Stability and strength of male-female associations in a promiscuous primate society

Close associations between adult males and lactating females occur in several promiscuous primate species. Benefits gained by males from such bonds may include increases in offspring fitness through paternal effort (the "mate-then-care" hypothesis) and/or subsequent mating opportunities with the female (the "care-then-mate" hypothesis). Heterosexual friendships between males and females have been described as tightly linked to the presence of a dependent infant, but few studies have investigated whether these associations may be longer, starting before an infant birth and lasting after its independence, and whether they may vary in strength across time and dyads. We investigated the stability and strength of heterosexual bonds in two groups of wild chacma baboons (Papio ursinus) to test whether male-female associations (1) last from offspring conception to independence, as expected under the mate-then-care hypothesis, (2) last after maternal cycling resumption and increase male mating success, as expected under the care-then-mate hypothesis, and (3) vary in strength depending on female reproductive state, age and rank. Our results show that most male-female bonds were already present at offspring conception, were maintained during pregnancy and lactation and disappeared when mothers resumed cycling. Moreover, heterosexual bonds were most intense during early lactation and for high-ranking females, and did not predict subsequent mating activity. Those findings favour the mate-then-care hypothesis, and confirm that male paternity assessment may, at least partially, rely on mating history. Overall, stable heterosexual friendships exist outside early lactation and last longer than previously thought, suggesting that male-female bonds could play an important and under-appreciated role on the social structure of groups in promiscuous primate societies. Stable male-female bonds are rare in promiscuous mammals. Baboons are unusual in this respect: tight friendships have been described between adult males and lactating females and may protect infants against infanticide, but few studies have investigated whether these associations may start before an infant's birth, or extend after its nutritional independence. We explored the stability and strength of heterosexual relationships in the chacma baboon, and found that friendships start before or at infant's conception, are maintained throughout pregnancy, strengthen during lactation and disappear when mothers resume cycling. Such pattern of association suggests that male-female bonds represent paternal effort, and may arise from sexual activity before and during the conceptive cycle. Most females appear permanently associated with one male regardless of their reproductive state, suggesting that heterosexual bonds play an important, and under-appreciated, role in structuring the social organization of baboon societies.