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Charpentier, M. J.

Publications and source records attributed to Charpentier, M. J..

3 recordsLinked to original sources

Disparate social structures are underpinned by distinct social rules across a primate radiation

Over six decades of research on wild baboons and their close relatives (collectively, the African papionins) have uncovered substantial variation in their behavior and social systems. While most papionins form discrete social groups (single-level societies), a few others form small social units that are nested within larger supergroups (multi-level societies). These two systems are generally thought to be qualitatively distinct, but data from wild populations increasingly suggest that there may be areas of overlap. To quantify this potential gradient in social structure, a more systematic, comparative analysis is needed. Here, we constructed a database of behavioral and demographic records spanning 135 group-years, 28 social groups, 13 long-term field studies, and 11 species to quantify variation in grooming network structure, and identify the individual and dyadic properties (e.g., kinship and social status effects) that underlie this variation. Consistent with accumulating observations in the field, the single-level species could be divided into two categories: cohesive and cliquish. Cohesive single-level networks were dense, kin-biased, and moderately rank-structured, while cliquish single-level networks were more differentiated, slightly more kin-biased, and strongly rank-structured. As expected, multi-level networks were very modular and shaped by females ties to specific dominant males but varied in their kin biases. Taken together, these data suggest that (i) kin and rank biases are widespread but vary in their strength; (ii) male-centered subgroups are exclusive to multi-level systems; and (iii) increases in network modularity can emerge in response to heightened nepotism and male-centered clustering. SIGNIFICANCE STATEMENTWhat forces explain variation in primate societies? While kinship and dominance shape the social lives of many of our close relatives, it is unclear how their effects differ across species. Using a new database comprising decades of field research, we found that baboons and their close relatives fell into three general patterns: one in which groups were cohesive, kin-biased, and moderately rank-biased, another in which groups were more cliquish and nepotistic, and a third in which groups were divided into clusters centered on dominant males. Distinct primate societies may thus reflect differences in the strength of females nepotistic biases and the degree of males social influence.

animal behavior and cognition↗

Primate mothers promote proximity between their offspring and infants who look like them

Behavioral discrimination of kin is a key process structuring social relationships in animals. In this study, we provide a first example of discrimination towards non-kin by third-parties through a mechanism of phenotype matching. In mandrills, we recently demonstrated increased facial resemblance among paternally-related juvenile and adult females indicating adaptive opportunities for paternal kin recognition. Here, we hypothesize that mothers use offsprings facial resemblance with other infants to guide offsprings social opportunities towards similarly-looking ones. Using deep learning for face recognition in 80 wild mandrill infants, we first show that infants born to the same father or conceived during the tenure of the same alpha male resemble each other the most, independently of their age, sex or maternal origin, extending previous results to the youngest age class. Using long-term behavioral observations on association patterns and controlling for matrilineal origin, maternal relatedness and infant age and sex, we then demonstrate that, as hypothesized, mothers are spatially closer to infants that resemble their own offspring more, thereby facilitating associations among similar-looking infants. Using theoretical modeling, we describe a plausible evolutionary process whereby mothers gain fitness benefits by promoting nepotism among paternally related infants. This mechanism, that we call "second-order kin selection", may extend beyond mother-infant interactions and has the potential to explain cooperative behaviors among non-kin in social species, including humans.

evolutionary biology↗

Same father, same face: deep-learning reveals paternally-derived signalling of kinship in a wild primate

Animal faces convey important information such as individual health status1 or identity2,3. Human and nonhuman primates rely on highly heritable facial traits4,5 to recognize their kin6-8. However, whether these facial traits have evolved for this specific function of kin recognition remains unknown. We present the first unambiguous evidence that inter-individual facial similarity has been selected to signal kinship using a state-of-the-art artificial intelligence approach based on deep neural networks and long-term data on a natural population of nonhuman primates. The typical matrilineal society of mandrills, is characterized by an extreme males reproductive skew with one male generally siring the large majority of offspring born into the different matrilines each year9. Philopatric females are raised and live throughout their lives with familiar maternal half-sisters (MHS) but because of males reproductive monopolization, they also live with unfamiliar paternal half-sisters (PHS). Because kin selection predicts differentiated interactions with kin rather than nonkin10 and that PHS largely outnumber MHS in a mandrills social group, natural selection should favour mechanisms to recognize PHS. Here, we first show that PHS socially interact with each other as much as MHS do, both more than nonkin. Second, using artificial intelligence trained to recognize individual mandrills from a database of 16k portrait pictures, we demonstrate that facial similarity increases with genetic relatedness. However, PHS resemble more to each other than MHS do, despite both kin categories sharing similar degrees of genetic relatedness. We propose genomic imprinting as a plausible genetic mechanism to explain paternally-derived facial similarity among PHS selected to improve kin recognition. This study further highlights the potential of artificial intelligence to study evolutionary mechanisms driving variation between phenotypes.

evolutionary biology↗