Monkeys shifted their focus to the social domain and became socially more selective

As humans age, they become more selective regarding their personal goals [] and social partners []. Whereas the selectivity in goals has been attributed to losses in resources (e.g., physical strength) [], the increasing focus on emotionally meaningful partners is, according to socioemotional selectivity theory, driven by the awareness of one’s decreasing future lifetime []. Similar to humans, aging monkeys show physical losses [] and reductions in social activity []. To disentangle a general resource loss and the awareness of decreasing time, we combined field experiments with behavioral observations in a large age-heterogeneous population of Barbary macaques (Macaca sylvanus) at La Forêt des Singes. Novel object tests revealed a loss of interest in the nonsocial environment in early adulthood, which was modulated by the availability of a food reward. Experiments using vocal and visual representations of social partners indicated that monkeys maintained an interest in social stimuli and a preferential interest in friends and socially important individuals into old age. Old females engaged in fewer social interactions, although other group members continued to invest in relationships with them. Consequently, reductions in sociality were not due to a decrease in social interest. In conclusion, some of the motivational shifts observed in aging humans, particularly the increasing focus on social over nonsocial stimuli, may occur in the absence of a limited time perspective and are most likely deeply rooted in primate evolution. Our findings highlight the value of nonhuman primates as valuable models for understanding human aging [].

On the incomplete architecture of human ontogeny. Selection, optimization, and compensation as foundation of developmental theory.

In order to determine potential age-associated decreases in sociality [], we conducted focal observation of females (n = 45) of two groups (Grand Bassin [GB] and Petit Bassin [PB]) [] ( Supplemental Experimental Procedures , section 6). With increasing age, females spent less time actively grooming and groomed fewer adult partners ( Figure 4 Supplemental Experimental Procedures , section 8). For the females of the GB group (n = 26), we additionally determined the frequency of affiliative contact. Older females had lower frequencies of affiliative interactions (LM with log-transformed response: F= 9.45, p < 0.01) and a lower number of adult partners (LM: F= 5.52, p < 0.05) than younger ones. The time females received grooming and the number of individuals by whom they were groomed did not vary with age, however ( Figure 4 ). An inspection of the grooming data revealed no clear pattern for the partners of old females (>19 years old; n = 16). The females did not show an increasing focus on relatives with age, as there were only three daughters or sons among the top two grooming partners of the old females.

Depicted are the estimated (mixed additive distributional regression, MADR) 2.5%, 10%, 25%, 75%, 90%, and 97.5% quantiles (shaded areas) and expected values (line) of the respective response distribution over the domain of age (n observations = 68, n subjects = 45). Pairs of values with exclusive expected values and inner 97.5% quantile intervals reveal strong evidence for age-related distributional differences. With increasing age, female Barbary macaques engaged less in active grooming (A) and had a lower number of adult partners they actively groomed (active partners) (B). There was no substantial change in the time females received grooming (C) or the number of adult partners by which females were groomed (passive partners) (D).

Post-conflict affiliation in Barbary macaques is influenced by conflict characteristics and relationship quality, but does not diminish short-term renewed aggression.

In order to determine potential age-related changes in social interest, we presented male and female subjects with portrait photographs [] of newborn Barbary macaques, a close friend or a non-friend ( Supplemental Experimental Procedures , sections 3 and 4). Note that in this species, females maintain close bonds with both related and unrelated females [], and males interact with infants remarkably frequently []. The close friend was defined as the female in the group with which a subject exchanged most affiliative interactions during group scans, whereas the non-friend was a female with whom no affiliative interactions were recorded. For female subjects, we additionally conducted playback experiments [] in which we played recruitment screams elicited in agonistic contexts [] from close partners and non-friends ( Supplemental Experimental Procedures , section 5). In all experiments, stimuli that represented socially important individuals elicited stronger responses than those representing other group members ( Figure 3 ). The preferential interest in photographs of important partners remained constant into old age (LMMs: males, n subjects = 44 in one to three experimental conditions, n trials = 85; age × partner type, χ= 1.92, df = 2, p > 0.1; females, n subjects = 54 in one to three experimental conditions, n trials = 127; age × partner type, χ= 1.50, df = 2, p > 0.1), as did females’ preferential interest in recruitment screams for close partners (permutation test of LMM: n subjects = 47 in one to two experimental conditions, n trials = 69; age × partner type, p > 0.1). Moreover, there was no general effect of age on looking time to portrait photographs (males, χ= 0.89, p > 0.1; females, χ= 1.46, p > 0.1) or on female responses toward recruitment screams (permutation test of LMM: p > 0.1). As a further measure of social interest, we quantified the frequency at which Barbary macaques emit vocalizations while observing interactions of conspecifics [] for a subset of focal females (n = 26) ( Supplemental Experimental Procedures , section 6). We found no effect of age on the frequency females emitted vocalizations in response to infant interactions (linear model [LM]: p > 0.1) or conflicts (LM: p > 0.1) among third parties ( Supplemental Experimental Procedures , section 7).

(C) Females looked longer toward the loudspeaker after playback of close friend’s (CF) compared to non-friend’s (NF) recruitment screams (permutation test of LMM with log-transformed [after adding c = 1] response: n subjects = 47 in one to two experimental conditions, n trials = 69). See also Movie S7

(B) Females spent more time looking at photographs (LMM with log-transformed response: n subjects = 54 in one to three experimental conditions, n trials = 127) depicting an infant of conspecifics (I) (estimate = −0.27, SE = 0.08) or a close friend (CF) (estimate = −0.18, SE = 0.09) compared to a non-friend (NF). See also Movie S6

(A) Males spent more time looking at photographs (LMM with log 10 -transformed response: n subjects = 44 in one to three experimental conditions, n trials = 85) depicting an infant of conspecifics (I) than a close friend (CF) (estimate = −0.32, SE = 0.09) or a non-friend (NF) (estimate = −0.22, SE = 0.09).

Do Barbary macaques ‘comment’ on what they see? A first report on vocalizations accompanying interactions of third parties.

Post-conflict affiliation in Barbary macaques is influenced by conflict characteristics and relationship quality, but does not diminish short-term renewed aggression.

To assess potential age-related changes in Barbary macaques’ interest to engage with the nonsocial environment, we presented male and female subjects with three different types of novel objects: animal toys, a cube filled with colorful plastic pieces in a viscose liquid, and an opaque tube closed with soft tissue at both ends and baited with a food reward ( Supplemental Experimental Procedures , sections 1 and 2). Monkeys lost interest in toys in early adulthood but did not show further age-related variation ( Figure 1 ). The interest in the baited tube was generally higher than in the other toys, and the exploration time ( Figure 1 ) and likelihood of physical manipulation in this task were reduced only for individuals >24 years old (generalized linear mixed model [GLMM]: n subjects = 98 in one to three experimental conditions, n trials = 202; age × novel object type, χ= 8.85, degrees of freedom [df] = 2, p < 0.05). The latency to open the tube steadily increased from young adulthood on, however, and subjects >19 years old were unable to retrieve the reward ( Figure 2 ).

Old subjects (>19 years) failed to retrieved the peanut out of the tube (generalized linear model [GLM]: n trials and subjects = 53; age, χ= 11.81, df = 1, p < 0.001; sizing of points corresponds to number of subjects [1–6] tested at a certain age) (A), and the latency to open the tube steadily increased from young adulthood on (Spearman-rank correlation: n trials and subjects = 21, rho = 0.61, p < 0.01) (B). See also Movies S3 S4 , and S5

Barbary macaques’ exploration times of animal toys (A), a cube (B), and an opaque tube baited with peanuts (C), indicating that the age-related change in interest during adulthood was modulated by the potential availability of a food reward (permutation test of linear mixed model [LMM]: n trials = 192, n subjects = 93; age × novel object type, p < 0.05). See also Movies S1 S2 , and S4

Discussion

17 Blakemore S.-J.

Robbins T.W. Decision-making in the adolescent brain. 18 Lucas R.E.

Donnellan M.B. Personality development across the life span: longitudinal analyses with a national sample from Germany. 17 Blakemore S.-J.

Robbins T.W. Decision-making in the adolescent brain. 19 Spear L.-P. Adolescent brain development and animal models. We found a sharp loss of monkeys’ interest in the nonsocial environment in young adulthood. This mirrors findings for humans, in which adolescents also show a higher degree of novelty and sensation seeking than adults, leading to a greater propensity to take risks [], whereas the eagerness for new experiences declines across adulthood []. Thus, the nonlinear development of the internal reward system, which has been associated with risk taking in adolescence [], is most likely a shared and ancestral trait []. Notably, the potential availability of a food reward strongly influenced the monkeys’ approach behavior: except for very old individuals, monkeys continued to explore the tube, albeit with diminishing success. Whether this is due to a loss of cognitive competence or due to motor impairments remains an issue for further investigation.

20 Cummings E.

Henry W.E. Growing Old: The Process of Disengagement. For the older monkeys, we found a striking dissociation between the diminished social activity and a narrowing social network on the one hand, and the continued interest in social information on the other. The reduction in social activity was apparently driven by the old individuals themselves, whereas they were not less attractive to other group members. The keen interest of old individuals in social information challenges the notion that their shrinking social activity and social networks are a result of a general loss of social interest []. In contrast to our expectations, old individuals also maintained a basal interest in social information involving non-friends. In other words, we did not observe a relative increase in interest in socially important partners. In sum, the increased social selectivity at the behavioral level is not based on shifts in social interest.

1 Riediger M.

Freund A.M. Focusing and restricting: two aspects of motivational selectivity in adulthood. 3 Baltes P.B. On the incomplete architecture of human ontogeny. Selection, optimization, and compensation as foundation of developmental theory. 21 Ebner N.C.

Freund A.M.

Baltes P.B. Developmental changes in personal goal orientation from young to late adulthood: from striving for gains to maintenance and prevention of losses. 22 Freund A.M. Age-differential motivational consequences of optimization versus compensation focus in younger and older adults. 4 Roth G.S.

Mattison J.A.

Ottinger M.A.

Chachich M.E.

Lane M.A.

Ingram D.K. Aging in rhesus monkeys: relevance to human health interventions. For humans, the increased selectivity in personal goals [] has been linked to losses in resources (e.g., declines in some physical and cognitive abilities) []. Increasing resource losses are associated with a shift in motivational orientation across adulthood, such that younger adults are more oriented toward achieving gains, whereas older adults are more oriented toward maintaining functioning and avoiding losses []. Future studies should aim to clarify to which degree the decrease in active social time is driven by energy constraints—more specifically, to which degree the reduction in activity is the result of reduced energy intake and/or metabolic deficiencies []. In addition, the valuation of specific social interactions or activities might change, possibly due to differential internal reward patterns.

5 Corr J. Social behavior in aged rhesus macaques. 23 Shutt K.

MacLarnon A.

Heistermann M.

Semple S. Grooming in Barbary macaques: better to give than to receive?. 24 Silk J.B.

Alberts S.C.

Altmann J. Social bonds of female baboons enhance infant survival. 25 Silk J.B.

Beehner J.C.

Bergman T.J.

Crockford C.

Engh A.L.

Moscovice L.R.

Wittig R.M.

Seyfarth R.M.

Cheney D.L. Strong and consistent social bonds enhance the longevity of female baboons. Counter to our expectations, we observed that other group members continued to groom older females [], raising questions about the value of social relationships per se. For Barbary macaques, there is some evidence that grooming lowers stress levels in the groomer [], which may account for the continued grooming of non-reciprocating older females at the proximate level. At the ultimate level, it has been shown that female monkeys that maintain strong bonds experience higher infant survival [] and an enhanced longevity [], indicating that the maintenance of strong bonds has been selected for. Thus, social bonds may acquire an intrinsic value, so that the animals continue to invest into relations with older individuals although they may only provide marginal benefits to them.

Taking these data together, we found evidence for higher selectivity in aging Barbary macaques. Their interest in novel objects waned first, followed by withdrawal from social interactions and a narrowing in network size, and finally a reduction in problem solving even with the prospect of a reward, whereas attentiveness to social information remained stable into old age.

2 Carstensen L.L.

Isaacowitz D.M.

Charles S.T. Taking time seriously. A theory of socioemotional selectivity. 2 Carstensen L.L.

Isaacowitz D.M.

Charles S.T. Taking time seriously. A theory of socioemotional selectivity. 2 Carstensen L.L.

Isaacowitz D.M.

Charles S.T. Taking time seriously. A theory of socioemotional selectivity. 26 Fredrickson B.L.

Carstensen L.L. Choosing social partners: how old age and anticipated endings make people more selective. What are the implications of these results for socioemotional selectivity theory (SST) []? According to SST, the prioritization of emotional goals and a narrowing in network in particular results from subjective impending endings []. In humans, the awareness of limited lifetime clearly has a strong impact on one’s preferences and goals [], as young adults who are struck by terminal illness or who are confronted with a geographic relocation scenario experience similar shifts in motivation and preferences as aged individuals []. This does not rule out the possibility that physiological decline also contributes to shifting preferences in older humans.

Our data provide evidence that in the absence of an awareness of limited lifetime, nonhuman primates experience an increasing focus on social over nonsocial stimuli and a reduction in social investment with age. Accordingly, in aging humans, both ancestral motivational shifts and the awareness of one’s increasingly limited remaining lifetime most likely contribute to shifting preferences and goals.