Nested Male Reproductive Strategies in a Tolerant Multilevel Primate Society

Male reproductive success often varies significantly within populations, and several theoretical models, mostly revolving around dominance, have been used to explain reproductive skew. The determinants of male reproductive success in egalitarian societies are less well understood. We investigated male reproductive monopolization in wild Guinea baboons (Papio papio), an egalitarian multilevel society in which one-male "units" are nested within larger social groups ("parties") and male-male contest competition is low. Using nine years of behavioral and genetic data from five parties, we examined how reproductive success is distributed across males at different social levels. Paternity data show that 93% of the 71 infants were sired by the females "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. The most successful males accounted for 23-40% of paternities within parties, well below the proportions reported in strictly hierarchical species. Takeovers of females were rare, suggesting male restraint. Reproductive success, assessed as the number of unit females, was positively associated with dominance ratings, yet males with average dominance ratings had the largest units. Altogether, prime-age was a better predictor of reproductive success than dominance. In conclusion, male Guinea baboons reproductive success is shaped less by dominance and more by long-term associations with females, who play an active role in inter-sexual relationships. Our study emphasizes the need to move beyond frameworks focused solely on dominance-based mechanisms and to incorporate species-specific social organization when evaluating reproductive strategies. Significance statementCurrent 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 units 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.