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


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
15 11 2022
Historique:
received: 12 04 2022
accepted: 03 10 2022
entrez: 15 11 2022
pubmed: 16 11 2022
medline: 18 11 2022
Statut: epublish

Résumé

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.

Identifiants

pubmed: 36377479
doi: 10.7554/eLife.79417
pii: 79417
pmc: PMC9665846
doi:
pii:

Banques de données

Dryad
['10.5061/dryad.dbrv15f3m', '10.5061/dryad.gtht76hqb']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2022, Charpentier, Poirotte et al.

Déclaration de conflit d'intérêts

MC, CP, BR, PA, EW, PK, FR, JR No competing interests declared

Références

Trends Neurosci. 2001 Oct;24(10):609-16
pubmed: 11576676
Sci Adv. 2020 May 27;6(22):eaba3274
pubmed: 32537486
Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10811-14
pubmed: 7479889
Evolution. 2007 Oct;61(10):2320-30
pubmed: 17711465
R Soc Open Sci. 2018 Apr 18;5(4):172159
pubmed: 29765670
PLoS One. 2012;7(10):e47508
pubmed: 23077627
Arch Sex Behav. 2008 Feb;37(1):64-77
pubmed: 18157627
Nat Commun. 2015 Jul 03;6:7609
pubmed: 26139329
Nature. 1970 Aug 1;227(5257):520-1
pubmed: 5428476
Nature. 2003 Sep 11;425(6954):179-81
pubmed: 12968180
Curr Biol. 2010 Aug 10;20(15):1359-61
pubmed: 20598541
J Theor Biol. 1964 Jul;7(1):1-16
pubmed: 5875341
Theor Popul Biol. 1971 Jun;2(2):125-41
pubmed: 5170716
Am J Phys Anthropol. 2016 Jan;159(Suppl 61):S105-29
pubmed: 26808101
Science. 2020 May 22;368(6493):
pubmed: 32439765
Am J Primatol. 2015 Oct;77(10):1036-48
pubmed: 26235675
Trends Genet. 1991 Feb;7(2):45-9
pubmed: 2035190
Nat Commun. 2014 Sep 16;5:4800
pubmed: 25226282
PLoS One. 2011;6(7):e22375
pubmed: 21818314
Ecology. 2015 Mar;96(3):631-41
pubmed: 26236860
Philos Trans R Soc Lond B Biol Sci. 2011 Jun 12;366(1571):1764-77
pubmed: 21536559
Proc Natl Acad Sci U S A. 2014 Dec 23;111(51):18189-94
pubmed: 25422411
Science. 1981 Mar 27;211(4489):1390-6
pubmed: 7466396
Science. 2002 Apr 5;296(5565):69-72
pubmed: 11935014
J Anim Breed Genet. 2005 Jun;122(3):172-6
pubmed: 16130468
Science. 2014 Aug 15;345(6198):771-6
pubmed: 25124431
Lancet. 2017 Mar 25;389(10075):1229-1237
pubmed: 28159391
PLoS Med. 2010 Jul 27;7(7):e1000316
pubmed: 20668659
Anim Cogn. 2003 Mar;6(1):73-6
pubmed: 12658537
Proc Biol Sci. 2014 Oct 22;281(1793):
pubmed: 25209936
J Evol Biol. 2011 May;24(5):1020-43
pubmed: 21371156
Philos Trans R Soc Lond B Biol Sci. 2014 Mar 31;369(1642):20130357
pubmed: 24686929
Curr Biol. 2016 Sep 26;26(18):2516-2521
pubmed: 27618264
Biol Lett. 2018 Oct 10;14(10):
pubmed: 30305461
Science. 2011 Dec 2;334(6060):1272-5
pubmed: 22144625

Auteurs

Marie J E Charpentier (MJE)

ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France.

Clémence Poirotte (C)

Behavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, Germany.

Berta Roura-Torres (B)

Behavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, Germany.
Projet Mandrillus, SODEPAL, Bakoumba, Gabon.

Paul Amblard-Rambert (P)

Projet Mandrillus, SODEPAL, Bakoumba, Gabon.

Eric Willaume (E)

SODEPAL-COMILOG, Bakoumba, Gabon.

Peter M Kappeler (PM)

Behavioral Ecology and Sociobiology Unit, German Primate Center, Leibniz Institute of Primate Research, Göttingen, Germany.

François Rousset (F)

ISEM, Univ Montpellier, CNRS, IRD, EPHE, Montpellier, France.

Julien P Renoult (JP)

CEFE, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France.

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