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Intersexual relationships in mandrills: dominance, sexual conflict and the influence of social integration

Relations intersexuelles chez les mandrills : dominance, conflit sexuel et influence de l’intégration sociale
Nikolaos Smit

Abstracts

The conflict of evolutionary interests between the sexes is commonly imprinted in social dynamics and physical asymmetries between the sexes. In species that live in polygynandrous groups, male-biased sexual size dimorphism often allows males to socially dominate and sexually coerce females. Yet, smaller female size might allow females to escape from males and female philopatry might promote female-female social support allowing females to resist or retaliate against males. The study of such intersexual conflicts is highly relevant in mandrills (Mandrillus sphinx) as they form large polygynandrous groups and exhibit extreme male-biased sexual dimorphism in size and ornaments, higher social integration of females than males, and female coalitions against males. The set up of Mandrillus Project over a decade ago has offered a unique opportunity to study intersexual relationships of mandrills in their natural habitat. Here, I present a synthesis of some recent studies that used the long-term behavioural and life-history dataset of Mandrillus Project and documented patterns of sexual coercion and intersexual dominance in mandrills. These studies show that male mandrills are generally dominant over females and use sexual coercion to increase their mating success. However, female social bonds and social integration permit females to occasionally outrank certain males. Finally, and surprisingly, higher-ranking and more socially integrated females receive higher rates of male sexual coercion, highlighting the need for future research to shed light on the trade-offs between costs and benefits of mandrill sociality.

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Editor’s notes

Received 13/03/24, accepted 19/06/2024, published online 18/07/2024.

The 2022 Thesis Award of the Société Francophone De Primatologie (SFDP) was awarded to Nikolaos Smit for his presentation entitled "Dynamics in intersexual dominance in a highly dimorphic primate" at the 34th SFDP conference held in Aix-en-Provence. This award is given annually to a young researcher who has distinguished himself/herself through his/her doctoral work in a field related to primatology.

Reçu le 13/03/24, accepté le 19/06/2024, publié le 18/07/2024.

Le prix de thèse de la Société Francophone De Primatologie (SFDP) 2022 a été décerné à Nikolaos Smit pour sa présentation intitulée « Dynamics in intersexual dominance in a highly dimorphic primate » lors du 34ème colloque de la SFDP qui s’est tenu à Aix-en-Provence. Ce prix est attribué chaque année à une jeune chercheuse, ou à un jeune chercheur, qui s’est distingué par son travail de doctorat dans un domaine en lien avec la primatologie.

Full text

1 Mandrills

1Mandrills (Mandrillus sphinx) are primates of the Cercopithecidae family that live in equatorial forests of Africa (Abernethy et al., 2002). They form polygynandrous groups that are structured around matrilines of philopatric females (Brockmeyer et al., 2015) and can contain several hundreds of individuals (Abernethy et al., 2002). The highest-ranking (alpha) male sires 60-70% of infants (Charpentier et al., 2005; 2020) and, similarly to other high-ranking males, mate-guards females when those exhibit perineal sexual swellings around ovulation (Setchell et al., 2005).

2Male-biased sexual size dimorphism is extreme in mandrills: males are on average 3.4 times heavier than females (Setchell et al., 2001) and exhibit brighter facial and hindquarter ornaments (Figure 1; Setchell & Wickings, 2005). Previous studies have suggested that female mandrills might exert mate choice based on male ornaments (Setchell, 2005; 2016) rather than male armaments which can be used against females during sexual conflict (Pradhan & van Schaik, 2009). Despite the extreme physical superiority of males, female mandrills are occasionally observed to form coalitions and retaliate against male approaches or aggression (personal observation; Setchell et al., 2006), highlighting the influence of social dynamics in mandrill intersexual relationships. Indeed, female mandrills form well differentiated social bonds biased in favour of close maternal and paternal kin (Charpentier et al., 2020) that might translate into social support in conflicts against adult males or other groupmates. Contrarily, several males enter the social group at the onset of the mating season and they often leave at the end of it (Brockmeyer et al., 2015), likely resulting in limited male social integration and support by groupmates.

3The physical and behavioural sexual dimorphism render the study of intersexual conflicts in mandrills highly relevant. Additionally, the influx of males during the mating season renders the patterns of mandrill intersexual relationships in the wild significantly different than those documented in captivity. The Mandrillus project was set up in 2012 and since then, it monitors the sole social group of wild mandrills habituated to human presence, offering a great opportunity to study intersexual relationships of mandrills in their natural habitat. Recent studies used the long-term behavioural and life-history dataset of Mandrillus project to document patterns of sexual coercion and intersexual dominance in this species. Here, I present a synthesis of this work.

Figure 1

Figure 1

An adult female (left) and and adult male (right) mandrill. Adapted from Smit et al., 2023.

2 Intersexual dominance is not binary

4Few recent studies have questioned the traditional dichotomy of species between strictly female and male dominant, suggesting that intersexual dominance varies along a continuum between these two extremes (Hemelrijk et al., 2020; Izar et al., 2021; Kappeler et al., 2022) and it might even be subject to social or ecological factors leading to variation within species (Kappeler et al., 2022). Accordingly, females appear to occasionally outrank certain males in the generally male dominant mandrills (Smit et al., 2022b). Demographic changes imposed by male immigration seem to have a strong influence on intersexual dominance, as females outrank more males during the mating season, when the number of males per female is higher (Smit et al., 2022b). This result might reflect that increased male-male competition during the mating season generates ‘winner-loser effects' (Dugatkin, 1997; but see also: Bonabeau, 1999) which make ‘loser' males to eventually submit further to females. Additionally, an increased number of males during the mating season can lead to an increased number of low-ranking males who try to increase their mating success via sneaky copulations (similarly to rock hyraxes, Procavia capensis; Bar Ziv et al., 2016) or other non-aggressive strategies. Thus, these males might avoid agonistic interactions and submit to females. In line with this hypothesis, lower-ranking male mandrills show lower sexual coercion rates (Smit et al., 2022a).

3 The influence of social integration and bonds on intersexual dominance

5Sex-biased dispersal might also influence intersexual dominance dynamics through its impact on social integration. Male mandrill social integration in the female social network can improve male social rank (Smit et al., 2022b) and male immigrants are likely little socially integrated. In vervet monkeys, Chlorocebus pygerythrus, females can impact male rank through social integration (Bonnell et al., 2020) and thus, they might bypass the constraints on their reproduction imposed by undesired high-ranking males (Young et al., 2017). Female mandrills might similarly use their social interactions with new males strategically to improve the social integration and increase the rank of preferred males and ‘isolate’ undesired ones.

6Social integration (integration within the social network, measured by some centrality metric) and social bonding (strong dyadic affiliative relationships) appear to have a broad impact on mandrill dominance relationships, influencing also female rank: more bonded and integrated females outrank more males (Smit et al., 2022b). Importantly, female social bonds might occasionally translate into female coalitions against males (personal observation; Setchell et al., 2006). This result suggests that female bonding does not influence intersexual agonism exclusively in species where females are commonly dominant over males, such as spotted hyenas (Crocuta crocuta; Vullioud et al., 2019) or bonobos (Pan paniscus; Parish et al., 2000), but also in species where females are generally subordinate to males, such as mandrills.

4 The influence of social integration and bonds on sexual coercion

7Surprisingly, both female rank (Smit et al., 2022a) and social bonds and integration (Smit et al., 2023) are associated with higher rates of received sexual coercion in female mandrills, in contrast to evidence from feral horses and humans where female social integration reduces sexual coercion (Cense & Brackenridge, 2001; Cameron et al. 2009). These results add to only few recent studies reporting detrimental effects of sociality (Kalbitzer et al., 2017; Blumstein et al., 2018; Thompson & Cords, 2018; Menz et al., 2020; Sabol et al. 2020); and they are at odds with a large body of work documenting its (fitness) benefits (Silk, 2007; Ryder et al., 2009; Schülke et al., 2010; Stanton & Mann, 2012). Although social bonds and integration have likely an overall positive influence on female mandrill fitness (Charpentier et al., 2012), these benefits might be slightly mitigated by costs relevant to sexual coercion.

8An association of sexual coercion and female social integration could reflect different mechanisms. First, males might need to use higher aggression rates to dominate or coerce powerful females, and socially integrated female mandrills are generally more powerful, that is, they have higher social ranks (Smit et al., 2022b). In humans, more powerful women often receive more sexual harassment, but they also respond to it more assertively (Gruber & Bjorn, 1986; Folke et al., 2020). However, a path analysis revealed that the effects of female social rank and integration on the rates of received sexual coercion are independent in mandrills (Smit et al., 2023). This result suggests that the association of rank and social integration or bonding in other species (Vullioud et al., 2019; Wooddell et al., 2020) does not entail that the costs (or benefits) of these traits necessarily coincide. Particularly in mandrills that form exceptionally large groups, even low-ranking females might have the latitude to form strong social bonds and integrate well in their social environment. Low-ranking matrilines can include several adult females that form strong bonds among them or with females from other low-ranking matrilines (personal observation).

9Second, as in many mammals (Pusey et al., 1997; Côté & Festa-Bianchet, 2001), high-ranking female mandrills usually have higher reproductive success than low-ranking ones (Setchell et al., 2002; Dezeure et al., 2022) and males might prefer to mate with them (Setchell & Jean Wickings, 2006). However, the influence of social integration on the rates of received male coercion is independent from female mandrill reproductive success (Smit et al., 2023). Altogether, as the effect of female social integration on the rates of received sexual coercion is not mediated by female reproductive success or social rank, females might receive more coercion simply because they are central in their group and interact often with their groupmates, including coercive males (Smit et al., 2023). This hypothesis is supported by a general association of female social bonding with females or males and the rates of received sexual coercion (Smit et al., 2023).

10Within female-male dyads, female mandrills receive more coercion from males with whom they form stronger bonds (Smit et al., 2023). This observation might suggest that females form bonds with males in order to appease them (i.e., in response to coercion; see also Baniel et al., 2021) or that the formation of these bonds is forced by males, similar to hamadryas baboons (Papio hamadryas hamadryas; Swedell & Schreier, 2009) or bottlenose dolphins (Tursiops aduncus; Connor & Vollmer, 2009). Alternatively, males might coerce their female associates in response to the presence of rival males in order to advertise their vigor to these rivals or menace their female associates not to mate or bond with these rivals. Similar patterns are observed in humans where intimate partner violence and sexual coercion are widespread and common after interactions of women with extra-pair men (Smuts, 1992; Basile, 2002). Finally, males might be innately coercive with all females, and thus, they direct most coercion to females close to them (Smit, under review).

5 Sexual intimidation: sexual coercion in the long-term

11Male mandrills appear to use particularly sexual intimidation against females, that is, a long-term sexually coercive strategy expressed as aggression over periods preceding a female's receptive period that increases mating success with the female victim when she will be receptive (Smit et al., 2022a). Previously, sexual intimidation had been documented only in chimpanzees (Pan troglodytes; Muller et al., 2007) and chacma baboons (Papio ursinus; Baniel et al., 2017) and researchers had analyzed only patterns of severe male aggression. Male mandrills intimidate females using also threats (such as head-bobs or ground-slaps) which produce inconspicuous immediate behavioural reactions of victims (Smit et al., 2022a); reminding the threats used against women by sexually coercive men (World Health Organization, 2012). Thus, male mandrills likely take advantage of their extreme physical superiority to intimidate females at low effort. These inconspicuous behaviours and the temporal dissociation of aggression and mating highlight the possibility that sexual intimidation is more common than previously though in polygynandrous and/or sexually dimorphic mammals (similar to chimpanzees, chacma baboons and mandrills). Future studies based on long-term fine-grained behavioural observations on more species might confirm or reject this claim.

6 Reproductive control - dominance, coercion and mate choice

12Species that live in polygynous or polygynandrous groups often show high levels of male intrasexual competition, which can lead to the evolution of sexual dimorphism in size and strength (Emlen & Oring, 1977). Then, males can use their physical superiority to dominate females socially (Davidian et al., 2022) and coerce them sexually (Smit, under review; Smuts & Smuts, 1993) leading to a general association of social and reproductive control (Huchard et al., in prep), that is control over when and with whom to mate (Beekman et al., 2003). Mandrills seem to generally follow these patterns as males usually dominate females (Smit et al., 2022b), they use mate-guarding, sexual intimidation (Smit et al., 2022a) and infanticide (unpublished data) to increase their mating success with them, and show high reproductive skew (Charpentier et al., 2005; 2020). Hence, the major physical asymmetry between the sexes likely offers high social and reproductive control of male over female mandrills.

13The increased reproductive control of males seems to question previous evidence that female mandrills express mate choice (Setchell, 2005). Then, the selective pressures that have promoted the evolution of extravagant male mandrill ornaments (Setchell & Dixson, 2001; Setchell, 2005) remain concealed. These ornaments might represent a ‘badge of status’. The extreme armaments of male mandrills (e.g., ~4.5cm long canines; Leigh et al., 2008) render fights too costly or even lethal (Setchell & Wickings, 2005). Male ornaments correlate with competitive ability and willingness to engage in fights (Setchell et al., 2008) and are ultimately correlated with dominance rank (Setchell & Dixson, 2001; Setchell et al., 2008; Renoult et al., 2011). Hence, male mandrills might use colours as conflict management signals that advertise, honestly (or not), competing abilities (Preuschoft & van Schaik, 2000; Setchell & Wickings, 2005; Setchell et al., 2008). A colour contest might resolve most conflicts minimizing superfluous fights. In line with this hypothesis, male mandrill fights are more common between similarly coloured males (Setchell & Wickings, 2005).

14Ultimately, female mandrills might be in fact able to express mate choice (based on male ornaments or otherwise) despite the male sexually coercive strategies. They are observed to copulate sneakily with males other than those who mate-guard them, to interrupt copulation before ejaculation and to escape males climbing trees (personal observation); while they might even influence male rank through social integration (Smit et al., 2022b). Female mate choice and male coercion may co-occur in mandrills as they do in chimpanzees (Muller et al., 2007; Pieta, 2008; Kaburu & Newton-Fisher, 2015; Watts 2022) and humans (Basile, 2002; Puts, 2010). Thus, the drivers of female behaviour towards males are occasionally hard to interpret: mating, solicitation or approach/avoidance of a male can reflect female mate choice or response to sexual coercion. Despite the apparent male-biased reproductive control, only future analyses can indicate the fitness benefits (for males) and costs (for females) of sexual coercion as well as which female behaviours have potentially evolved as counter-strategies to sexual coercion allowing the expression of female mate choice.

Acknowledgments

15I thank Marie Charpentier and Elise Huchard for their precious help and guidance in conducting my research in mandrills as well as all field assistants that have contributed in the Mandrillus project. I also thank Berta Roura-Torres and Axelle Delaunay for their comments on a previous version of this report. Finally, I thank the members of the committee at the 34ème colloque de la Société francophone de primatologie (SFDP) for awarding the prix de thèse to my talk and inviting me to write this report. This is ISEM publication number 2024-165.

Declaration of competing interests

16I declare no conflict of interest.

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List of illustrations

Title Figure 1
Caption An adult female (left) and and adult male (right) mandrill. Adapted from Smit et al., 2023.
URL http://journals.openedition.org/primatologie/docannexe/image/18340/img-1.png
File image/png, 5.4M
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References

Electronic reference

Nikolaos Smit, Intersexual relationships in mandrills: dominance, sexual conflict and the influence of social integrationRevue de primatologie [Online], 15 | 2024, Online since 18 July 2024, connection on 24 June 2025. URL: http://journals.openedition.org/primatologie/18340; DOI: https://doi.org/10.4000/121oy

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About the author

Nikolaos Smit

Institut des Sciences de l’Évolution, Université de Montpellier, Montpellier, France
Email: snikos@tutanota.com

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