Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.
In humans, being more socially integrated is associated with better physical and mental health and/or with lower mortality. This link between sociality and health may have ancient roots: sociality also predicts survival or reproduction in other mammals, such as rats, dolphins, and non‐human primates. A key question, therefore, is which factors influence the degree of sociality over the life course. Longitudinal data can provide valuable insight into how environmental variability drives individual differences in sociality and associated outcomes. The first year of life—when long‐lived mammals are the most reliant on others for nourishment and protection—is likely to play an important role in how individuals learn to integrate into groups. Using behavioral, demographic, and pedigree information on 376 wild capuchin monkeys (
Having more maternal kin (mother and siblings) is associated with spending more time near others across developmental stages in both male and female capuchins. Having more offspring as a subadult or adult female is additionally associated with spending more time near others. A mother's average sociality (time near others) is predictive of how social her daughters (but not sons) become as juveniles and subadults (a between‐mother effect). Additional variation within sibling sets in this same maternal phenotype is not predictive of how social they become later relative to each other (no within‐mother effect).
- NSF-PAR ID:
- 10493011
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Developmental Science
- ISSN:
- 1363-755X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Taborsky, Michael (Ed.)Abstract The juvenile period is a challenging life-history stage, especially in species with a high degree of fission–fusion dynamics, such as bottlenose dolphins, where maternal protection is virtually absent. Here, we examined how juvenile male and female bottlenose dolphins navigate this vulnerable period. Specifically, we examined their grouping patterns, activity budget, network dynamics, and social associations in the absence of adults. We found that juveniles live in highly dynamic groups, with group composition changing every 10 min on average. Groups were generally segregated by sex, and segregation was driven by same-sex preference rather than opposite-sex avoidance. Juveniles formed strong associations with select individuals, especially kin and same-sex partners, and both sexes formed cliques with their preferred partners. Sex-specific strategies in the juvenile period reflected adult reproductive strategies, in which the exploration of potential social partners may be more important for males (which form long-term alliances in adulthood) than females (which preferentially associate with kin in adulthood). Females spent more time alone and were more focused on foraging than males, but still formed close same-sex associations, especially with kin. Males cast a wider social net than females, with strong same-sex associations and many male associates. Males engaged in more affiliative behavior than females. These results are consistent with the social bonds and skills hypothesis and suggest that delayed sexual maturity in species with relational social complexity may allow individuals to assess potential associates and explore a complex social landscape without the risks associated with sexual maturity (e.g., adult reproductive competition; inbreeding).more » « less
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null (Ed.)Bornean orangutans' extended life history may be an adaptation to their forest habitat, characterized by dramatically fluctuating fruit availability. We hypothesize that juveniles rest and are carried more when fruit availability is low, spending less time in developmentally important behavior including play and independent travel to conserve energy. We test this using generalized linear mixed models and data derived from 976 follows of infant and juvenile orangutans collected during periods of varying fruit availability. Age (p<0.001), but not fruit availability (p>0.05) significantly affected offsprings’ time being carried (β=-8,1) and resting (β=-2.6, p<0.001). Younger individuals spent more time clinging and resting regardless of fruit availability. Fruit availability and offspring age interact to affect the proportion of time juveniles play (β=1.5, p<0.001) and travel (β=-0.8, p<0.001). Fruit availability impacts younger juveniles’ play behavior more dramatically than older juveniles: younger juveniles play more when fruit availability is high than when it is low, while older juveniles exhibit little variation in time spent playing depending on fruit availability. Juveniles aged 6-8 travel more when fruit availability is medium and high, juveniles aged 2-5 travel slightly less when fruit availability is high, and juveniles under 2 rarely travel independently. We also examined relationships between fruit availability, offspring age, and maternal travel distance using 2065 mother-offspring follows, demonstrating that females travel shorter distances with offspring under four, and when fruit availability is low. Thus, orangutans shift activity in response to fruit availability and throughout development, buffering young orangutans against energy depletion but suppressing developmentally important activities. Funders: NSF (9414388, BCS-1638823, BCS-0936199); National Geographic; USFish/Wildlife (F18AP00898, F15AP00812, F13AP00920, 96200-0-G249, 96200-9-G110); Leakey; Disney Conservation Fund; Wenner-Gren; Nacey-Maggioncalda; Conservation-Food-Health; Orangutan Conservancy; Woodland Park Zoomore » « less
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Abstract Various aspects of sociality in mammals (e.g., dyadic connectedness) are linked with measures of biological fitness (e.g., longevity). How within- and between-individual variation in relevant social traits arises in uncontrolled wild populations is challenging to determine but is crucial for understanding constraints on the evolution of sociality. We use an advanced statistical method, known as the ‘animal model’, which incorporates pedigree information, to look at social, genetic, and environmental influences on sociality in a long-lived wild primate. We leverage a longitudinal database spanning 20 years of observation on individually recognized white-faced capuchin monkeys (
Cebus capucinus imitator ), with a multi-generational pedigree. We analyze two measures of spatial association, using repeat sampling of 376 individuals (mean: 53.5 months per subject, range: 6–185 months per subject). Conditioned on the effects of age, sex, group size, seasonality, and El Niño–Southern Oscillation phases, we show low to moderate long-term repeatability (across years) of the proportion of time spent social (posterior mode [95% Highest Posterior Density interval]: 0.207 [0.169, 0.265]) and of average number of partners (0.144 [0.113, 0.181]) (latent scale). Most of this long-term repeatability could be explained by modest heritability (h 2 social : 0.152 [0.094, 0.207];h 2 partners : 0.113 [0.076, 0.149]) with small long-term maternal effects (m 2 social : 0.000 [0.000, 0.045];m 2 partners : 0.000 [0.000, 0.041]). Our models capture the majority of variance in our behavioral traits, with much of the variance explained by temporally changing factors, such as group of residence, highlighting potential limits to the evolvability of our trait due to social and environmental constraints. -
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Abstract Objectives In humans and other mammals, maternal hormones are transferred to offspring during lactation via milk and may regulate postnatal development, including the pace of early growth. Here, we used a nonhuman primate model to test the hypotheses that milk cortisol and dehydroepiandrosterone‐sulfate (DHEAS) concentrations reflect maternal characteristics, and that changes in these hormones across lactation are associated with early postnatal growth rates.
Methods Demographic information, morphometrics, and milk samples were collected from rhesus macaque mothers and their infants at the California National Primate Research Center in Davis, California. Using linear models, we examined the relationship between maternal traits and milk hormone concentrations (N = 104 females) and explored the effect of milk hormones on the rate of offspring growth (N = 72 mother‐infant dyads), controlling for available milk energy.
Results Contrary to previous studies, we found that milk cortisol concentrations were categorically higher in multiparous females than in primiparous females. However, milk DHEAS concentrations decreased with maternal parity. Neither milk cortisol nor DHEAS were related to maternal rank. Finally, changes in milk hormones predicted offspring growth in a sex‐specific and temporal manner: increases in cortisol from peak to late lactation predicted faster female growth, and increases in DHEAS concentrations from early to peak and peak to late lactation predicted faster male growth.
Conclusions Our findings shed light on how hormonal components of milk have sex‐specific effects on offspring growth during early postnatal life with varying temporal windows of sensitivity.
