Nested Male Reproductive Strategies in a Tolerant Multilevel Primate Society

Abstract Male reproductive success varies within populations. Models explaining reproductive skew largely emphasize dominance, yet the determinants of male reproductive success in egalitarian societies remain poorly understood. Using nine years of behavioral and genetic data from five parties, we investigated male reproductive monopolization in wild Guinea baboons ( Papio papio ), an egalitarian multilevel society with one-male “units” nested within “parties” and low male-male contest competition. Genetic analyses showed 93% of the 71 infants were sired by the female’s “unit male”, with rare extra-unit paternities consistent with limited control models. Within parties, reproduction was shared among multiple unit males, resulting in low reproductive skew, with top males siring 23-40% of offspring, well below levels in hierarchical species. Female takeovers were rare, suggesting male restraint. Reproductive success, assessed as the number of unit females, was positively associated with dominance ratings, yet males with average ratings held the largest units. Prime-age predicted reproductive success better than dominance. In conclusion, male Guinea baboons’ reproductive success is shaped less by dominance than by age and stable associations with females, who play an active role in inter-sexual relationships. These results emphasize the need to move beyond frameworks focused solely on dominance-based mechanisms and to consider species-specific social organization. Significance statement Current theoretical models of male reproductive success often focus on dominance and males’ ability to monopolize access to females. Yet, less is known about the determinants of reproductive success in societies with egalitarian male relationships, such as the multilevel society of wild Guinea baboons. Using nine years of behavioral and genetic data from five groups (“parties”), we show that unit males almost always sire their unit’s offspring. However, at the party level, male reproductive skew is low. Reproductive success is better predicted by prime-age than dominance and appears to result from long-term associations with females, likely shaped by female choice. Our results highlight the need to examine diverse social systems to understand the evolution of reproductive strategies beyond dominance-centered models.