Title: Social Structure Predicts Eye Contact Tolerance in Nonhuman Primates: Evidence from a Crowd-Sourcing Approach Authors: Ethan G. Harrod, Christopher L. Coe, Paula M. Niedenthal 5 Department of Psychology, University of Wisconsin-Madison Correspondence to: [email protected], [email protected], and [email protected] Abstract: In most primates, eye contact is an implicit signal of threat, and often signals social status and imminent physical aggression. However, in humans and the more gregarious species 10 of nonhuman primates, eye contact is more tolerated and used to communicate emotional and mental states. What accounts for the variation in this critical social behavior across primate species? We crowd-sourced primatologists and found a strong positive correlation between eye contact tolerance and primate social structure. In more egalitarian social structures, eye contact is more tolerated. In addition to constituting the first generalizable demonstration of this 15 relationship, our findings can inform the related question of why eye contact is deferentially avoided in some human cultures, while in others eye contact is both frequent and even encouraged. 1 Being looked at elicits a reflexive, involuntary response. Humans can detect that they are the target of another’s gaze through subcortical neural pathways, even without conscious awareness (1). Detection of direct gaze in turn triggers a cascade of activation in social cognition centers of the brain that underlie the self-conscious state of arousal and endocrine responses we 5 experience as the “feeling of being looked at” (2). Achieving eye contact with another has important significance both for the sender of this social signal and the recipient. Among most primates, direct gaze can serve as an explicit and implicit signal of threat or dominance, suggesting that overt physical aggression might soon follow (3-9). It is thus often associated with social status and may elicit an avoidance response in a subordinate individual or an antagonistic 10 counter response by another higher in the social hierarchy (3, 5, 10). On the other hand, humans and members of some of the more gregarious primate species, while still recognizing the context in which direct gaze signals threat, are more tolerant of direct gaze and respond by making eye contact (7, 10-17). In these species, eye contact may be used to communicate complex emotional and mental states and to establish affiliative bonds (7, 14, 15, 17, 18). What accounts for the fact 15 that in some nonhuman primates direct gaze typically signals threat and does not invite eye contact, while in other species eye contact is important for nuanced features of a social interaction? We conducted an investigation into the relationship between tolerance of eye contact and the nature of the social structure in which different primate species live. In order to collect data 20 that spanned numerous primate species, we used novel crowd-sourcing method. Specifically, primatologists were surveyed about the social behavior of the species that had been the subject of their scientific research for many years. In spite of some limitations (discussed below), the method offers the benefits of control over definitions and responses that represent numerous observations over a career rather than during a single experiment or time period. We 25 hypothesized that eye contact is tolerated more in species that live in egalitarian groups with more social fluidity as compared to hierarchical groups with more rigid social stratification. Our a priori predictions were based on extant theory in social and cognitive psychology and derived from numerous previous ethological studies of nonhuman primates. Eye Contact 30 Eye contact, defined as the prolonged looking of two animals directly into each other’s eyes (13), is distinct from gaze following and joint attention, which has been defined as the ability to detect and interpret gaze and to mutually attend to an object or cooperate on a task (10, 19, 20, 21). While eye contact and gaze following are undoubtably related, they serve different and distinct purposes among primates. Additionally, we recognize and expect that the use of gaze 35 following and joint attention in one species may not directly align with the use of eye contact in that same species. Eye Contact in Human Primates Among humans, there are clear distinctions in how eye contact is used and tolerated, and these behaviors are socialized and entrained from early childhood. The initial basis for making 40 eye contact starts soon after birth, with the ability to distinguish between direct and averted gaze arising in infants within 2-5 days after delivery. By 4 months of age, faces with a direct, as compared to averted, gaze elicit more attention and result in enhanced neural processing in infants (22). Across cultures, eye contact between mothers and infants is initially actively sought and sustained (23, 24) and plays an important role in bonding with parents. However, as infants 2 develop, the caregivers socialize their eye gaze patterns to encourage patterns of eye contact that are more congruent with culture-specific norms and expectations (23, 25-27). The result of this shaping of looking behavior is that the meaning, use, and tolerance of eye contact in adults differs across cultures. For example, the frequency and duration of eye 5 contact is lower in East Asian than in Western European and American cultures (13, 28, 29). Japanese adults engage in significantly less eye contact than do either Canadians or Trinidadians during face-to-face interactions (30, 31). There is also cultural variation in how eye contact is interpreted, with East Asians, as compared to Western Europeans, viewing eye contact as more aggressive and signifying that the person is less approachable (28-30). In addition, in many 10 Asian as well as Middle Eastern cultures, the use of eye contact and staring is also a way to convey social status and rank, obliging subordinate individuals to avert or lower their gaze. Thus, there appear to be both universal and specific aspects to the meaning of direct gaze and eye contact which may correspond to how eye contact is used among nonhuman primates in more hierarchical versus egalitarian social systems. 15 Although the terms hierarchical and egalitarian as we understand them in the context of nonhuman primates are not commonly used to describe human social structures, we can still draw connections between nonhuman and human social structures by references to the strategies for accomplishing the social tasks common to group living within these structures. Such tasks include negotiating one’s status in the social hierarchy, affiliative behaviors like consolation and 20 trust building, and responding to unfamiliar and unrelated conspecifics. Human cultures and societies with tighter social norms and more rigid status social hierarchies employ strategies that are comparable to those used in hierarchical social structures seen in nonhuman primates. Conversely, cultures in which norms are looser and less based in explicit assertion and maintenance of social status, can be likened to the social structures of more egalitarian primates, 25 such as the bonobo communities and muriqui troops. Eye Contact in Nonhuman Primates The idea that eye contact conveys primarily an agonistic message in nonhuman primates has been supported by many experimental studies in rhesus macaques using photographs of direct gazing monkeys or human faces with, wide-open eyed, intentional looking as threatening 30 stimuli (20, 32, 33). However, the conclusions from this research generalize to other primates, including many prosimians, most monkeys, and the great apes, all of which use a directed stare as a threatening signal (10, 34, 35). Especially among the species that live in groups with clearer dominance hierarchies, the use of direct gaze is a means to convey higher social status and to exert control over the behavior and proximity of subordinates. In contrast, eye contact is used 35 infrequently and typically not prolonged in joint action for many of these species (10, 15, 16, 19, 36). As an example, rhesus macaques typically make eye contact in order to impose their social standing or to challenge a conspecific, most often leading to avoidance and spatial displacement by the subordinate (6, 15, 18, 35). Even when engaging in prosocial behaviors such as reconciliation and consolation, rhesus macaques often avoid eye contact (17, 18). Similar 40 findings have been obtained in the mostly solitary and territorial mouse lemurs, with prolonged eye contact initiating aggressive encounters, but avoided during affiliative behaviors or when first encountering an unfamiliar conspecific (34). In contrast, the more gregarious bonobos rarely engage in affiliative behaviors without first establishing eye contact (16, 35, 37). In bonobos, marmosets that live in small family 3 groups, and other species of macaques, such as the stumptailed and tonkean macaques, eye contact is made more regularly in order to initiate non-agonistic social interactions, establish and maintain affiliative bonds, to initiate play, and serves to aid in cohesion when animals are searching for food and resources, even while a more prolonged direct stare is maintained in the 5 behavioral repertoire as a threat signal (16, 17, 38, 39, 40). Among nonhuman primates, the distinction between the use of eye contact as a threat or an affiliative signal appears to follow a logical pattern that is congruent with both their phylogenetic relationships and the nomenclature used to categorize different social group structures (10). Thus, rather than just focusing on gaze behavior in one type of primate and 10 ascribing it to inherent dispositions of functions within that particular species (18), we sought a larger, overarching and parsimonious framework that could better inform research on this communicative behavior among humans. Results As hypothesized, there was a strong positive correlation between the rating of eye contact 15 tolerance and the typical group social structure exhibited by the 19 species sampled, r = .771, t(17) = 4.99, p < .001 (Fig.