Abstract
Nonhuman primates don’t have formal kinship systems, but genetic relatedness shapes patterns of residence, behavior, mating preferences, and cognition in the primate order. The goal of this article is to provide insight about the ancestral foundations on which the first human kinship systems were built. In order for evolution to favor nepotistic biases in behavior, individuals need to have opportunities to interact with their relatives and to be able to identify them. Both these requirements impose constraints on the evolution of kinship bonds in primate species. For nonhuman primates and many other mammals, maternal care generates close ties between mothers and offspring and among littermates. For species in which mother–offspring bonds extend beyond weaning, associations with the mother also generate familiarity among siblings of different ages. For species with female philopatry, mother–offspring ties provide the foundation for lifelong relationships between mothers and daughters, and dense matrilineal kin networks. However, several factors constrain the development of kinship bonds in nonhuman primates. First, dispersal strategies, which are designed to reduce inbreeding, bias kinship networks in favor of the philopatric sex. Second, hostile relationships between groups mean that kin ties are usually severed when individuals move from one group to another. Third, in species with polygynandrous mating systems, uncertainty about paternity and restricted periods of male reproductive monopoly limit the scope for development of ties among fathers and offspring, paternal siblings, or extended paternal kin networks. In this article, I explore the impact of these factors on the evolution of ancestral human kinship systems.
Similar content being viewed by others
References
Alberts SC (2012) Magnitude and sources of variation in male reproductive performance. In: Mitani J, Call J, Kappeler PM, Palombit R, Silk JB (eds) The evolution of primate societies. Chicago University Press, Chicago, pp 245–268
Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons Papio cynocephalus. Anim Behav 65(4):821–840
Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: from mating opportunities to paternity success. Anim Behav 72(5):1177–1196
Altmann J (1979) Age cohorts as paternal sibships. Behav Ecol Sociobiol 6:161–164
Altmann J (1990) Primate males go where the females are. Anim Behav 39:193–195
Andelman S (1986) Ecological and social determinants of cercopithecine mating patterns. In: Rubenstein D, Wrangham RW (eds) Ecological aspects of social evolution. Princeton University Press, Princeton, pp 201–216
Arandjelovic M, Head JS, Boesch C, Robbins MM, Vigilant L (2014) Genetic inference of group dynamics and female kin structure in a western lowland gorilla population (Gorilla gorilla gorilla). Primate Biol 1(1):29–38
Aureli F, Cozzolino R, Cordischi C, Scucchi S (1992) Kin-oriented redirection among Japanese macaques: an expression of a revenge system? Anim Behav 44:283–291
Borries C, Launhardt K, Epplen C, Epplen JT, Winkler P (1999) Males as infant protectors in Hanuman langurs (Presbytis entellus) living in multimale groups–defence pattern, paternity and sexual behavior. Behav Ecol Sociobiol 46(5):350–356
Bradley BJ (2006) Reconstructing phylogenies and phenotypes: a molecular view of human evolution. J Anat 212(4):337–353
Bradley BJ, Robbins MM, Williamson EA, Steklis HD, Steklis NG, Eckhardt N et al (2005) Mountain gorilla tug-of-war: silverbacks have limited control over reproduction in multimale groups. Proc Natl Acad Sci USA 102(26):9418–9423
Bradley BJ, Doran-Sheehy DM, Vigilant L (2007) Potential for female kin associations in wild western gorillas despite female dispersal. Proc R Soc B Biol Sci 274:2179–2185
Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425(6954):179–181
Chapais B (2001) Primate nepotism: what is the explanatory value of kin selection? Int J Primatol 22(2):203–229
Chapais B (2009) Primeval kinship: how pair-bonding gave birth to human society. Harvard University Press, Cambridge
Chapais B (2014) Complex kinship patterns as evolutionary constructions, and the origins of sociocultural universals. Curr Anthropol 55(6):751–783
Charpentier MJ, Peignot P, Hossaert-McKey M, Wickings EJ (2007) Kin discrimination in juvenile mandrills Mandrillus sphinx. Anim Behav 73(1):37–45
Charpentier MJ, Harté M, Ngoubangoye B, Herbert A, Kappeler PM (2017) Visual discrimination of kin in mandrills. Ethology 123(3):251–259
Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28(2):362–367
Cheney DL, Seyfarth RM (1989) Redirected aggression and reconciliation among vervet monkeys, Cercopithecus aethiops. Behaviour 110:258–275
Cords M, Minich T, Roberts SJ, Sleator C (2018) Evidence for paternal kin bias in the social affiliation of adult female blue monkeys. Am J Primatol 80(5):e22761
Dasser V (1988) A social concept in Java monkeys. Anim Behav 36(1):225–230
Diaz-Muñoz SL (2011) Paternity and relatedness in a polyandrous nonhuman primate: testing adaptive hypotheses of male reproductive cooperation. Anim Behav 82:561–573
Foerster S, McLellan K, Schroepfer-Walker K, Murray CM, Krupenye C, Gilby IC, Pusey AE (2015) Social bonds in the dispersing sex: partner preferences among adult female chimpanzees. Anim Behav 105:139–152
Gilby IC, Wrangham RW (2008) Association patterns among wild chimpanzees (Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behav Ecol Sociobiol 62(11):1831. https://doi.org/10.1007/s00265-008-0612-6
Greuter CC, Chapais B, Zinner D (2012) Evolution of multilevel social systems in nonhuman primates and humans. Int J Primatol 33(5):1002–1037
Hamilton WD (1964) The genetical evolution of social behavior. II. J Theor Biol 7(1):17–52
Harcourt AH, Purvis A, Liles L (1995) Sperm competition: mating system, not breeding season, affects testes size of primates. Funct Ecol 9:468–476
Hawkes K, O’Connell JF, Jones NB, Alvarez H, Charnov EL (1998) Grandmothering, menopause, and the evolution of human life histories. Proc Natl Acad Sci USA 95(3):1336–1339
Hill RA, Lee PC (1998) Predation risk as an influence on group size in cercopithecoid primates: implications for social structure. J Zool 245(4):447–456
Hohmann G, Fruth B (2002) Dynamics in social organization of bonobos (Pan paniscus). In: Boesch C, Hohmann G, Marchant LF (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge University Press, Cambridge, pp 138–150
Huck M, Fernandez-Duque E, Babb P, Schurr T (2014) Correlates of genetic monogamy in socially monogamous mammals: insights from Azara's owl monkeys. Proc R Soc B Biol Sci 281(1782):20140195
Kapsalis E, Berman CM (1996) Models of affiliative relationships among free-ranging rhesus monkeys (Macaca mulatta) I. Criteria for kinship. Behaviour 133:1209–1234
Langergraber KE (2012) Cooperation among kin. In: Mitani J, Call J, Kappeler PM, Palombit R, Silk JB (eds) The evolution of primate societies. Chicago University Press, Chicago, pp 412–431
Langergraber KE, Mitani JC, Vigilant L (2007) The limited impact of kinship on cooperation in wild chimpanzees. Proc Natl Acad Sci USA 104(19):7786–7790
Langergraber K, Mitani J, Vigilant L (2009) Kinship and social bonds in female chimpanzees (Pan troglodytes). Amer J Primatol 71(10):840–851
Langergraber K, Mitani JC, Watts DP, Vigilant L (2013) Male-female socio-spatial relationships and reproduction in wild chimpanzees. Behav EcolSociobiol 67(6):861–873
Langergraber KE, Watts DP, Vigilant L, Mitani JC (2017) Group augmentation, collective action, and territorial boundary patrols by male chimpanzees. Proc Natl Acad Sci USA 114(28):7337–7342
Langos D, Kulik L, Mundry R, Widdig A (2013) The impact of paternity on male–infant association in a primate with low paternity certainty. Mol Ecol 22(13):3638–3651
Lehmann J, Fickenscher G, Boesch C (2006) Kin biased investment in wild chimpanzees. Behaviour 143(8):931–956
Levréro F, Carrete-Vega G, Herbert A, Lawabi I, Courtiol A, Willaume E et al (2015) Social shaping of voices does not impair phenotype matching of kinship in mandrills. Nat Commun 6:7609
Londorf EV, Ross SR (2012) Socialization and development of behavior. In: Mitani J, Call J, Kappeler PM, Palombit R, Silk JB (eds) The evolution of primate societies. Chicago University Press, Chicago, pp 195–219
Lukas D, Clutton-Brock T (2012) Cooperative breeding and monogamy in mammalian societies. Proc R Soc B Biol Sci 1736:2151–2156
Lynch EC, Di Fiore A, Lynch RF, Palombit RA (2017) Fathers enhance social bonds among paternal half-siblings in immature olive baboons (Papio hamadryas anubis). Behav Ecol Sociobiol 71(8):71–120
Mateo JM (2015) Perspectives: Hamilton's legacy: mechanisms of kin recognition in humans. Ethology 121(5):419–427
Mitani JC, Gros-Louis J, Manson JH (1996) Number of males in primate groups: comparative tests of competing hypotheses. Am J Primatol 38(4):315–332
Moscovice LR, Heesen M, Di Fiore A, Seyfarth RM, Cheney DL (2009) Paternity alone does not predict long-term investment in juveniles by male baboons. Behav Ecol Sociobiol 63(10):1471–1482
Muniz L, Perry S, Manson JH, Gilkenson H, Gros-Louis J, Vigilant L (2006) Father–daughter inbreeding avoidance in a wild primate population. Curr Biol 16(5):R156–R157
Murray CM, Stanton MA, Lonsdorf EV, Wroblewski EE, Pusey AE (2016) Chimpanzee fathers bias their behaviour towards their offspring. R Soc Open Sci 3(11):160441
Perry S, Manson JH, Muniz L, Gros-Louis J, Vigilant L (2008) Kin-biased social behaviour in wild adult female white-faced capuchins Cebus capucinus. Anim Behav 76(1):187–199
Pfefferle D, Kazem AJ, Brockhausen RR, Ruiz-Lambides AV, Widdig A (2014a) Monkeys spontaneously discriminate their unfamiliar paternal kin under natural conditions using facial cues. Curr Biol 24(15):1806–1810
Pfefferle D, Ruiz-Lambides AV, Widdig A (2014b) Female rhesus macaques discriminate unfamiliar paternal sisters in playback experiments—support for acoustic phenotype matching. Proc R Soc B Biol Sci 281:20131628
Pusey A (1990) Mechanisms of inbreeding avoidance in nonhuman primates. In: Feierman JR (ed) Pedophilia. Springer, New York, pp 201–220
Pusey A, Wolf M (1996) Inbreeding avoidance in animals. Trends Ecol Evol 11(5):201–206
Reichard UH, Ganpanakngan M, Barelli C (2012) White-handed gibbons of Khao Yai: social flexibility, complex reproductive strategies, and a slow life history. In: Kappeler PM, Watts DP (eds) Long-term field studies of primates. Springer, Berlin, pp 237–258
Riehl C, Stern CA (2015) How cooperatively breeding birds identify relatives and avoid incest: new insights into dispersal and kin recognition. BioEssays 37(12):1303–1308
Roberts SJ, Nikitopoulos E, Cords M (2014) Factors affecting low resident male siring success in one-male groups of blue monkeys. Behav Ecol 25(4):852–861
Robbins MM, Robbins AM (2018) Variation in the social organization of gorillas: life history and socioecological perspectives. Evol Anthropol 27:218–233
Rodseth L, Wrangham RW (2004) Human kinship: a continuation of politics by other means. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, Oxford, pp 389–419
Rosenbaum S, Vigilant L, Kuzawa CW, Stoinski TS (2018) Caring for infants is associated with increased reproductive success for male mountain gorillas. Sci Rep 8(1):15223
Rosenbaum S, Hirwa JP, Silk JB, Vigilant L, Stoinski TS (2015) Male rank, not paternity, predicts male–immature relationships in mountain gorillas, Gorilla beringei beringei. Anim Behav 104:13–24
Sakamaki T, Ryu H, Toda K, Tokuyama N, Furuichi T (2018) Increased frequency of intergroup encounters in wild bonobos (Pan paniscus) around the yearly peak in fruit abundance at Wamba. Int J Primatol 39(4):685–704
Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani J, Call J, Kappeler PM, Palombit R, Silk JB (eds) The evolution of primate societies. Chicago University Press, Chicago, pp 195–219
Schülke O, Wenzel S, Ostner J (2013) Paternal relatedness predicts the strength of social bonds among female rhesus macaques. PLoS ONE 8(3):e59789
Silk JB (2009) Nepotistic cooperation in nonhuman primate groups. Philos Trans R Soc Lond B Biol Sci 364:3243–3254
Silk JB, Altmann J, Alberts SC (2006) Social relationships among adult female baboons (Papio cynocephalus) I. Variation in the strength of social bonds. Behav Ecol Sociobiol 61(2):183–195
Smith K, Alberts SC, Altmann J (2003) Wild female baboons bias their social behaviour towards paternal half-sisters. Proc R Soc B Biol Sci 270(1514):503–510
Snyder-Mackler N, Alberts SC, Bergman TJ (2012) Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups. Proc R Soc B Biol Sci B 279(1743):3788–3795
Städele V, Roberts ER, Barrett BJ, Strum SC, Vigilant L, Silk JB (2019) Male–female relationships in olive baboons (Papio anubis): Parenting or mating effort? J Hum Evol 127:81–92
Strier KB, Chaves PB, Mendes SL, Fagundes V, Di Fiore A (2011) Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate. Proc Natl Acad Sci USA 108(47):18915–18919
Tan J, Ariely D, Hare B (2017) Bonobos respond prosocially toward members of other groups. Sci Rep 7(1):1–11
van Noordwijk MA, Arora N, Willems EP, Dunkel LP, Amda RN, Mardianah N et al (2012) Female philopatry and its social benefits among Bornean orangutans. Behav Ecol Sociobiol 66(6):823–834
van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60
Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch FB (2001) Paternal relatedness and age proximity regulate social relationships among adult female rhesus macaques. Proc Natl Acad Sci USA 98(24):13769–13773
Wilson ML, Wrangham RW (2003) Intergroup relations in chimpanzees. Annu Rev Anthropol 32(1):363–392
Wilson ML, Boesch C, Fruth B, Furuichi T, Gilby IC, Hashimoto C et al (2014) Lethal aggression in Pan is better explained by adaptive strategies than human impacts. Nature 513(7518):414–417
Wittig RM, Crockford C, Wikberg E, Seyfarth RM, Cheney DL (2007) Kin-mediated reconciliation substitutes for direct reconciliation in female baboons. Proc R Soc B Biol Sci 274(1613):1109–1115
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Silk, J.B. The Phylogenetic Roots of Human Kinship Systems. Biol Theory 16, 127–134 (2021). https://doi.org/10.1007/s13752-020-00349-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13752-020-00349-4