Skip to main content

Maternal influences on primate social development

Abstract

Primate mothers have the potential to influence the development of species-typical aspects of their offspring’s behavior as well as their individual sociosexual and reproductive strategies. If mothers experience psychosocial stress during pregnancy or lactation, their own stress hormones can have a long-term impact on their offspring’s physiology. The mother’s own behavior, especially weaning-related rejection, can be stressful to infants and have long-lasting effects on their infants’ neuroendocrine reactivity to stress. Exposure to variable maternal style early in life has long-term effects on the development of offspring behavior, including exploration and play, affiliation and aggression, and parenting. Primate mothers influence the kinship- and rank-related social preferences of their offspring, typically by providing opportunities to interact with some individuals more than others. Although mothers can contribute to the development of sex-typical behavior in the offspring (along with other environmental and genetic factors), sex-typical behavior is generally not the product of maternal socialization. Mothers provide their offspring with opportunities for social learning but rarely teach their infants new skills. In primate species with despotic dominance hierarchies, maternal transmission of rank through agonistic aid to their offspring makes a crucial contribution to the offspring’s fitness (as the daughters of high-ranking mothers reproduce more successfully than the daughters of low-ranking mothers). Future studies of maternal influences on social development could benefit from a deeper theoretical and experimental investigation of the evolutionary significance of these effects as well as of their underlying proximate mechanisms.

This is a preview of subscription content, access via your institution.

References

  • Andrews MW, Rosenblum LA (1991) Attachment in monkey infants raised in variable and low-demand environments. Child Dev 62:686–693

    PubMed  Article  CAS  Google Scholar 

  • Bardi M, Bode AE, Ramirez SM (2005) Maternal care and development of stress responses in baboons. Am J Primatol 66:263–278

    PubMed  Article  Google Scholar 

  • Bardi M, Huffman MA (2006) Maternal behavior and maternal stress are associated with infant behavioral development. Dev Psychobiol 48:1–9

    PubMed  Article  Google Scholar 

  • Berghänel A, Heistermann M, Schülke O, Ostner J (2016) Prenatal stress effects in a wild, long-lived primate: predictive adaptive responses in an unpredictable environment. Proc R Soc B 283:20161304

    PubMed  Article  Google Scholar 

  • Berghänel A, Heistermann M, Schülke O, Ostner J (2017) Prenatal stress accelerates offspring growth to compensate for reduced maternal investment across mammals. Proc Natl Acad USA 114:E10658–E10666

    Article  CAS  Google Scholar 

  • Berman CM (1990) Intergenerational transmission of maternal rejection rates among free-ranging rhesus monkeys. Anim Behav 39:329–337

    Article  Google Scholar 

  • Berman CM (2004) Developmental aspects of kin bias in behavior. In: Chapais B, Berman CM (eds) Kinship and behavior in primates. Oxford University Press, Oxford, pp 317–346

    Google Scholar 

  • Blomquist GE, Sade DS, Berard JD (2011) Rank-related fitness differences and their demographic pathways in semi-free-ranging rhesus macaques (Macaca mulatta). Int J Primatol 32:193–208

    Article  Google Scholar 

  • Boesch C (1991) Teaching among wild chimpanzees. Anim Behav 41:530–532

    Article  Google Scholar 

  • Bowlby J (1969) Attachment and loss. Attachment, vol I. Basic Books, New York

    Google Scholar 

  • Caro TM, Hauser MD (1992) Is there teaching in nonhuman animals? Q Rev Biol 67:151–174

    PubMed  Article  CAS  Google Scholar 

  • Cartmill E, Maestripieri D (2012) Socio-cognitive specializations of nonhuman primates: evidence from gestural communication. In: Vonk J, Shackelford T (eds) The Oxford handbook of comparative evolutionary psychology. Oxford University Press, Oxford, pp 166–193

    Google Scholar 

  • Chapais B (1992) The role of alliances in social inheritance of rank among female primates. In: Harcourt A, de Waal FBM (eds) Coalitions and alliances in humans and other animals. Oxford University Press, New York, pp 29–59

    Google Scholar 

  • Cheney DL (1977) The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behav Ecol Sociobiol 2:303–318

    Article  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

  • De Lathouwers M, van Elsacker L (2004) Comparing maternal styles in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Am J Primatol 64:411–423

    PubMed  Article  Google Scholar 

  • de Waal FBM (1990) Do rhesus mothers suggest friends to their offspring? Primates 31:597–600

    Article  Google Scholar 

  • de Waal FBM (1996) Macaque social culture: development and perpetuation of affiliative networks. J Comp Psychol 110:147–154

    PubMed  Article  Google Scholar 

  • Del Giudice M, Ellis BJ, Shirtcliff EA (2011) The adaptive calibration model of stress responsivity. Neurosci Biobehav Rev 35:1562–1592

    PubMed  Article  Google Scholar 

  • Dettmer AM, Kaburu SSK, Simpson EA et al (2016) Neonatal face-to-face interactions promote later social behavior in infant rhesus monkeys. Nat Commun 7:11940

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Duboscq J, Neumann C, Agil M, Perwitasari-Farajallah D, Thierry B, Engelhardt A (2017) Degrees of freedom in social bonds of crested macaque females. Anim Behav 123:411–426

    Article  Google Scholar 

  • Fairbanks LA (1989) Early experience and cross-generational continuity of mother-infant contact in vervet monkeys. Dev Psychobiol 22:669–681

    PubMed  Article  CAS  Google Scholar 

  • Fairbanks LA (1996) Individual differences in maternal styles: causes and consequences for mothers and offspring. Adv Study Behav 25:579–611

    Article  Google Scholar 

  • Fairbanks LA, Jorgensen MJ, Huff A, Blau K, Hung Y, Mann JJ (2004) Adolescent impulsivity predicts adult dominance attainment in male vervet monkeys. Am J Primatol 64:1–17

    PubMed  Article  Google Scholar 

  • Fairbanks LA, McGuire MT (1987) Mother-infant relationships in vervet monkeys: response to new adult males. Int J Primatol 8:351–366

    Article  Google Scholar 

  • Fairbanks LA, McGuire MT (1988) Long-term effects of early mothering behavior on responsiveness to the environment in vervet monkeys. Dev Psychobiol 21:711–724

    PubMed  Article  CAS  Google Scholar 

  • Fairbanks LA, McGuire MT (1993) Maternal protectiveness and response to the unfamiliar in vervet monkeys. Am J Primatol 30:119–129

    Article  Google Scholar 

  • Fairbanks LA, McGuire MT (1995) Maternal condition and the quality of maternal care in vervet monkeys. Behaviour 132:733–754

    Article  Google Scholar 

  • Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 19:1768–1772

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Flinn MV, Nepomnaschy PA, Muehlenbein MP, Ponzi D (2011) Evolutionary functions of early social modulation of hypothalamic-pituitary-adrenal axis development in humans. Neurosci Biobehav Rev 35:1611–1629

    PubMed  Article  CAS  Google Scholar 

  • Georgiev AV, Christie D, Rosenfield KA, Ruiz-Lambides A, Maldonado E, Emery Thompson M, Maestripieri D (2016) Breaking the succession rule: the costs and benefits of an alpha-status take-over by an immigrant rhesus macaque on Cayo Santiago. Behaviour 153:325–351

    Article  Google Scholar 

  • Groothuis TTG, Maestripieri D (2013) Parental influences on offspring personality traits in oviparous and placental vertebrates. In: Carere C, Maestripieri D (eds) Animal personalities: behavior, physiology, and evolution. The University of Chicago Press, Chicago, pp 317–352

    Chapter  Google Scholar 

  • Higham JP, Maestripieri D (2010) Revolutionary coalitions in male rhesus macaques. Behaviour 147:1889–1908

    Article  Google Scholar 

  • Higley JD (2003) Aggression. In: Maestripieri D (ed) Primate psychology. Harvard University Press, Cambridge, pp 17–40

    Google Scholar 

  • Hinde K (2009) Richer milk for sons but more milk for daughters: sex-biased investment during lactation varies with maternal life history in rhesus macaques. Am J Hum Biol 21:512–519

    PubMed  Article  Google Scholar 

  • Hinde RA, Spencer-Booth Y (1971) Towards understanding individual differences in rhesus mother-infant interaction. Anim Behav 19:165–173

    Article  Google Scholar 

  • Hinde RA, Spencer-Booth Y (1967) The behaviour of socially living rhesus monkeys in their first two and a half years. Anim Behav 15:169–196

  • Hirata S, Celli ML (2003) Role of mothers in the acquisition of tool-use behaviors by captive infant chimpanzees. Anim Cogn 6:235–244

    PubMed  Article  Google Scholar 

  • Hiraiwa-Hasegawa M (1993) Skewed birth sex ratios in primates: should high ranking mothers have daughters or sons? Trends Ecol Evol 8:395–400

    PubMed  Article  CAS  Google Scholar 

  • Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D (2010) Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 21:972–978

    PubMed  PubMed Central  Article  Google Scholar 

  • Hoffman CL, Maestripieri D (2011) Costs of reproduction among rhesus macaque females on Cayo Santiago. In: Wang Q (ed) Bones, genetics, and behavior of rhesus macaques. Springer, Berlin, pp 209–226

    Google Scholar 

  • Holekamp KE, Smale L (1991) Dominance acquisition during mammalian social development: the "inheritance" of maternal rank. Am Zool 31:306–317

    Article  Google Scholar 

  • Hoppitt WJE, Brown GR, Kendal R, Rendell L, Thornton A, Webster MM, Laland KN (2008) Lessons from animal teaching. Trends Ecol Evol 23:486–493

    PubMed  Article  Google Scholar 

  • Horrocks J, Hunte W (1983) Maternal rank and offspring rank in vervet monkeys: an appraisal of the mechanisms of rank acquisition. Anim Behav 31:772–782

    Article  Google Scholar 

  • Howell S, Westergaard G, Hoos B, Chavanne TJ, Shoaf SE, Cleveland A, Snoy PJ, Suomi SJ, Higley JD (2007) Serotonergic influences on life-history outcomes in free-ranging male rhesus macaques. Am J Primatol 69:851–865

    PubMed  Article  CAS  Google Scholar 

  • Kaplan JR, Fontenot MB, Berard J, Manuck SB, Mann JJ (1995) Delayed dispersal and elevated monoamine activity in free-ranging rhesus monkeys. Am J Primatol 35:229–234

    Article  CAS  Google Scholar 

  • Koch H, McCormack KM, Sanchez MM, Maestripieri D (2014) The development of the hypothalamic-pituitary-adrenal axis function in rhesus monkeys: effects of age, sex, and early experience. Dev Psychobiol 56:86–95

    PubMed  Article  CAS  Google Scholar 

  • Kulik L, Amici F, Langos D, Widdig A (2015a) Sex differences in the development of social relationships in rhesus macaques (Macaca mulatta). Int J Primatol 36:353–376

    PubMed  PubMed Central  Article  Google Scholar 

  • Kulik L, Amici F, Langos D, Widdig A (2015b) Sex differences in the development of aggressive behavior in rhesus macaques (Macaca mulatta). Int J Primatol 36:764–789

    Article  Google Scholar 

  • Kulik L, Langos D, Widdig A (2016) Mothers make a difference: mothers develop weaker bonds with immature sons than daughters. PLoS One 11:e0154845

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Lonsdorf EV (2005) Sex differences in the development of termite-fishing skills in wild chimpanzees (Pan troglodytes schweinfurthii) of Gombe National Park, Tanzania. Anim Behav 70:673–683

    Article  Google Scholar 

  • Lonsdorf EV (2006) What is the role of the mother in the acquisition of tool-use skills in wild chimpanzees? Anim Cogn 9:36–46

    PubMed  Article  Google Scholar 

  • Lonsdorf EV (2017) Sex differences in nonhuman primate behavioral development. J Neurosci Res 95:213–221

    PubMed  Article  CAS  Google Scholar 

  • Lonsdorf EV, Anderson KE, Stanton MA, Shender M, Heintz MR, Murray CM (2014a) Boys will be boys: sex differences in wild infant chimpanzee social interactions. Anim Behav 88:79–83

    PubMed  PubMed Central  Article  Google Scholar 

  • Lonsdorf EV, Markham AC, Heintz MR, Anderson KE, Ciuk DJ, Goodall J, Murray CM (2014b) Sex differences in wild chimpanzee behavior emerge during infancy. PLoS One 9:e99099

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Lonsdorf EV, Pusey AE, Eberly L (2004) Sex differences in learning in chimpanzees. Nature 428:715–716

    PubMed  Article  CAS  Google Scholar 

  • Lonsdorf EV, Ross SR (2012) Socialization and development of behavior. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 245–268

    Google Scholar 

  • Maestripieri D (1994) Social structure, infant handling, and mothering styles in group-living Old World monkeys. Int J Primatol 15:531–553

    Article  Google Scholar 

  • Maestripieri D (1995a) Maternal encouragement in nonhuman primates and the question of animal teaching. Hum Nat 6:361–378

    PubMed  Article  CAS  Google Scholar 

  • Maestripieri D (1995b) First steps in the macaque world: do rhesus mothers encourage their infants' independent locomotion? Anim Behav 49:1541–1549

    Article  Google Scholar 

  • Maestripieri D (1995c) Assessment of danger to themselves and their infants by rhesus macaque (Macaca mulatta) mothers. J Comp Psychol 109:416–420

    PubMed  Article  Google Scholar 

  • Maestripieri D (1996a) Maternal encouragement of infant locomotion in pigtail macaques, Macaca nemestrina. Anim Behav 51:603–610

    Article  Google Scholar 

  • Maestripieri D (1996b) Gestural communication and its cognitive implications in pigtail macaques (Macaca nemestrina). Behaviour 133:997–1022

    Article  Google Scholar 

  • Maestripieri D (1998) Parenting styles of abusive mothers in group-living rhesus macaques. Anim Behav 55:1–11

    PubMed  Article  CAS  Google Scholar 

  • Maestripieri D (2001a) Intraspecific variability in parenting styles of rhesus macaques: the role of the social environment. Ethology 107:237–248

    Article  Google Scholar 

  • Maestripieri D (2001b) Female-biased maternal investment in rhesus macaques. Folia Primatol 72:44–47

    PubMed  Article  CAS  Google Scholar 

  • Maestripieri D (2002) Parent-offspring conflict in primates. Int J Primatol 23:923–951

    Article  Google Scholar 

  • Maestripieri D (2003) Attachment. In: Maestripieri D (ed) Primate psychology. Harvard University Press, Cambridge, pp 108–143

    Google Scholar 

  • Maestripieri D (2004) Genetic aspects of mother-offspring conflict in rhesus macaques. Behav Ecol Sociobiol 55:381–387

    Article  Google Scholar 

  • Maestripieri D (2005) Effects of early experience on female behavioral and reproductive development in rhesus monkeys. Proc R Soc Lond B 272:1243–1248

    Article  Google Scholar 

  • Maestripieri D (2007) Macachiavellian intelligence: how rhesus macaques and humans have conquered the world. The University of Chicago Press, Chicago

    Book  Google Scholar 

  • Maestripieri (2008) Neuroendocrine mechanisms underlying the intergenerational transmission of maternal behavior and infant abuse in rhesus monkeys. In: Pfaff D, Kordon C, Chanson P, Christen Y (eds) Hormones and social behavior. Springer, Berlin, pp 121–130

    Chapter  Google Scholar 

  • Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. The University of Chicago Press, Chicago, pp 256–291

    Chapter  Google Scholar 

  • Maestripieri D (2010) Neurobiology of social behavior. In: Platt M, Ghazanfar A (eds) Primate Neuroethology. Oxford University Press, Oxford, pp 359–384

    Chapter  Google Scholar 

  • Maestripieri D, Higley JD, Lindell SG, Newman TK, McCormack KM, Sanchez MM (2006a) Early maternal rejection affects the development of monoaminergic systems and adult abusive parenting in rhesus macaques. Behav Neurosci 120:1017–1024

    PubMed  Article  Google Scholar 

  • Maestripieri D, Hoffman CL, Anderson GM, Carter CS, Higley JD (2009) Mother-infant interactions in free-ranging rhesus macaques: relationships between physiological and behavioral variables. Physiol Behav 96:613–619

    PubMed  Article  CAS  Google Scholar 

  • Maestripieri D, Klimczuk ACE (2013) Prenatal and maternal psychosocial stress in primates: adaptive plasticity or vulnerability to pathology? In: Laviola G, Macrí S (eds) Adaptive and maladaptive aspects of developmental stress. Springer, Berlin, pp 45–64

    Chapter  Google Scholar 

  • Maestripieri D, Lindell SG, Higley JD (2007) Intergenerational transmission of maternal behavior in rhesus monkeys and its underlying mechanisms. Dev Psychobiol 49:165–171

    PubMed  Article  Google Scholar 

  • Maestripieri D, Mateo JM (eds) (2009) Maternal effects in mammals. The University of Chicago Press, Chicago

    Google Scholar 

  • Maestripieri D, McCormack KM, Lindell SG, Higley JD, Sanchez MM (2006b) Influence of parenting style on the offspring's behavior and CSF monoamine metabolite levels in crossfostered and noncrossfostered female rhesus macaques. Behav Brain Res 175:90–95

    PubMed  Article  CAS  Google Scholar 

  • Maestripieri D, Ross SR (2004) Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure. Am J Phys Anthropol 123:52–61

    PubMed  Article  Google Scholar 

  • Maestripieri D, Ross SR, Megna NL (2002) Mother-infant interactions in western lowland gorillas (Gorilla gorilla gorilla): spatial relationships, communication, and opportunities for social learning. J Comp Psychol 116:219–227

    PubMed  Article  Google Scholar 

  • Maestripieri D, Wallen K (1997) Affiliative and submissive communication in rhesus macaques. Primates 38:127–138

    Article  Google Scholar 

  • Maestripieri D, Wallen K (2003) Nonhuman primate models of developmental psychopathology: problems and prospects. In: Cicchetti D, Walker E (eds) Neurodevelopmental mechanisms in psychopathology. Cambridge University Press, Cambridge, pp 187–214

    Chapter  Google Scholar 

  • Majolo B, Lehmann J, de Bortoli Vizioli A, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Primatol 147:652–660

    CAS  Google Scholar 

  • Mandalaywala TM, Higham JP, Heistermann M, Parker KJ, Maestripieri D (2014a) Physiological and behavioral responses to weaning conflict in free-ranging primate infants. Anim Behav 97:241–247

    PubMed  PubMed Central  Article  Google Scholar 

  • Mandalaywala TM, Parker KJ, Maestripieri D (2014b) Early experience affects the strength of vigilance for threat in rhesus monkey infants. Psychol Sci 25:1893–1902

    PubMed  PubMed Central  Article  Google Scholar 

  • Markham AC, Lonsdorf EV, Pusey AE, Murray CM (2015) Maternal rank influences the outcome of aggressive interactions between immature chimpanzees. Anim Behav 100:192–198

    PubMed  PubMed Central  Article  Google Scholar 

  • McCormack KM, Newman TK, Higley JD, Maestripieri D, Sanchez MM (2009) Serotonin transporter gene variation, infant abuse, and responsiveness to stress in rhesus macaque mothers and infants. Horm Behav 55:538–547

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Mehlman PT, Higley JD, Faucher I, Lilly AA, Taub DM, Vickers JH, Suomi SJ, Linnoila M (1995) Correlation of CSF 5-HIAA concentration with sociality and the timing of emigration in free-ranging primates. Am J Psychiatry 152:907–913

    PubMed  Article  CAS  Google Scholar 

  • Mehlman PT, Higley JD, Fernald BJ, Sallee FR, Suomi SJ, Linnoila M (1997) CSF 5-HIAA, testosterone, and sociosexual behaviors in free-ranging male rhesus macaques in the mating season. Psychiatry Res 72:89–10

    PubMed  Article  CAS  Google Scholar 

  • Murray CM, Lonsdorf EV, Stanton MA, Wellens KR, Miller JA, Goodall J, Pusey AE (2014) Early social exposure in wild chimpanzees: mothers with sons are more gregarious than mothers with daughters. Proc Natl Acad Sci USA 111:18189–18194

    PubMed  Article  CAS  Google Scholar 

  • Murray CM, Stanton MA, Wellens KR, Santymire RM, Heintz MR, Lonsdorf EV (2018) Maternal effects on offspring stress physiology in wild chimpanzees. Am J Primatol 80:e22525

    Article  CAS  Google Scholar 

  • Musgrave S, Morgan D, Lonsdorf EV, Mundry R, Sanz C (2016) Tool transfers are a form of teaching among chimpanzees. Sci Rep 6:34783

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Nakamichi M (1989) Sex differences in social development during the first 4 years in a free-ranging group of Japanese monkeys, Macaca fuscata. Anim Behav 38:737–748

    Article  Google Scholar 

  • Parker KJ, Buckmaster CL, Schatzberg AF, Lyons DM (2006) Maternal mediation, stress inoculation, and the development of neuroendocrine stress resistance in primates. Proc Natl Acad Sci USA 30:924–929

    Google Scholar 

  • Parker KJ, Maestripieri D (2011) Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates. Neurosci Biobehav Rev 35:1466–1483

    PubMed  Article  Google Scholar 

  • Pereira ME (1995) Development and social dominance among group living primates. Am J Primatol 37:143–175

    Article  Google Scholar 

  • Petrullo LA, Mandalaywala TM, Parker KJ, Maestripieri D, Higham JP (2016) Effects of early life adversity on cortisol/salivary alpha-amylase symmetry in free-ranging juvenile rhesus macaques. Horm Behav 86:78–84

    PubMed  Article  CAS  Google Scholar 

  • Roney JR, Maestripieri D (2003) Social development and affiliation. In: Maestripieri D (ed) Primate psychology. Harvard University Press, Cambridge, pp 171–204

    Google Scholar 

  • Sanchez MM, Alagbe O, Felger JC, Zhang J, Graff AE, Grand AP, Maestripieri D, Miller AH (2007) Activated p38 MAPK is associated with decreased CSF 5-HIAA and increased maternal rejection during infancy in rhesus monkeys. Mol Psychiatry 12:895–897

    PubMed  Article  CAS  Google Scholar 

  • Sanchez MM, McCormack KM, Grand AP, Fulks R, Graff A, Maestripieri D (2010) Effects of sex and early maternal abuse on adrenocorticotropin hormone and cortisol responses to the corticotropin-releasing hormone challenge during the first 3 years of life in group-living rhesus monkeys. Dev Psychopathol 22:45–53

    PubMed  PubMed Central  Article  Google Scholar 

  • Schino G, Aureli F, Ventura R, Troisi A (2004) A test of the cross-generational transmission of grooming preferences in macaques. Ethology 110:137–146

    Article  Google Scholar 

  • Schino G, Speranza L, Troisi A (2001) Early maternal rejection and later social anxiety in juvenile and adult Japanese macaques. Dev Psychobiol 38:186–190

    PubMed  Article  CAS  Google Scholar 

  • Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234

    PubMed  Article  CAS  Google Scholar 

  • Simpson MJA (1985) Effects of early experience on the behavior of yearling rhesus monkeys (Macaca mulatta) in the presence of a strange object: classification and correlation approaches. Primates 26:57–72

    Article  Google Scholar 

  • Simpson MJA, Datta SB (1990) Predicting infant enterprise from early relationships in rhesus macaques. Behaviour 116:42–63

    Article  Google Scholar 

  • Simpson MJA, Gore MA, Janus M, Rayment FDG (1989) Prior experience of risk and individual differences in enterprise shown by rhesus monkey infants in the second half of their first year. Primates 30:493–509

    Article  Google Scholar 

  • Simpson AE, Simpson MJA (1985) Short-term consequences of different breeding histories for captive rhesus macaque mothers and their young. Behav Ecol Sociobiol 18:83–89

  • Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291–309

    Article  Google Scholar 

  • Symons D (1978) Play and aggression. In: A study of rhesus monkeys. Columbia University Press, New York

    Google Scholar 

  • Thornton A, Raihani NJ (2008) The evolution of animal teaching. Anim Behav 75:1823–1836

    Article  Google Scholar 

  • Trivers RL, Willard D (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92

    PubMed  Article  CAS  Google Scholar 

  • van de Rijt-Plooy HHC, Plooy FX (1987) Growing independence, conflict and learning in mother-infant relations in free-ranging chimpanzees. Behaviour 101:1–86

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (1985) Male migration and rank acquisition in wild long-tailed macaques (Macaca fascicularis). Anim Behav 33:849–861

    Article  Google Scholar 

  • van Noordwijk MA, van Schaik CP (1988) Male careers in Sumatran long-tailed macaques (Macaca fascicularis). Behaviour 107:24–43

    Article  Google Scholar 

  • van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley R (eds) Comparative socioecology: the behavioral ecology of humans and other mammals. Blackwell, Boston, pp 195–218

    Google Scholar 

  • Vochteloo JD, Timmermans PJA, Duijghuisen JAH, Vossen JMH (1993) Effects of reducing the mother's radius of action on the development of mother-infant relationships in longtailed macaques. Anim Behav 45:603–612

    Article  Google Scholar 

  • Whiten A (1999) Parental encouragement in gorilla in comparative perspective: implications for social cognition and the evolution of teaching. In: Parker ST, Mitchell RW, Miles HL (eds) The mentalities of gorillas and orangutans: comparative perspectives. Cambridge University Press, Cambridge, pp 342–366

    Chapter  Google Scholar 

  • Widdig A, Nürnberg P, Krawczak M, Streich WJ, Bercovitch F (2002) Affiliation and aggression among adult female rhesus macaques: a genetic analysis of paternal cohorts. Behaviour 139:371–391

    Article  Google Scholar 

Download references

Acknowledgments

I am grateful to Federica Amici and Anja Widdig for their invitation to contribute to the Behavioral Ecology and Sociobiology topical collection “An evolutionary perspective on the development of primate sociality.” I also thank Anja Widdig and two anonymous reviewers for helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dario Maestripieri.

Ethics declarations

Conflict of interest

The author declares that he has no conflict of interest.

Additional information

This article is a contribution to the Topical Collection An evolutionary perspective on the development of primate sociality – Guest Editors: Federica Amici and Anja Widdig

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Maestripieri, D. Maternal influences on primate social development. Behav Ecol Sociobiol 72, 130 (2018). https://doi.org/10.1007/s00265-018-2547-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00265-018-2547-x

Keywords

  • Maternal effects
  • Social development
  • Stress reactivity
  • Sex differences
  • Social learning
  • Primates