Early predictors of impaired social functioning in male rhesus macaques (Macaca mulatta)

Autism spectrum disorder (ASD) is characterized by social cognition impairments but its basic disease mechanisms remain poorly understood. Progress has been impeded by the absence of animal models that manifest behavioral phenotypes relevant to ASD. Rhesus monkeys are an ideal model organism to address this barrier to progress. Like humans, rhesus monkeys are highly social, possess complex social cognition abilities, and exhibit pronounced individual differences in social functioning. Moreover, we have previously shown that Low-Social (LS) vs. High-Social (HS) adult male monkeys exhibit lower social motivation and poorer social skills. It is not known, however, when these social deficits first emerge. The goals of this study were to test whether juvenile LS and HS monkeys differed as infants in their ability to process social information, and whether infant social abilities predicted later social classification (i.e., LS vs. HS), in order to facilitate earlier identification of monkeys at risk for poor social outcomes. Social classification was determined for N = 25 LS and N = 25 HS male monkeys that were 1–4 years of age. As part of a colony-wide assessment, these monkeys had previously undergone, as infants, tests of face recognition memory and the ability to respond appropriately to conspecific social signals. Monkeys later identified as LS vs. HS showed impairments in recognizing familiar vs. novel faces and in the species-typical adaptive ability to gaze avert to scenes of conspecific aggression. Additionally, multivariate logistic regression using infant social ability measures perfectly predicted later social classification of all N = 50 monkeys. These findings suggest that an early capacity to process important social information may account for differences in rhesus monkeys’ motivation and competence to establish and maintain social relationships later in life. Further development of this model will facilitate identification of novel biological targets for intervention to improve social outcomes in at-risk young monkeys

Contra-hierarchical aggression among female rhesus macaques (Macaca mulatta)

Among rhesus macaques, bi-directional aggression may occur between animals with shifting or ambiguous ranks, or between those whose relative ranks are well established. Factors that influence the latter case (here termed "insubordinate aggression") are not well understood. These factors are of interest because insubordinate aggression may be associated with stability in dominance relationships, and stability in dominance relationships is critically related to group stability. We hypothesized that in well-established female dominance relationships, the likelihood of insubordination during conflicts is influenced by characteristics of both opponents. Multivariate analysis of 11,591 dyadic conflicts among females in six captive rhesus groups shows that dyadic and individual characteristics related to weight, rank, age, and access to social support affect the likelihood of insubordinate aggression. As expected, insubordinate aggression is less likely to occur among dyads with high disparity in weight. The effects of age, rank, and access to social support are more complex. Increasing subordinate age is associated with increased modulation of insubordinate aggression according to opponent age. Age-based deference, i.e. suppression of insubordination associated with opponent age, decreases with increasing age of the lower-ranking opponent. Similarly, dyadic rank disparity has different effects on insubordination rate according to the age of the subordinate opponent. As females age, their likelihood of insubordination is less dependent on the degree to which they are outranked by their opponent. Also, the lower-ranking opponent's level of social support significantly affects her likelihood of insubordination, but the dominant animal's level of social support does not affect her likelihood of receiving insubordination. We predicted that for the lower-ranking opponent, having many maternal kin would promote insubordinate behavior, whereas for the higher-ranking opponent, having many maternal kin would inhibit insubordination. However, our results show that the dominant's matriline size has no effect on her likelihood of receiving insubordination. Further, matriline size has the opposite of the predicted effect for subordinates--subordinates with many maternal kin are significantly less likely to be insubordinate than those with few kin. We propose some possible explanations for this, which will require further investigation. Taken together, this research suggests that females gauge their degree of deference to dominants based on their own characteristics relative to their opponent's, taking into account size, age and weight differences as well as their own access to social support. Features of subordinate animals emerge as more important than those of dominants in determining the likelihood of insubordinate aggression in dyadic conflicts. Understanding determinants of insubordination will contribute to management practices aimed at maintenance of group stability, as the ultimate act of insubordinate aggression, social overthrow, poses a major welfare and management problem

Human–wildlife conflict: Proximate predictors of aggression between humans and rhesus macaques in India

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co-inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3-month study of four free-ranging populations of rhesus macaques in Dehradun, India from October-December 2012, using event sampling to record all instances of human-macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one another's behavior. Mitigation of human-primate conflict, and indeed other types of human-wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other

Prevalence of enteric bacterial parasites with respect to anthropogenic factors among commensal rhesus macaques in Dehradun, India

There has been a recent surge in research on primate infectious disease ecology. Two major areas remain relatively unaddressed to date-the prevalence of enteric bacterial parasites and the role of anthropogenic environmental factors in parasite acquisition in commensally living primate populations. In this preliminary assessment, we address both these gaps by assessing the prevalence, and the role of anthropogenic factors in shaping this prevalence, of three enteric bacterial parasites-E . coli O157:H7, Salmonella sp., Shigella sp.-across populations of rhesus macaques (M. mulatta) that live commensally with humans in Dehradun, northern India. Across 10-week study period, we collected data on (1) human-macaque behavioral interactions, (2) macaque and human demographic and activity scans, and (3) macaque fecal samples from the environment at four different locations in Dehradun. Biochemical tests and morphology-based confirmations clearly established the presence of all three enteric bacterial parasites in rhesus macaques. Overall prevalence ranged from 2 to 5 %, with Shigella sp. being the most prevalent. Regression analyses linking anthropogenic factors to bacterial prevalence showed a positive association between rates of macaques eating human garbage and E. coli O157:H7 (β = 0.23, p = 0.083), but a negative association with Salmonella sp. (β = -0.17, p = 0.026). Rather, the prevalence of Salmonella sp. was positively linked to rates of macaque eating provisioned food (β = 0.0012, p = 0.058). Finally, we found no relationship between anthropogenic factors and the prevalence of Shigella sp. Our findings establish the prevalence of enteric bacterial parasites in commensal populations of primates and suggest that although anthropogenic factors are linked to bacterial prevalence, the nature of the relationships may depend on the socioecological/foraging strategies of macaques and the food sources that facilitate the environmental survival of particular types of enteric bacteria over others

Visual attention distribution during the response to conspecific social stimuli test.

<p>Infants later classified as Low-Social (LS) showed a lower rate of gaze aversion to aggression, and looked at the social stimuli less frequently than infants later classified as High-Social (HS), but both monkey groups spent a greater percentage of time looking at aggressive vs. neutral behavioral displays. (a) The rate of gaze aversion differed between infants later classified as LS and HS only during the aggression exemplars. (b) The rate of looking also differed between infants later classified as LS and HS only during the aggression exemplars. Infants later classified as HS, but not LS, differed in their rate of looking between aggression and neutral exemplar types. (c) The percentage of time spent looking at aggression did not differ between monkey groups, and both groups spent more time looking at aggressive displays over neutral ones.</p

Preference for novel faces on the face recognition memory test.

<p>During recognition trials, infants later classified as Low-Social (LS) did not show a preference above chance for the novel face (percentage of time looking on target directed to the novel face) (97.5% CI: 43.6% - 53.3%); whereas infants later classified as High-Social (HS) did (97.5% CI: 51.6% - 61.0%). Data are plotted as LSM +/- SE. Effect size is given in the text as partial eta ().</p

Face recognition memory test.

<p>During a familiarization trial (a) infants were presented with two identical unfamiliar rhesus monkey faces. During the subsequent recognition trial (b) infants were presented with the same rhesus monkey face from the immediately preceding familiarization trial as well as a novel face.</p

Network Stability Is a Balancing Act of Personality, Power, and Conflict Dynamics in Rhesus Macaque Societies

Stability in biological systems requires evolved mechanisms that promote robustness. Cohesive primate social groups represent one example of a stable biological system, which persist in spite of frequent conflict. Multiple sources of stability likely exist for any biological system and such robustness, or lack thereof, should be reflected and thus detectable in the group's network structure, and likely at multiple levels. Here we show how network structure and group stability are linked to the fundamental characteristics of the individual agents in groups and to the environmental and social contexts in which these individuals interact. Both internal factors (e.g., personality, sex) and external factors (e.g., rank dynamics, sex ratio) were considered from the level of the individual to that of the group to examine the effects of network structure on group stability in a nonhuman primate species. The results yielded three main findings. First, successful third-party intervention behavior is a mechanism of group stability in rhesus macaques in that successful interventions resulted in less wounding in social groups. Second, personality is the primary factor that determines which individuals perform the role of key intervener, via its effect on social power and dominance discrepancy. Finally, individuals with high social power are not only key interveners but also key players in grooming networks and receive reconciliations from a higher diversity of individuals. The results from this study provide sound evidence that individual and group characteristics such as personality and sex ratio influence network structures such as patterns of reconciliation, grooming and conflict intervention that are indicators of network robustness and consequent health and well-being in rhesus macaque societies. Utilizing this network approach has provided greater insight into how behavioral and social processes influence social stability in nonhuman primate groups