Primates frequently form affiliative relationships that have important fitness consequences. Affiliative relationships between unrelated males and females are ubiquitous in humans but are not widely reported in humans' closest living relatives, chimpanzees (Pan troglodytes). Instead, adult male chimpanzees are extremely aggressive to females, using the aggression to coerce females to mate with them. Adolescent male chimpanzees are physically and socially immature and unable to use aggression toward females in the same way as adult males. Instead, adolescent males might build affiliative relationships with females as an alternative tactic to increase their chances of mating and reproducing. To investigate this possibility, we recorded social interactions between 20 adolescent and 10 young adult males and 78 adult female chimpanzees over 2 years at Ngogo in Kibale National Park, Uganda. Analyses using grooming and proximity as assays revealed that adolescent and young adult males formed differentiated, affiliative relationships with females. These relationships were as strong as the bonds young males formed with maternal kin and unrelated males and increased in strength and number as males aged and started to dominate females. Male-female relationships extended outside the immediate context of mating. Although males affiliated slightly more often with females when they were cycling, they also did so when females were pregnant and nursing young infants. Males and females who formed bonds reassured each other, looked back and waited for each other while traveling, and groomed more equitably than other male-female pairs, even after the time they spent together in association and the female's reproductive state were taken into account. Despite the affiliative nature of these relationships, adolescent and young adult males selectively targeted their female partners for aggression. These findings provide new insights into the evolution of social bonds between human females and males, which can involve both affiliation and coercive violence.
Obligation as defined by Tomasello requires mutually capable parties, but one-sided caregiver relationships reveal its developmental and evolutionary precursors. Specifically, “coercive” emotions may prompt protective action by caregivers toward infant primates, and infants show distress toward caregivers when they appear to violate expectations in their relationships. We argue that these early social-relational expectations and emotions may form the base of obligation.
Mothers provide indispensable care for infants in many mammalian species. In some long-lived species, the maternal-offspring bond persists after infancy with mothers continuing to provide resources and social support to their adult progeny. Maternal presence is associated with fitness benefits through adolescence for male chimpanzees despite the fact that mature males dominate females and form their strongest bonds with other males. How mothers support grown sons is unknown, because few studies have examined developmental shifts in mother-son relationships during adolescence and adulthood. We investigated social interactions between 29 adolescent (9-15 years) and young adult male (16-20 years) chimpanzees and their mothers at Ngogo in Kibale National Park, Uganda over 3 years. All males under 12 years old had their mother as their top grooming and proximity partner, as did one-third of the young adult males. As males grew older, the amount of time they associated with, maintained proximity to, groomed with, and kept track of their mothers while traveling decreased. When males were together in the same party as their mothers, however, young adult males affiliated with their mothers as frequently as did adolescent males, with sons initiating the majority of these interactions. In contrast to adult sons, however, adolescent sons became distressed when separated from mothers and relied on their mothers for agonistic support and reassurance after conflicts. These findings indicate that the chimpanzee maternal – offspring bond continues but changes through adolescence and adulthood, with mothers remaining occasional social companions for most adult sons and frequent companions for some.
Respiratory viruses of human origin infect wild apes across Africa, sometimes lethally. Here we report simultaneous outbreaks of two distinct human respiratory viruses, human metapneumovirus (MPV; Pneumoviridae: Metapneumovirus) and human respirovirus 3 (HRV3; Paramyxoviridae; Respirovirus, formerly known as parainfluenza virus 3), in two chimpanzee (Pan troglodytes schweinfurthii) communities in the same forest in Uganda in December 2016 and January 2017. The viruses were absent before the outbreaks, but each was present in ill chimpanzees from one community during the outbreak period. Clinical signs and gross pathologic changes in affected chimpanzees closely mirrored symptoms and pathology commonly observed in humans for each virus. Epidemiologic modelling showed that MPV and HRV3 were similarly transmissible (R0 of 1.27 and 1.48, respectively), but MPV caused 12.2% mortality mainly in infants and older chimpanzees, whereas HRV3 caused no direct mortality. These results are consistent with the higher virulence of MPV than HRV3 in humans, although both MPV and HRV3 cause a significant global disease burden. Both viruses clustered phylogenetically within groups of known human variants, with MPV closely related to a lethal 2009 variant from mountain gorillas (Gorilla beringei beringei), suggesting two independent and simultaneous reverse zoonotic origins, either directly from humans or via intermediary hosts. These findings expand our knowledge of human origin viruses threatening wild chimpanzees and suggest that such viruses might be differentiated by their comparative epidemiological dynamics and pathogenicity in wild apes. Our results also caution against assuming common causation in coincident outbreaks.
When their mothers die, chimpanzees often adopt younger vulnerable siblings who survive with their care. This phenomenon has been widely reported, but few studies provide details regarding how sibling relationships change immediately following the deaths of their mothers. A disease outbreak that killed several females at Ngogo in Kibale National Park, Uganda, furnished an opportunity to document how maternal death influenced the social relationships of siblings. We describe social interactions between four adolescent and young adult males and their younger immature maternal siblings 9 months before and 8 months after their mothers died. We also show how the behavior of individuals in the four recently orphaned sibling pairs contrasts to the behavior displayed by chimpanzees in 30 sibling pairs whose mothers were alive. Following the death of their mothers, siblings increased the amount of time they associated, maintained spatial proximity, groomed, reassured, and consoled each other. During travel, younger orphans followed their older siblings, who frequently looked back and waited for them. Both siblings showed distress when separated, and older siblings demonstrated heightened vigilance in dangerous situations. Chimpanzees who were recently orphaned interacted in the preceding ways considerably more than did siblings whose mothers were alive. These findings suggest that siblings provide each other support after maternal loss. Further research is needed to determine whether this support buffers grief and trauma in the immediate aftermath of maternal loss and whether sibling support decreases the probability that orphans will suffer long-term consequences of losing a mother if they survive.
Dominance hierarchies are a prominent feature of the lives of many primate species. These hierarchies have important fitness consequences, as high rank is often positively correlated with reproduction. Although adult male chimpanzees strive for status to gain fitness benefits, the development of dominance relationships is not well understood. While two prior studies found that adolescent males do not display dominance relationships with peers, additional research at Ngogo in Kibale National Park, Uganda, indicates that adolescents there form a linear dominance hierarchy. These conflicting findings could reflect different patterns of rank acquisition across sites. An alternate possibility arises from a recent re-evaluation of age estimates at Ngogo and suggests that the report describing decided dominance relationships between adolescent males may have been due to the accidental inclusion of young adult males in the sample. To investigate these issues, we conducted a study of 23 adolescent male chimpanzees of known age during 12 months at Ngogo. Adolescent male chimpanzees exchanged pant grunts, a formal signal of submission, only 21 times. Recipients of pant grunts were late adolescent males, ranging between 14 and 16 years old. In contrast, younger adolescent males never received pant grunts from other males. Aggression between adolescent males was also rare. Analysis of pant grunts and aggressive interactions did not produce a linear dominance hierarchy among adolescent males. These data indicate that adolescent male chimpanzees do not form decided dominance relationships with their peers and are consistent with the hypothesis that the hierarchy described previously at Ngogo resulted from inaccurate age estimates of male chimpanzees. Because dominance relationships develop before adulthood in other primates, our finding that adolescent male chimpanzees do not do so is surprising. We offer possible explanations for why this is the case and suggest future studies that may help clarify the matter.
Among some haplorhine primates, including humans, relaxed yawns spread contagiously. Such contagious yawning has been linked to social bonds and empathy in some species. However, no studies have investigated contagious yawning in strepsirhines. We conducted an experimental study of contagious yawning in strepsirhines, testing ring-tailed and ruffed lemurs (n = 24) in a paradigm similar to one that has induced contagious yawning in haplorhines. First, in a control experiment, we investigated whether lemurs responded to projected video content in general (experiment 1). We showed them two videos to which we expected differential responses: one featured a terrestrial predator and the other a caretaker holding food. Next, to test for yawn contagion, we showed individual lemurs life-size video projections of groupmates and conspecific strangers yawning, and control footage of the same individuals at rest (experiment 2). Then, to examine whether a group context might enhance or allow for contagion, we exposed subjects to the same videos in a group setting (experiment 3). Lemurs produced alarm vocalizations and moved upward while viewing the predator, but not the caretaker, demonstrating that they do perceive video content meaningfully. However, lemurs did not yawn in response to yawning stimuli when tested alone, or with their groupmates. This study provides preliminary evidence that lemurs do not respond to yawning stimuli similarly to haplorhines, and suggests that this behavior may have evolved or become more exaggerated in haplorhines after the two major primate lineages split.
We tested five lemur species-ring-tailed lemurs, ruffed lemurs, mongoose lemurs, black lemurs, and Coquerel's sifakas-(N = 52) in an experiment that evaluated skills for inhibitory control in a social context. First, two human experimenters presented identical food rewards; the "generous" experimenter allowed the subject to eat from her hand, whereas the "competitive" experimenter always withheld the reward. Lemurs quickly learned to approach the generous experimenter and avoid the competitive one. In the inhibition test phase, we endowed the competitive experimenter with a more valuable food reward but the competitive experimenter continued to withhold food from the subject. Thus, lemurs were required to inhibit approaching the more desirable reward in favor of the lesser but obtainable reward presented by the generous experimenter. In test trials, lemurs' tendency to approach the competitive experimenter increased from the reputation phase, demonstrating sensitivity to the experimental manipulation. However, subjects approached the larger reward less frequently in test trials compared with pretest food-preference trials, evidencing some capacity for inhibitory control in this context. Despite differences in sociality and ecology, the five lemur species did not differ in this ability. Although the study did not uncover species differences, this experimental task may provide a useful measure of social inhibition in broader comparative studies.
EL MacLean, B Hare, CL Nunn, E Addessi, F Amici, RC Anderson, F Aureli, JM Baker, AE Bania, AM Barnard, NJ Boogert, EM Brannon, EE Bray, J Bray, LJN Brent, JM Burkart, J Call, JF Cantlon, LG Cheke, NS Clayton, MM Delgado, LJ DiVincenti, K Fujita, E Herrmann, C Hiramatsu, LF Jacobs, KE Jordan, JR Laude, KL Leimgruber, EJE Messer, AC A de Moura, L Ostojic, A Picard, ML Platt, JM Plotnik, F Range, SM Reader, RB Reddy, AA Sandel, LR Santos, K Schumann, AM Seed, KB Sewall, RC Shaw, KE Slocombe, Y Su, A Takimoto, J Tan, R Tao, CP van Schaik, Z Virányi, E Visalberghi, JC Wade, A Watanabe, J Widness, JK Young, TR Zentall, and Y Zhao. 2014. “The evolution of self-control.” Proceedings of the National Academy of Sciences, 111, 20, Pp. E2140-E2148. Publisher's VersionAbstract
Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.
The social intelligence hypothesis suggests that living in large social networks was the primary selective pressure for the evolution of complex cognition in primates. This hypothesis is supported by comparative studies demonstrating a positive relationship between social group size and relative brain size across primates. However, the relationship between brain size and cognition remains equivocal. Moreover, there have been no experimental studies directly testing the association between group size and cognition across primates. We tested the social intelligence hypothesis by comparing 6 primate species (total N = 96) characterized by different group sizes on two cognitive tasks. Here, we show that a species’ typical social group size predicts performance on cognitive measures of social cognition, but not a nonsocial measure of inhibitory control. We also show that a species’ mean brain size (in absolute or relative terms) does not predict performance on either task in these species. These data provide evidence for a relationship between group size and social cognition in primates, and reveal the potential for cognitive evolution without concomitant changes in brain size. Furthermore our results underscore the need for more empirical studies of animal cognition, which have the power to reveal species differences in cognition not detectable by proxy variables, such as brain size.