Mandrillus face database: Portrait pictures of the population of wild mandrills from Bakoumba (Gabon)

Behavioral discrimination of kin is a key process structuring social
relationships in animals. In this study, we provide evidence for
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 mandrill mothers use offspring’s facial resemblance with
other infants to guide offspring’s social opportunities towards
similar-looking ones. Using deep learning for face recognition in 80 wild
mandrill infants, we first show that infants sired by the same father
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 show, as hypothesized, that mothers are spatially closer to infants
that resemble their own offspring more, and that this maternal behavior
leads to similar-looking infants being spatially associated. We then
discuss the different scenarios explaining this result, arguing that
adaptive maternal behavior is a likely explanation. In support of this
mechanism and using theoretical modeling, we finally describe a plausible
evolutionary process whereby mothers gain fitness benefits by promoting
nepotism among paternally related infants. This mechanism, which we call
“second-order kin selection”, may extend beyond mother-infant interactions
and has the potential to explain cooperative behaviors among non-kin in
other social species, including humans.