Food sharing patterns in three species of callitrichid monkeys (Callithrix jacchus, Leontopithecus chrysomelas, Saguinus midas): Individual and species differences.

Food sharing (FS) in cooperatively breeding callitrichids is unusual among nonhuman primates because they regularly share significant amounts of preferred food with immatures and engage in proactive FS. However, it is still unclear which classes of individuals (males or females, breeders or helpers) engage most in FS, and whether differences exist among callitrichid species. In the first part of this study, we characterized general FS patterns in common marmosets (Callithrix jacchus). We found substantial adult-immature FS, and female breeders shared the least with immatures. This conflicts with previously published studies, where data were collected with the prevailing standard method of providing a food bowl to the entire group. In the second part, a comparison of our access-bias-free method and the standard method suggested that previous findings are likely the result of access bias. In the third part, we investigated species differences in adult-adult FS among common marmosets, golden-headed lion tamarins (Leontopithecus chrysomelas), and red-handed tamarins (Saguinus midas). As common marmosets show lower levels of interdependence within groups, we expected more adult-adult FS in tamarins compared with marmosets. Adult-adult FS was indeed more prevalent in tamarins and not exclusively directed from male breeders to female breeders. Therefore, our results suggest that adult-adult FS in marmosets mostly reflects the high energetic demands of female breeders, whereas in the more interdependent tamarins, it may be used to reinforce cooperative bonds between adult group members. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Why help? Relationship quality, not strategic grooming predicts infant-care in group-living marmosets.

Cooperatively breeding common marmosets raise their infants with the help of other adult group members, but individual care-taking contribution can vary considerably. We tested four hypotheses that may explain this variation within marmoset family groups. The pay-for-help hypothesis argues that allogrooming is used strategically by parents to pay helpers for helping. The pay-for-infant-access hypothesis claims that helpers use allogrooming as payment for infant-access. The intrinsic predisposition hypothesis suggests that more affiliative individuals are also more motivated for infant-care, and the relationship quality hypothesis that individuals involved in highly affiliative relationships with main caregivers contribute more to infant-care. To test these hypotheses, we followed five marmoset family groups over a total of eight reproductive cycles, and quantified affiliative behavior, infant-carrying, and food sharing over six to 12 weeks around infant-birth. We found no evidence for either the pay-for-help or pay-for-infant-access hypotheses nor did intrinsic prosocial predisposition determine individual infant-care. Mutual dyadic affiliation, however, was positively linked to infant-carrying and food sharing in female and male breeders and in male helpers. This suggests that cooperation during infant-care is mediated by relationship quality rather than strategic grooming in marmosets. Overall, these results may also contribute to a better understanding of cooperation in humans.

Long-term-stability of relationship structure in family groups of common marmosets, and its link to proactive prosociality.

Cooperatively breeding, group-living common marmosets show differentiated relationships, where more strongly bonded dyads within a group engage more in affiliative interactions than less strongly bonded ones. Intriguingly, recent results suggest that strong bonds do not only occur between breeding partners but between individuals from any sex or status, and that strong-bond partners exhibit correlated oxytocin fluctuations (dyadic oxytocin synchrony, OTS) over a period of six weeks. To date, it is unclear whether such relationships are stable over time and whether they are also reflected in higher partner-specific proactive prosociality. To assess the long-term stability of the relationship structure of common marmoset family groups, we investigated whether hormonal and behavioral markers of group structure (dyadic OTS, dyadic affiliation, and individual group integration) in common marmoset families remained stable over a period of six months. We collected baseline urinary OT and social behavior of 36 dyads from three family groups in a non-reproductive period (period A), and again six months later, around the birth of new infants (period B). Patterns of dyadic OTS, dyadic affiliation, and individual group integration were consistent between the two study periods. Oxytocin data from a fourth group (10 dyads), collected in two non-reproductive periods separated by a period of more than five years, could replicate this finding. Furthermore, OTS was also correlated with proactive prosociality that was assessed experimentally for 38 dyads during an earlier study. These results suggest that differentiated relationships are stable over time, even between group members other than the breeding pair, and that more strongly bonded partners also show higher levels of proactive prosociality. Future studies are necessary to identify whether these relationships have an adaptive function, perhaps with regard to positive consequences on cooperativeness.

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys.

The neurohormone oxytocin (OT) is positively involved in the regulation of parenting and social bonding in mammals, and may thus also be important for the mediation of alloparental care. In cooperatively breeding marmosets, infants are raised in teamwork by parents and adult and sub-adult non-reproductive helpers (usually older siblings). Despite high intrinsic motivation, which may be mediated by hormonal priming, not all individuals are always equally able to contribute to infant-care due to competition among care-takers. Among the various care-taking behaviors, proactive food sharing may reflect motivational levels best, since it can be performed ad libitum by several individuals even if competition among surplus care-takers constrains access to infants. Our aim was to study the link between urinary OT levels and care-taking behaviors in group-living marmosets, while taking affiliation with other adults and infant age into account. Over eight reproductive cycles, 26 individuals were monitored for urinary baseline OT, care-taking behaviors (baby-licking, -grooming, -carrying, and proactive food sharing), and adult-directed affiliation. Mean OT levels were generally highest in female breeders and OT increased significantly in all individuals after birth. During early infancy, high urinary OT levels were associated with increased infant-licking but low levels of adult-affiliation, and during late infancy, with increased proactive food sharing. Our results show that, in marmoset parents and alloparents, OT is positively involved in the regulation of care-taking, thereby reflecting the changing needs during infant development. This particularly included behaviors that are more likely to reflect intrinsic care motivation, suggesting a positive link between OT and motivational regulation of infant-care.

Strongly bonded family members in common marmosets show synchronized fluctuations in oxytocin.

Oxytocin is a key regulator of social bonding and is positively linked to affiliation and prosocial behavior in several mammal species. In chimpanzees, this link is dyad-specific as affiliative interactions only elicit high oxytocin release if they involve strongly bonded individuals. These studies involved isolated dyads and sampling events. Little is known about the role of oxytocin in affiliation and social bonding, and about potential long-term patterns of bonding-related and dyad-specific oxytocin effects within highly affiliative and cooperative social groups. Our aim was to investigate whether bonding-related oxytocin signatures linked to dyadic affiliation are present in family groups of cooperatively breeding marmoset monkeys (Callithrix jacchus) that show high levels of cohesion and cooperation. In 30 dyads from four family groups and one pair, we measured urinary baseline oxytocin over six weeks and analyzed the link to bond strength (mean dyadic affiliation). Strongly bonded dyads showed synchronized longitudinal fluctuations of oxytocin, indicating that dyad-specific oxytocin effects can also be traced in the group context and in an interdependent species. We discuss these results in light of the potential function of differentiated relationships between marmoset dyads other than the breeding pair, and the role of oxytocin as a mediator for social bonding.

Marmosets as model species in neuroscience and evolutionary anthropology.

Marmosets are increasingly used as model species by both neuroscientists and evolutionary anthropologists, but with a different rationale for doing so. Whereas neuroscientists stress that marmosets share many cognitive traits with humans due to common descent, anthropologists stress those traits shared with marmosets - and callitrichid monkeys in general - due to convergent evolution, as a consequence of the cooperative breeding system that characterizes both humans and callitrichids. Similarities in socio-cognitive abilities due to convergence, rather than homology, raise the question whether these similarities also extend to the proximate regulatory mechanisms, which is particularly relevant for neuroscientific investigations. In this review, we first provide an overview of the convergent adaptations to cooperative breeding at the psychological and cognitive level in primates, which bear important implications for our understanding of human cognitive evolution. In the second part, we zoom in on two of these convergent adaptations, proactive prosociality and social learning, and compare their proximate regulation in marmosets and humans with regard to oxytocin and cognitive top down regulation. Our analysis suggests considerable similarity in these regulatory mechanisms presumably because the convergent traits emerged due to small motivational changes that define how pre-existing cognitive mechanisms are quantitatively combined. This finding reconciles the prima facie contradictory rationale for using marmosets as high priority model species in neuroscience and anthropology.