Several studies have documented the importance of social bonding for the enhancement of individual fitness. However, little is known about how social relationships develop through ontogeny, and whether their development follows the same trajectory in males and females. Here we analyzed affiliative interactions (proximity, social grooming, play) combined with demographic and genetic data in semi-free-ranging rhesus macaques (Macaca mulatta) on Cayo Santiago over their first 4 yr of life (from birth to sexual maturation) to understand how these interactions change through development in both sexes. Generalized linear mixed models revealed that social behaviors mostly followed different developmental trajectories in males and females and were highly dependent on the social context. In particular, sex differences in social behavior varied through development depending on the partner’s sex and age. Females engaged in more social interactions than males, especially with other females, and were more involved in grooming around the time of maturation. In contrast, males interacted more with males and age peers, especially around maturation. Sex differences in social behavior varied through development, but also depended on rank, partner’s rank, and kin line, although not consistently. High-ranking individuals, especially older females, were generally preferred as social partners. Moreover, both male and female individuals interacted mostly with maternal kin, although males also preferred paternal kin over nonkin. Importantly, most developmental changes in sociality happened when individuals were ca. 2 yr old, suggesting that this might be a milestone in the development of sociality in rhesus macaques. The only notable exception to this pattern was play, which was more pronounced in males from the beginning of their lives. We propose that play might serve as a trigger of sex differences in social behavior, with sex differences emerging early in development and increasing through time as males and females gradually grow into their adult social roles.

In multi-male groups where females mate promiscuously, male-infant associations have rarely been studied. However, recent studies have shown that males selectively support their offspring during agonistic conflicts with other juveniles and that father’s presence accelerates offspring maturation. Furthermore, it was shown that males invest in unrelated infants to enhance future mating success with the infant’s mother. Hence, infant care might provide fitness gain for males. Here we investigate male-infant associations in rhesus macaques (Macaca mulatta), a primate with low paternity certainty as females mate with multiple partners and males ensure paternity less efficiently through mate-guarding. We combined behavioral data with genetic paternity analyses of one cohort of the semifree-ranging population of Cayo Santiago (Puerto Rico) and recorded affiliative and aggressive interactions between focal subjects and adult males from birth to sexual maturation (0–4 years) of focal subjects. Our results revealed, that 9.6% of all interactions of focal subjects involved an adult male and 94% of all male-infant interactions were affiliative, indicating the rareness of male-infant aggression. Second and most interestingly, sires were more likely to affiliate with their offspring than non-sires with unrelated infants. This preference was independent of mother’s proximity and emphasized during early infancy. Male-infant affiliation rose with infant age and was pronounced between adult males and male rather than female focal subjects. Overall our results suggest that male-infant affiliation are also an important component in structuring primate societies and affiliation directed towards own offspring presumably represent low cost paternal care.

Preferential affiliative relationships, or social bonds, play a crucial role in primate social life, but little is known about their development. Here, we review macaque studies investigating the social development of both sexes. Firstly, we highlight the emergence of sex differences in mother-offspring bonds, as macaque mothers form stronger bonds with daughters, while being more aggressive towards sons, possibly contributing to maintain female philopatry and/or male dispersal. Secondly, despite paternity uncertainty, we discuss studies reporting that fathers of several macaque species preferentially engage with their offspring, but less than mothers and only in periods of high infant mortality. Thirdly, we show that immature females, the philopatric sex in macaques, already form stronger bonds with close maternal kin than immature males, mirroring social patterns during adulthood. However, this bias seems not caused by kin availability, as kin availability is similar for both sexes prior to male dispersal. Moreover, immature males might preferentially affiliate with paternal kin over non-kin, possibly because of lower maternal integration in their maternal family and/or in preparation of dispersal. Fourthly, we discuss how immature females engage in grooming and proximity with female partners as they grow older, while immature males preferentially interact with adult males and peers, playing more than females from early on. Finally, we show that most developmental changes in sociality happen around 2-3 years of age, probably representing a milestone in macaque social development. We conclude that sex differences in sociality emerge early in development and increase through time, with sexes gradually growing into their adult roles.