Chimpanzees: Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males

The development of affiliative and coercive reproductive tactics in male chimpanzees. Rachna B. Reddy, Kevin E. Langergraber, Aaron A. Sandel, Linda Vigilant and John C. Mitani. Proceedings of the Royal Society B: Biological Sciences, January 6 2021. https://doi.org/10.1098/rspb.2020.2679

Rolf Degen's take: https://twitter.com/DegenRolf/status/1346820516317949954

Abstract: Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.

4. Discussion

The results presented here suggest that adolescent male chimpanzees, who cannot effectively compete with older males nor sexually coerce adult females, employ at least two behavioural tactics to mate and reproduce. First, as reported in previous research, adolescent males appear to target adolescent, nulliparous females as mating partners; they mate with nulliparous females frequently and father their first offspring more often in adolescence than they do in adulthood [42,48]. Our findings also corroborate past research indicating that nulliparous female chimpanzees are less preferred as mating partners than are parous females. Specifically, as male chimpanzees transition from adolescence to adulthood and rise in dominance rank, they show less sexual interest in nulliparous females and target them for aggression infrequently [47]. High-ranking males also rarely father the first offspring of these females [33–37,42]. Second, mating success for adolescent and young adult males was predicted by the strength of affiliative bonds that males formed with females. Male aggression, by contrast, had a relatively weak relationship with mating success, but one that strengthened as males grew older and increasingly dominant to females.

These findings increase our understanding of the nature of sexual coercion in chimpanzees. We have recently shown that adolescent and young adult males selectively direct aggression toward females with whom they form strong affiliative bonds [49]. Here, we demonstrate that aggression has a reduced effect on mating success outside of these bonds for young, adolescent males who are not yet physically mature and unlikely to dominate females [49,54,71]. Instead, mating success increases when an older adolescent or young adult male directs aggression to a female with whom he frequently affiliates and can dominate.

These results complement prior research that indicates aggression, mating and reproduction are linked in chimpanzees [28,30,31] and clarify the role that affiliation plays in creating those linkages. Specifically, sexual coercion is more effective when adolescent and young adult males have affiliative bonds with the females they attack. One reason may be that females suffer higher costs if they refuse to mate with males with whom they frequently affiliate compared to males with whom they rarely affiliate [12]. The nature of these costs remains to be explored. Nor is it clear whether and how affiliative relationships with males benefit female chimpanzees. It is important to note that our findings are consistent with patterns of intersexual aggression in other species where males are highly aggressive to females with whom they share bonds. This includes hamadryas baboons (Papio hamadryas), where females live in one-male groups, and most social activity is directed by the single males in these groups, i.e. ‘leader males’. After being attacked by their leader male, hamadryas females appear fearful and follow him even more closely than they had previously [72]. In our own species too, many women are subject to frequent sexual coercion by their male partners, but often remain in such relationships for reasons that vary widely [73].

Scant data exist about the proximate psychological mechanisms that underlie male aggression and female compliance in chimpanzees. However, investigating these proximate mechanisms may provide information about how bonds that affect paternity in chimpanzees might lead to a human-like social system [74]. One interpretation consistent with our preliminary observations is that male aggression toward their social partners is motivated by sexual possessiveness (e.g. [73]), and that females have a psychologically distinct experience when attacked by a male with whom they have an affiliative bond. For example, adolescent and young adult males make direct attacks on male peers infrequently, but when they do so, it is when another male mates or attempts to mate with one of their female social partners [49]. Anecdotally, when female chimpanzees received aggression from an adult male who did not have a strong affiliative bond with them, they often just screamed and ran away. Females receiving similar aggression from males with whom they shared strong affiliative relationships, however, react in an entirely different way. When attacked, these females remain in place, lunge toward their male partners while clutching their arms, rocking back and forth, and screaming repeatedly until making choking sounds.

Our study has several limitations. First, we cannot evaluate the relative impacts of affiliation and aggression on adolescent male paternity success. Only seven males in this study have reproduced thus far, siring 15 offspring, creating a small sample to make strong inferences. Our preliminary findings based on this small sample suggest that males who affiliate with and direct aggression to specific females gain a reproductive advantage with those females, but additional data are clearly needed. As these data accumulate, evaluating the effects of affiliation and aggression on male reproduction will be complicated because additional factors that we have not considered will require examination. For instance, we are likely to have underestimated the importance of sexual coercion, as it may act to ensure mating exclusivity as well as increasing a male's ability to mate with a specific female [12]. In this context, aggression is often used to initiate consortships in chimpanzees, where males lead females away from other community members and mate with them exclusively for several days (e.g. [21]). The challenge of maintaining exclusivity is not uniform. It may be relatively easy for high-ranking males because fewer males will challenge them to mate, or easier to accomplish with nulliparas, who are not preferred mating partners [47]. Second, we conducted this study over a relatively short period spanning two years, which covered only a single reproductive cycle for most females. Additional research is required to determine whether affiliative bonds between males and females endure and whether the patterns of aggressive and affiliative behaviour between bonded pairs persist and impact male reproduction over the long term (e.g. [30,37]). Determining whether such long-term relationships exist and how they impact male mating and reproductive success will improve our understanding of male chimpanzee development and the functional consequences of their behaviour.

Our findings also provide insights into the evolution of human pair bonds. Although the mechanisms that ensure paternity certainty in our species are diverse, including intimate partner violence [73–75] and larger cultural structures (e.g. religion: [76,77]), our finding that affiliative bonds between males and females appear entwined with sexual coercion in one of our two closest living relatives suggests that this aspect of intersexual relationships may be embedded deeply in our past.