Mandrill mothers associate with infants who look like their own offspring using phenotype matching

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 p...

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Main Authors: Marie JE Charpentier, Clémence Poirotte, Berta Roura-Torres, Paul Amblard-Rambert, Eric Willaume, Peter M Kappeler, François Rousset, Julien P Renoult
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/79417
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author Marie JE Charpentier
Clémence Poirotte
Berta Roura-Torres
Paul Amblard-Rambert
Eric Willaume
Peter M Kappeler
François Rousset
Julien P Renoult
author_facet Marie JE Charpentier
Clémence Poirotte
Berta Roura-Torres
Paul Amblard-Rambert
Eric Willaume
Peter M Kappeler
François Rousset
Julien P Renoult
author_sort Marie JE Charpentier
collection DOAJ
description 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 predicted, 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 an 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, 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 other social species, including humans.
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spelling doaj.art-f410247f0bbc4b408317212cf81ff9362022-12-22T04:14:09ZengeLife Sciences Publications LtdeLife2050-084X2022-11-011110.7554/eLife.79417Mandrill mothers associate with infants who look like their own offspring using phenotype matchingMarie JE Charpentier0https://orcid.org/0000-0001-6530-5874Clémence Poirotte1Berta Roura-Torres2Paul Amblard-Rambert3Eric Willaume4Peter M Kappeler5François Rousset6Julien P Renoult7ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, FranceBehavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, GermanyBehavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, Germany; Projet Mandrillus, SODEPAL, Bakoumba, GabonProjet Mandrillus, SODEPAL, Bakoumba, GabonSODEPAL-COMILOG, Bakoumba, GabonBehavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, GermanyISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, FranceCEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, FranceBehavioral 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 predicted, 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 an 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, 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 other social species, including humans.https://elifesciences.org/articles/79417primateAfrican monkeymandrillus sphinx
spellingShingle Marie JE Charpentier
Clémence Poirotte
Berta Roura-Torres
Paul Amblard-Rambert
Eric Willaume
Peter M Kappeler
François Rousset
Julien P Renoult
Mandrill mothers associate with infants who look like their own offspring using phenotype matching
eLife
primate
African monkey
mandrillus sphinx
title Mandrill mothers associate with infants who look like their own offspring using phenotype matching
title_full Mandrill mothers associate with infants who look like their own offspring using phenotype matching
title_fullStr Mandrill mothers associate with infants who look like their own offspring using phenotype matching
title_full_unstemmed Mandrill mothers associate with infants who look like their own offspring using phenotype matching
title_short Mandrill mothers associate with infants who look like their own offspring using phenotype matching
title_sort mandrill mothers associate with infants who look like their own offspring using phenotype matching
topic primate
African monkey
mandrillus sphinx
url https://elifesciences.org/articles/79417
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