Patterns and Consequences of Male–Infant Relationships in Wild Assamese Macaques (Macaca assamensis)

Abstract

Male care for offspring is unexpected in polygynandrous mammals. Evidence from nonhuman primates, however, indicates not only the existence of stable male–immature associations in multimale–multifemale groups, but also male care in the form of protection from infanticidal attacks and conspecific harassment. Here, we investigate the relationship characteristics, dynamics, and consequences of male–immature associations in wild Assamese macaques, Macaca assamensis, at Phu Khieo Wildlife Sanctuary, Thailand, to inform hypotheses of their evolutionary origins. Female Assamese macaques reproduce seasonally and do not signal ovulation, resulting in low mating and paternity skew. However, male–immature associations are predicted by paternity, and male behavior potentially reflects paternal effort. We present focal animal data on 12 immatures followed from birth beyond weaning into their juvenile life (1188 focal hours). The distribution of composite sociality indices suggests that male–immature relationships were highly differentiated. Association patterns and the degree of differentiation remained stable from 6 mo well into the juvenile phase, suggesting that male protection extends beyond the phase of high infanticide risk. Based on Hinde indices, immatures were responsible for maintaining the relationships. The likelihood that an infant was associated with its preferred male increased if the mother was absent and if other males were present in proximity, suggesting that immatures sought protection. The presence of the preferred male did not decrease the rate of mild aggression immatures received from group members, but the stronger the relationship between an immature and a male, the more often it received agonistic support from him. Future studies will have to assess whether this agonistic support translates into improved fitness and represents true paternal care.

Triadic male-infant-male interaction serves in bond maintenance in male Assamese macaques

“…Interestingly, male Assamese macaques sharing a stronger affiliative relationship (CSI≥1) were about five times more often involved in MIMIs than male-male dyads with a weaker relationship (CSI<1) and relationship strength was positively associated with MIMI frequency even after controlling for the time they spent in 5m spatial proximity. These results, together with the finding that the dyadic frequency of MIMIs influences future cooperation in Barbary macaque males [ 74 ] and that affiliative male-infant relationships are initiated by infants rather than by the males of this study [ 92 ], support the hypothesis that MIMIs function to form and reinforce male social bonds [ 65 ]. In this sense, MIMIs in macaque males may functionally parallel greetings exchanged between baboon males that are also proposed as a bonding mechanism enhancing a male’s willingness to cooperate [ 65 , 93 , 94 ].…”

“…Yet the opportunity to bond might be limited in Assamese macaques since a male approaches any other male on average only 0.22 times per hour and only 10% of these approaches are followed by an affiliative social interaction. A male’s time budget and its ability to devote time to establish and maintain affiliative relationships with other males is restricted by time devoted to other activities such as bonding with females [ 19 , 32 , 96 ] and infants [ 92 , 97 – 99 ], sexual consortships [ 100 – 104 ] and foraging [ 105 – 107 ]. In light of these time constraints, males should optimize the little time they can afford to invest in bonding.…”

Growing into adulthood—a review on sex differences in the development of sociality across macaques

“…A recent study of the same population confirmed that these associations persist until the juvenile period is reached; however, infants maintain these bonds as they approach males more than vice versa. It was therefore suggested that infants actively seek male protection, and indeed, males provide agonistic support to immatures, which increases with the strength of their relationship (Minge et al 2016).…”

Variation in Adult Male-Juvenile Affiliative Behavior in Japanese Macaques (Macaca fuscata)

“…Paternal behavior has largely been observed to take the form of grooming, playing, and carrying, with increases in the rate of these behaviors during the birthing season [Itani, 1959;Alexander, 1970]. Male affiliative bonds with juveniles have been reported repeatedly for a number of macaque species, and it may be a function of their high gregariousness and adaptability [Itani, 1959;Mitchell, 1969;Alexander, 1970;Maestripieri and Carroll, 1998;Berghänel et al, 2011;Minge et al, 2016]. As such, macaques present a uniquely well-suited model genus for examining juvenile-directed affiliative behavior.…”