Celebrating the continued importance of "Machiavellian Intelligence" 30 years on

The question of what has shaped primates’ (and other species’) cognitive capacities, whether technical or social demands, remains a hot topic of inquiry. Indeed, a key area of study within the field of comparative psychology in the last few decades has been the focus on social life as a driving force behind the evolution of cognition, studied from behavioral and neurological perspectives and from theoretical and empirical perspectives. Reflecting on contemporary studies of primate social cognition specifically, one cannot ignore the book, Machiavellian Intelligence, coedited by Richard Byrne and Andrew Whiten (Byrne & Whiten, 1988a). It is a keystone for the field: The volume as a whole has been cited over 3,000 times, without even including citations to individual chapters. This year, 2018, is the 30th anniversary of the first publication of Machiavellian Intelligence, and with this special issue of the Journal of Comparative Psychology, we mark that milestone. The key concept put forth in Machiavellian Intelligence was that primates’ sociocognitive abilities were shaped by the complex social worlds that they inhabited, rather than the technical or foraging challenges that they faced, as had previously been posited. In this issue, we consider the strength of the Machiavellian intelligence hypothesis 30 years on to explain primate social cognition, and we consider its applicability to nonprimate species and to other cognitive domains

Social learning, culture and the ‘socio-cultural brain’ of human and non-human primates

AW was supported during the writing of this review by the John Templeton Foundation (grant number ID40128). EvdW was supported by the Swiss National Science Foundation (grant number P300P3-151187) and Society in Science - Branco Weiss Fellowship.Noting important recent discoveries, we review primate social learning, traditions and culture, together with associated findings about primate brains. We survey our current knowledge of primate cultures in the wild, and complementary experimental diffusion studies testing species’ capacity to sustain traditions. We relate this work to theories that seek to explain the enlarged brain size of primates as specializations for social intelligence, that have most recently extended to learning from others and the cultural transmission this permits. We discuss alternative theories and review a variety of recent findings that support cultural intelligence hypotheses for primate encephalization. At a more fine-grained neuroscientific level we focus on the underlying processes of social learning, especially emulation and imitation. Here, our own and others’ recent research has established capacities for bodily imitation in both monkeys and apes, results that are consistent with a role for the mirror neuron system in social learning. We review important convergences between behavioural findings and recent non-invasive neuroscientific studies.PostprintPeer reviewe

Similarity in Food Cleaning Techniques within Matrilines in Wild Vervet Monkeys

Social learning and the formation of traditions rely on the ability and willingness to copy one another. A central question is under which conditions individuals adapt behaviour to social influences. Here, we demonstrate that similarities in food processing techniques emerge on the level of matrilines (mother – offspring) but not on the group level in an experiment on six groups of wild vervet monkeys that involved grapes covered with sand. Monkeys regularly ate unclean grapes but also used four cleaning techniques more similarly within matrilines: rubbing in hands, rubbing on substrate, open with mouth, and open with hands. Individual cleaning techniques evolved over time as they converged within matrilines, stabilised at the end and remained stable in a follow-up session more than one year later. The similarity within matrilines persisted when we analyzed only foraging events of individuals in the absence of other matriline members and matriline members used more similar methods than adult full sisters. Thus, momentary conversion or purely genetic causation are unlikely explanations, favouring social learning as mechanism for within matriline similarities. The restriction of traditions to matriline membership rather than to the group level may restrict the development of culture in monkeys relative to apes or humans

Urbanization does not increase “object curiosity” in vervet monkeys, but semi-urban individuals selectively explore food-related anthropogenic items

Urban environments expose animals to abundant anthropogenic materials and foods that facilitate foraging innovations in species with opportunistic diets and high behavioral flexibility. Neophilia and exploration tendency are believed to be important behavioral traits for animals thriving in urban environments. Vervet monkeys (Chlorocebus pygerythrus) are one of few primate species that have successfully adapted to urban environments, thus making them an ideal species to study these traits. Using a within-species cross-habitat approach, we compared neophilia and exploration of novel objects (jointly referred to as “object curiosity”) between semi-urban, wild, and captive monkeys to shed light on the cognitive traits facilitating urban living. To measure “object curiosity,” we exposed monkeys to various types of novel stimuli and compared their approaches and explorative behavior. Our results revealed differences in the number of approaches and explorative behavior toward novel stimuli between the habitat types considered. Captive vervet monkeys were significantly more explorative than both semi- urban and wild troops, suggesting that positive experiences with humans and lack of predation, rather than exposure to human materials per se, influence object curiosity. Across habitats, juvenile males were the most explorative age-sex class. This is likely due to males being the dispersing sex and juveniles being more motivated to learn about their environment. Additionally, we found that items potentially associated with human food, elicited stronger explorative responses in semi-urban monkeys than non-food related objects, suggesting that their motivation to explore might be driven by “anthrophilia”, that is, their experience of rewarding foraging on similar anthropogenic food sources. We conclude that varying levels of exposure to humans, predation and pre-exposure to human food packaging explain variation in “object curiosity” in our sample of vervet monkeys

Molecular assessment of dietary variation in neighbouring primate groups

Facing rapid environmental changes and anthropogenic habitat destruction, animal behavioural plasticity becomes an adaptive potential that needs to be considered in conservation strategies along with, for example, genetic diversity. Here, we evaluate to what extent non-invasive environmental DNA (eDNA) methods may contribute to the assessment of intraspecies behavioural plasticity in terms of foraging behaviour. We analysed DNA metabarcoding data for plant components in the diet of four neighbouring groups of wild vervet monkeys Chlorocebus pygerythrus to identify intergroup variation (IGV). The faecal samples considered for the analyses were limited to the summer season to minimise the impact of seasonality. Each sample was attributed by observation to individuals with known life history data. A plant survey was conducted in each group home range during the study period to account for environmental variation. We observed mixed results when testing whether IGV in plant consumption was greater than intragroup variation, indicating that the influence of social dynamics must be considered. Intragroup variation was positively correlated with group size. We observed IGV in diet composition among all groups as well as in some pairwise comparisons. We found significant dietary differences between two group pairs when considering only adult females. Lastly, we observed IGV in foraging of specific plants that were not explained by their distribution, suggesting behavioural differences in selectivity between groups. Our study system and organism, being a highly social and non-threatened primate species, with constant gene flow and overlapping territories between groups, provides an ideal model to evaluate the usage of eDNA-based methods to better understand the impact of social factors on IGV. Our results highlight the need to consider social and demographic factors, the impact of which remains complicated to disentangle from environmental factors. However, we emphasise the great potential for studying social groups using eDNA and that such studies are needed to better understand intraspecific behavioural plasticity in wild populations. </ol

Dynamics of Intersexual Dominance and Adult Sex- Ratio in Wild Vervet Monkeys

Intersexual dominance relations are important for female mammals, because of their consequences for accessing food and for the degree of sexual control females experience from males. Female mammals are usually considered to rank below males in the dominance hierarchy, because of their typical physical inferiority. Yet, in some groups or species, females are nonetheless dominant over some males (partial female dominance). Intersexual dominance, therefore, also depends on traits other than sexual dimorphism, such as social support, social exchange, group adult sex-ratio, and the widespread self-reinforcing effects of winning and losing fights, the “winner-loser effect.” The importance of sex-ratio and the winner-loser effect remains poorly understood. A theoretical model, DomWorld, predicts that in groups with a higher proportion of males, females are dominant over more males when aggression is fierce (not mild). The model is based on a small number of general processes in mammals, such as grouping, aggression, the winner-loser effect, the initially greater fighting capacity of males than females, and sex ratio. We expect its predictions to be general and suggest they be examined in a great number of species and taxa. Here, we test these predictions in four groups of wild vervet monkeys (Chlorocebus pygerythrus) in Mawana game reserve in Africa, using 7 years of data. We confirm that a higher proportion of males in the group is associated with greater dominance of females over males; a result that remains when combining these data with those of two other sites (Amboseli and Samara). We additionally confirm that in groups with a higher fraction of males there is a relatively higher (a) proportion of fights of males with other males, and (b) proportion of fights won by females against males from the fights of females with any adults. We reject alternative hypotheses that more dominance of females over males could be attributed to females receiving more coalitions from males, or females receiving lowered male aggression in exchange for sexual access (the docile male hypothesis). We conclude that female dominance relative to males is dynamic and that future empirical studies of inter-sexual dominance will benefit by considering the adult sex-ratio of groups.</p