Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi)

Abstract

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Keywords: affiliative relationships; infants; juveniles; maternal care; social bonds.

Figure 1

Probability that immatures groomed with group members other than their mothers, as a function of their age (p = 0.026). For each study subject, black circles represent the mean monthly probability of grooming for male offspring, whereas grey asterisks represent the mean monthly probability of grooming for female offspring. Data points are slightly jittered to avoid overlapping. The line represents the fitted model, which is like Model 2, with observational effort expressed in 15 min intervals.

Figure 2

Probability that immatures played with group members other than their mothers, as a function of their squared age (p = 0.048) (separately for male and female immatures). For each study subject, black circles represent the mean monthly probability of grooming for male offspring, whereas grey asterisks represent the mean monthly probability of grooming for female offspring. Data points are slightly jittered to avoid overlapping. The two lines represent the fitted model (the black one for males, the grey one for females), which is like Model 3, with observational effort expressed in 15 min intervals.

Figure 3

Probability that immatures played with group members other than their mothers, as a function of maternal investment (i.e., a score between 0 and 1, based on the proportion of time mothers spent nursing, carrying, grooming, touching and playing with their offspring, with 0 meaning no maternal investment; see text for more details; p = 0.017) (separately for male and female immatures). For each study subject, black circles represent the mean monthly probability of grooming for male offspring, whereas grey asterisks represent the mean monthly probability of grooming for female offspring. Data points are slightly jittered to avoid overlapping. The two lines represent the fitted model (the black one for males, the grey one for females), which is like Model 3, with observational effort expressed in 15 min intervals.

Figure 4

Social networks of the spider monkey group observed, based on the undirected, weighted matrix of proximity (left) and grooming interactions (right) after removing interactions between immatures and their mothers. Dots represent individuals of the group and are the nodes of the social network, whereas lines represent their edges. The thickness of weighted edges and the size of the nodes are proportional to the individual’s strength in the social network (i.e., the sum of all edge weights connected to the node). Communities (i.e., groups of nodes including a high proportion of the edge weight, detected using leading eigenvector communities) are depicted in different colours (Farine & Whitehead, 2015 [73]).

Figure 5

Correlations between eigenvector centralities of female immatures and their mothers for proximity (left) and grooming interactions (right). Dots represent female immatures, the line represents the regression line and the grey area represents the confidence intervals.