eugène Bataillon (cc065), 34095 Montpellier, France
2 Center for Evolution and Medicine, Arizona State University, Tempe, AZ, 85281, USA
3 School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA
4 Behavioral Ecology & Sociobiology Unit, German Primate Center, Leibniz Institute for Primate Research, Kellnerweg 4, 37077 Gottingen, Germany
5 Department of Sociobiology/Anthropology, Johann-Friedrich-Blumenbach, Institute of Zoology and Anthropology, Georg-August University Gottingen, Kellnerweg 6, 37077 Gottingen, Germany
6 Projet Mandrillus, BP 52, Bakoumba, Gabon
@article{10_24072_pcjournal_134,
     author = {Smit, Nikolaos and Baniel, Alice and Roura-Torres, Berta and Amblard-Rambert, Paul and Charpentier, Marie J. E. and Huchard, Elise},
     title = {Sexual coercion in a natural mandrill population},
     journal = {Peer Community Journal},
     eid = {e36},
     publisher = {Peer Community In},
     volume = {2},
     year = {2022},
     doi = {10.24072/pcjournal.134},
     url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.134/}
}
TY  - JOUR
TI  - Sexual coercion in a natural mandrill population
JO  - Peer Community Journal
PY  - 2022
DA  - 2022///
VL  - 2
PB  - Peer Community In
UR  - https://peercommunityjournal.org/articles/10.24072/pcjournal.134/
UR  - https://doi.org/10.24072/pcjournal.134
DO  - 10.24072/pcjournal.134
ID  - 10_24072_pcjournal_134
ER  - 
%0 Journal Article
%T Sexual coercion in a natural mandrill population
%J Peer Community Journal
%D 2022
%V 2
%I Peer Community In
%U https://doi.org/10.24072/pcjournal.134
%R 10.24072/pcjournal.134
%F 10_24072_pcjournal_134
Smit, Nikolaos; Baniel, Alice; Roura-Torres, Berta; Amblard-Rambert, Paul; Charpentier, Marie J. E.; Huchard, Elise. Sexual coercion in a natural mandrill population. Peer Community Journal, Volume 2 (2022), article  no. e36. doi : 10.24072/pcjournal.134. https://peercommunityjournal.org/articles/10.24072/pcjournal.134/

Peer reviewed and recommended by PCI : 10.24072/pci.ecology.100099

[1] Arnqvist, G. Multiple mating in a water strider: mutual benefits or intersexual conflict?, Animal Behaviour, Volume 38 (1989) no. 5, pp. 749-756 | Article

[2] Baniel, A.; Cowlishaw, G.; Huchard, E. Male Violence and Sexual Intimidation in a Wild Primate Society, Current Biology, Volume 27 (2017) no. 14 | Article

[3] Altmann, J. Observational Study of Behavior: Sampling Methods, Behaviour, Volume 49 (1974) no. 3-4, pp. 227-266 | Article

[4] Baniel, A.; Webb, C. E.; Cowlishaw, G.; Huchard, E. The submissive pattern of postconflict affiliation in asymmetric relationships: a test in male and sexually coerced female baboons, Animal Behaviour, Volume 175 (2021), pp. 87-97 | Article

[5] Basile, K. C. Prevalence of Wife Rape and Other Intimate Partner Sexual Coercion in a Nationally Representative Sample of Women, Violence and Victims, Volume 17 (2002) no. 5, pp. 511-524 | Article

[6] Bateman, A. J. Intra-sexual selection in Drosophila, Heredity, Volume 2 (1948) no. 3, pp. 349-368 | Article

[7] Bates, D.; Mächler, M.; Bolker, B.; Walker, S. Fitting Linear Mixed-Effects Models Using<b>lme4</b>, Journal of Statistical Software, Volume 67 (2015) no. 1 | Article

[8] Boeuf Burney J. Le , ; Mesnick, S. Sexual Behavior of Male Northern Elephant Seals: I. Lethal Injuries To Adult Females, Behaviour, Volume 116 (1991) no. 1-2, pp. 143-162 | Article

[9] Bro-Jørgensen, J. Intra- and Intersexual Conflicts and Cooperation in the Evolution of Mating Strategies: Lessons Learnt From Ungulates, Evolutionary Biology, Volume 38 (2010) no. 1, pp. 28-41 | Article

[10] Brockmeyer, T.; Kappeler, P. M.; Willaume, E.; Benoit, L.; Mboumba, S.; Charpentier, M. J. Social organization and space use of a wild mandrill (<i>Mandrillus sphinx</i>) group, American Journal of Primatology, Volume 77 (2015) no. 10, pp. 1036-1048 | Article

[11] Brooks Mollie E. et al., glmmTMB Balances Speed and Flexibility among Packages for Zero- Inflated Generalized Linear Mixed Modeling, The R Journal, Volume 9 (2017), pp. 378-400

[12] Cassini, M. A model on female breeding dispersion and the reproductive systems of pinnipeds, Behavioural Processes, Volume 51 (2000) no. 1-3, pp. 93-99 | Article

[13] Cassini, M. H. A mixed model of the evolution of polygyny and sexual size dimorphism in mammals, Mammal Review, Volume 50 (2019) no. 1, pp. 112-120 | Article

[14] Cassini, M. H. Sexual aggression in mammals, Mammal Review, Volume 51 (2021) no. 2, pp. 247-255 | Article

[15] Charpentier, M. J. E.; Givalois, L.; Faurie, C.; Soghessa, O.; Simon, F.; Kappeler, P. M. Seasonal glucocorticoid production correlates with a suite of small-magnitude environmental, demographic, and physiological effects in mandrills, American Journal of Physical Anthropology, Volume 165 (2018) no. 1, pp. 20-33 | Article

[16] Charpentier, M. J. E.; Harté, M.; Poirotte, C.; de Bellefon, J. M.; Laubi, B.; Kappeler, P. M.; Renoult, J. P. Same father, same face: Deep learning reveals selection for signaling kinship in a wild primate, Science Advances, Volume 6 (2020) no. 22 | Article

[17] Charpentier, M.; Peignot, P.; Hossaert-McKey, M.; Gimenez, O.; Setchell, J. M.; Wickings, E. J. Constraints on control: factors influencing reproductive success in male mandrills (Mandrillus sphinx), Behavioral Ecology, Volume 16 (2005) no. 3, pp. 614-623 | Article

[18] Chung, Y.; Rabe-Hesketh, S.; Dorie, V.; Gelman, A.; Liu, J. A Nondegenerate Penalized Likelihood Estimator for Variance Parameters in Multilevel Models, Psychometrika, Volume 78 (2013) no. 4, pp. 685-709 | Article

[19] Clutton-Brock, T. H.; Parker, G. A. Punishment in animal societies, Nature, Volume 373 (1995) no. 6511, pp. 209-216 | Article

[20] Clutton-Brock, T.; Parker, G. Sexual coercion in animal societies, Animal Behaviour, Volume 49 (1995) no. 5, pp. 1345-1365 | Article

[21] Clutton-Brock, T. Social evolution in mammals, Science, Volume 373 (2021) no. 6561 | Article

[22] Connor, R. C.; Vollmer, N. 9 Sexual Coercion in Dolphin Consortships: A Comparison with Chimpanzees, Sexual Coercion in Primates and Humans, Harvard University Press, 2009, pp. 218-243 | Article

[23] Cordero, C.; Eberhard, W. G. Female choice of sexually antagonistic male adaptations: a critical review of some current research, Journal of Evolutionary Biology, Volume 16 (2003) no. 1, pp. 1-6 | Article

[24] David, H. A. Ranking from unbalanced paired-comparison data, Biometrika, Volume 74 (1987) no. 2, pp. 432-436 | Article

[25] Dezeure, J.; Charpentier, M. J.; Huchard, E. Fitness effects of seasonal birth timing in a long-lived social primate living in the equatorial forest, Animal Behaviour, Volume 185 (2022), pp. 113-126 | Article

[26] Dibakou, S. E.; Basset, D.; Souza, A.; Charpentier, M.; Huchard, E. Determinants of Variations in Fecal Neopterin in Free-Ranging Mandrills, Frontiers in Ecology and Evolution, Volume 7 (2019) | Article

[27] Eberle, M.; Kappeler, P. M. Selected polyandry: female choice and inter-sexual conflict in a small nocturnal solitary primate (Microcebus murinus), Behavioral Ecology and Sociobiology, Volume 57 (2004) no. 1, pp. 91-100 | Article

[28] Fisher, R. The evolution of sexual preferenc, The Eugenic Review, Volume 7 (1915), pp. 184-192

[29] Fox, J.; Weisberg, S. An R companion to Applied Regression. Third., Sage, Thousand Oaks CA, 2019

[30] Fürtbauer, I.; Mundry, R.; Heistermann, M.; Schülke, O.; Ostner, J. You Mate, I Mate: Macaque Females Synchronize Sex not Cycles, PLoS ONE, Volume 6 (2011) no. 10 | Article

[31] Galbany, J.; Romero, A.; Mayo-Alesón, M.; Itsoma, F.; Gamarra, B.; Pérez-Pérez, A.; Willaume, E.; Kappeler, P. M.; Charpentier, M. J. E. Age-Related Tooth Wear Differs between Forest and Savanna Primates, PLoS ONE, Volume 9 (2014) no. 4 | Article

[32] Galdikas, B. M. F. Subadult male orangutan sociality and reproductive behavior at Tanjung Puting, American Journal of Primatology, Volume 8 (1985) no. 2, pp. 87-99 | Article

[33] Head, M. L.; Brooks, R. Sexual coercion and the opportunity for sexual selection in guppies, Animal Behaviour, Volume 71 (2006) no. 3, pp. 515-522 | Article

[34] Huchard, E.; Canale, C. I.; Le Gros, C.; Perret, M.; Henry, P.-Y.; Kappeler, P. M. Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1732, pp. 1371-1379 | Article

[35] Huk, T.; Winkel, W. Testing the sexy son hypothesis--a research framework for empirical approaches, Behavioral Ecology, Volume 19 (2007) no. 2, pp. 456-461 | Article

[36] Ims, R. A. The ecology and evolution of reproductive synchrony, Trends in Ecology &amp; Evolution, Volume 5 (1990) no. 5, pp. 135-140 | Article

[37] Kaburu, S. S. K.; Newton-Fisher, N. E. Trading or coercion? Variation in male mating strategies between two communities of East African chimpanzees, Behavioral Ecology and Sociobiology, Volume 69 (2015) no. 6, pp. 1039-1052 | Article

[38] Keddy-Hector, A. C. Mate Choice in Non-Human Primates, American Zoologist, Volume 32 (1992) no. 1, pp. 62-70 | Article

[39] King, S. L.; Allen, S. J.; Krützen, M.; Connor, R. C. Vocal behaviour of allied male dolphins during cooperative mate guarding, Animal Cognition, Volume 22 (2019) no. 6, pp. 991-1000 | Article

[40] Kunz, J. A.; Duvot, G. J.; Willems, E. P.; Stickelberger, J.; Spillmann, B.; Utami Atmoko, S. S.; van Noordwijk, M. A.; van Schaik, C. P. The context of sexual coercion in orang-utans: when do male and female mating interests collide?, Animal Behaviour, Volume 182 (2021), pp. 67-90 | Article

[41] Leigh, S. R.; Setchell, J. M.; Charpentier, M.; Knapp, L. A.; Wickings, E. J. Canine tooth size and fitness in male mandrills (Mandrillus sphinx), Journal of Human Evolution, Volume 55 (2008) no. 1, pp. 75-85 | Article

[42] McKinney, F.; Evarts, S. Sexual Coercion in Waterfowl and Other Birds, Ornithological Monographs (1998) no. 49, pp. 163-195 | Article

[43] Muller, M. N.; Kahlenberg, S. M.; Emery Thompson, M.; Wrangham, R. W. Male coercion and the costs of promiscuous mating for female chimpanzees, Proceedings of the Royal Society B: Biological Sciences, Volume 274 (2007) no. 1612, pp. 1009-1014 | Article

[44] Muller, M. N.; Thompson, M. E.; Kahlenberg, S. M.; Wrangham, R. W. Sexual coercion by male chimpanzees shows that female choice may be more apparent than real, Behavioral Ecology and Sociobiology, Volume 65 (2011) no. 5, pp. 921-933 | Article

[45] Muller, M. N.; Thompson, M. E.; Wrangham, R. W. Male Chimpanzees Prefer Mating with Old Females, Current Biology, Volume 16 (2006) no. 22, pp. 2234-2238 | Article

[46] Nunn, C. L.; van Schaik, C. P. Social evolution in primates: the relative roles of ecology and intersexual conflict, Infanticide by Males and its Implications, Cambridge University Press, 2000, pp. 388-420 | Article

[47] Ostner, J.; Nunn, C. L.; Schülke, O. Female reproductive synchrony predicts skewed paternity across primates, Behavioral Ecology, Volume 19 (2008) no. 6, pp. 1150-1158 | Article

[48] Paoli Tommaso, 16 The Absence of Sexual Coercion in Bonobos, Sexual Coercion in Primates and Humans, Harvard University Press, 2009, pp. 410-423 | Article

[49] Parker, G. Sexual selection and sexual conflict, Sexual Selection and Reproductive Competition in Insects, Elsevier, 1979, pp. 123-166 | Article

[50] Peignot, P.; Charpentier, M. J.; Bout, N.; Bourry, O.; Massima, U.; Dosimont, O.; Terramorsi, R.; Wickings, E. J. Learning from the first release project of captive-bred mandrills Mandrillus sphinx in Gabon, Oryx, Volume 42 (2008) no. 01 | Article

[51] Pinheiro, J. B. D. Mixed-Effects Models in S and S-PLUS, Statistics and Computing, 2006 | Article

[52] Pizzari, T.; Snook, R. R. Perspective: sexual conflict and sexual selection: chasing away paradigm shifts, Evolution, Volume 57 (2003) no. 6, pp. 1223-1236 | Article

[53] Podgórski, T.; Lusseau, D.; Scandura, M.; Sönnichsen, L.; Jędrzejewska, B. Long-Lasting, Kin-Directed Female Interactions in a Spatially Structured Wild Boar Social Network, PLoS ONE, Volume 9 (2014) no. 6 | Article

[54] Poirotte, C.; Massol, F.; Herbert, A.; Willaume, E.; Bomo, P. M.; Kappeler, P. M.; Charpentier, M. J. E. Mandrills use olfaction to socially avoid parasitized conspecifics, Science Advances, Volume 3 (2017) no. 4 | Article

[55] Pusey, A.; Williams, J.; Goodall, J. The Influence of Dominance Rank on the Reproductive Success of Female Chimpanzees, Science, Volume 277 (1997) no. 5327, pp. 828-831 | Article

[56] Reddy, R. B.; Mitani, J. C. Adolescent and young adult male chimpanzees form affiliative, yet aggressive, relationships with females, Journal of Human Evolution, Volume 144 (2020) | Article

[57] Rodseth, L. N. S. A. 12 The Political Significance of Gender Violence, Sexual Coercion in Primates and Humans, Harvard University Press, 2009, pp. 292-321 | Article

[58] Réale, D.; Boussès, P.; Chapuis, J.-L. Female-biased mortality induced by male sexual harassment in a feral sheep population, Canadian Journal of Zoology, Volume 74 (1996) no. 10, pp. 1812-1818 | Article

[59] Setchell, J. M. Do Female Mandrills Prefer Brightly Colored Males?, International Journal of Primatology, Volume 26 (2005) no. 4, pp. 715-735 | Article

[60] Setchell, J. M. Sexual Selection and the differences between the sexes in Mandrills (<i>M</i><i>andrillus sphinx</i>), American Journal of Physical Anthropology, Volume 159 (2016), pp. 105-129 | Article

[61] Setchell, J. M.; Charpentier, M.; Wickings, E. J. Mate guarding and paternity in mandrills: factors influencing alpha male monopoly, Animal Behaviour, Volume 70 (2005) no. 5, pp. 1105-1120 | Article

[62] Setchell, J. M.; Charpentier, M.; Wickings, E. J. Sexual selection and reproductive careers in mandrills (Mandrillus sphinx), Behavioral Ecology and Sociobiology, Volume 58 (2005) no. 5, pp. 474-485 | Article

[63] Setchell, J. M.; Dixson, A. F. Developmental variables and dominance rank in adolescent male mandrills (Mandrillus sphinx), American Journal of Primatology, Volume 56 (2002) no. 1, pp. 9-25 | Article

[64] Setchell, J. M.; Jean Wickings, E. Dominance, Status Signals and Coloration in Male Mandrills (Mandrillus sphinx), Ethology, Volume 111 (2005) no. 1, pp. 25-50 | Article

[65] Setchell, J. M.; Knapp, L. A.; Wickings, E. J. Violent coalitionary attack by female mandrills against an injured alpha male, American Journal of Primatology, Volume 68 (2006) no. 4, pp. 411-418 | Article

[66] Setchell, J. M.; Lee, P. C.; Wickings, E. J.; Dixson, A. F. Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx), American Journal of Physical Anthropology, Volume 115 (2001) no. 4, pp. 349-360 | Article

[67] Setchell, J. M.; Lee, P. C.; Wickings, E. J.; Dixson, A. F. International Journal of Primatology, 23 (2002) no. 1, pp. 51-68 | Article

[68] Smit, N. Sexual Coercion in a Natural Mandrill Population [Data Set]. Zenodo. https: //doi.org/10.5281/zenodo.6607803, 2022

[69] Smit, N.; Baniel, A.; Roura-Torres, B.; Amblard-Rambert, P.; Charpentier, M. J. E.; Huchard, E. bioRxiv, 2022.02.07.479393. https://doi.org/10.1101/2022.02.07.479393, 2022

[70] Smuts, B. Male aggression against women, Human Nature, Volume 3 (1992) no. 1, pp. 1-44 | Article

[71] Smuts, B. The evolutionary origins of patriarchy, Human Nature, Volume 6 (1995) no. 1, pp. 1-32 | Article

[72] Smuts, B. B.; Smuts, R. w. Male Aggression and Sexual Coercion of Females in Nonhuman Primates and Other Mammals: Evidence and Theoretical Implications, Advances in the Study of Behavior, Elsevier, 1993, pp. 1-63 | Article

[73] Snyder-Mackler, N.; Alberts, S. C.; Bergman, T. J. Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups, Proceedings of the Royal Society B: Biological Sciences, Volume 279 (2012) no. 1743, pp. 3788-3795 | Article

[74] Stumpf, R. M.; Boesch, C. The efficacy of female choice in chimpanzees of the Taï Forest, Côte d’Ivoire, Behavioral Ecology and Sociobiology, Volume 60 (2006) no. 6, pp. 749-765 | Article

[75] Stumpf, R. M.; Martinez-Mota, R.; Milich, K. M.; Righini, N.; Shattuck, M. R. Sexual conflict in primates, Evolutionary Anthropology: Issues, News, and Reviews, Volume 20 (2011) no. 2, pp. 62-75 | Article

[76] Swedell, L.; Schreier, A. 10 Male Aggression toward Females in Hamadryas Baboons: Conditioning, Coercion, and Control, Sexual Coercion in Primates and Humans, Harvard University Press, 2009, pp. 244-268 | Article

[77] Szykman, M.; Engh, A.; Van Horn, R.; Funk, S.; Scribner, K.; Holekamp, K. Association patterns among male and female spotted hyenas ( Crocuta crocuta ) reflect male mate choice, Behavioral Ecology and Sociobiology, Volume 50 (2001) no. 3, pp. 231-238 | Article

[78] Szykman, M.; Engh, A. L.; Van Horn, R. C.; Boydston, E. E.; Scribner, K. T.; Holekamp, K. E. Rare male aggression directed toward females in a female-dominated society: Baiting behavior in the spotted hyena, Aggressive Behavior, Volume 29 (2003) no. 5, pp. 457-474 | Article

[79] Thornhill, R.; Alcock, J.; et al. , The Evolution of Insect Mating Systems, Harvard University Press, 1983

[80] Valera, F. Male shrikes punish unfaithful females, Behavioral Ecology, Volume 14 (2003) no. 3, pp. 403-408 | Article

[81] Wallen, M. M.; Patterson, E. M.; Krzyszczyk, E.; Mann, J. The ecological costs to females in a system with allied sexual coercion, Animal Behaviour, Volume 115 (2016), pp. 227-236 | Article

[82] Watts, D. P. Male chimpanzee sexual coercion and mating success at Ngogo, American Journal of Primatology, Volume 84 (2022) no. 2 | Article

[83] Zuur, A. F.; Ieno, E. N.; Elphick, C. S. A protocol for data exploration to avoid common statistical problems, Methods in Ecology and Evolution, Volume 1 (2010) no. 1, pp. 3-14 | Article

[84] le Roux, A.; Snyder-Mackler, N.; Roberts, E. K.; Beehner, J. C.; Bergman, T. J. Evidence for tactical concealment in a wild primate, Nature Communications, Volume 4 (2013) no. 1 | Article

Cited by Sources: