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Prenatal maternal stress effects on the development of primate social behavior

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Abstract

Prenatal developmental plasticity in response to various environmental and social adversities can affect multiple aspects of offspring phenotype including social behavior strategies with effects that can last into adulthood. Here, we (1) identify adaptive social behavior strategies and their underlying mechanisms as potential targets of developmental plasticity in primates, (2) derive predictions about social behavior outcomes of prenatal adversity from different types of evolutionary models, (3) review the primate evidence for prenatal stress effects on offspring cognitive function, social, and non-social behavior, and (4) discuss avenues for future research. The scarce evidence currently available points towards increased distress behavior, particularly in infant offspring, and reductions of activity, exploration, and affiliative behavior in response to experimental prenatal adversity. Not all effects are stable, the results do not replicate well, and, for the most part, the current data cannot be used to test predictions of evolutionary models because relevant aspects of social behavior were not quantified and not assessed in the complex social environments they evolved for. More comprehensive research in developmental plasticity needs to incorporate sex differences and the interaction of effects from different sensitive periods including adolescence. Moreover, future research needs to assess the role of social buffering in mediating intergenerational effects and trade-offs between the pace of life and social cognitive performance.

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References

  • Alberts SC (2012) Magnitude and sources of variation in male reproductive performance. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 412–431

    Google Scholar 

  • Alberts SC, Altmann J (1995a) Balancing costs and opportunities: dispersal in male baboons. Am Nat 145:279–306

    Google Scholar 

  • Alberts SC, Altmann J (1995b) Preparation and activiation: determinants of age at reproductive maturity in male baboons. Behav Ecol Sociobiol 36:397–406

    Google Scholar 

  • Almeling L, Hammerschmidt K, Sennhenn-Reulen H, Freund AM, Fischer J (2016) Motivational shifts in aging monkeys and the origins of social selectivity. Curr Biology 26:1744–1749

    CAS  PubMed  Google Scholar 

  • Amici F, Kulik L, Langos D, Widdig A (2019) Growing into adulthood—a review on sex differences in the development of sociality across macaques. Behav Ecol Sociobiol 73:18. https://doi.org/10.1007/s00265-018-2623-2

    Article  Google Scholar 

  • Archie EA, Tung J, Clark M, Altmann J, Alberts SC (2014) Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proc R Soc B 281:20141261. https://doi.org/10.1098/rspb.2014.1261

    Article  PubMed  Google Scholar 

  • Arnstein AFT (2009) Stress signalling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410–422

    Google Scholar 

  • Bardi M, Huffman MA (2005) Maternal behavior and maternal stress are associated with infant behavioral development in macaques. Dev Psychobiol 48:1–9. https://doi.org/10.1002/dev.20111

    Article  Google Scholar 

  • Barker DJP (2007) The origins of the developmental origins theory. J Intern Med 261:412–417

    CAS  PubMed  Google Scholar 

  • Barker DJP, Osmond C (1986) Diet and coronary heart disease in England and Wales during and after the second world war. J Epidemiol Commun H 40:37–44

    CAS  Google Scholar 

  • Bateson P, Barker D, Clutton-Brock T et al (2004) Developmental plasticity and human health. Nature 430:419

    CAS  PubMed  Google Scholar 

  • Bateson P, Gluckman P, Hanson M (2014) The biology of developmental plasticity and the predictive adaptive response hypothesis. J Physiol 592:2357–2368

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bauman MD, Iosif AM, Smith SEP, Bregere C, Amaral DG, Patterson PH (2014) Activation of the maternal immune system during pregnancy alters behavioral development of rhesus monkey offspring. Biol Psychiatry 75:332–341

    CAS  PubMed  Google Scholar 

  • Belsky J, Ruttle PL, Boyce WT, Armstrong JM, Essex MJ (2015) Early adversity, elevated stress physiology, accelerated sexual maturation, and poor health in females. Dev Psychol 51:816–822

    PubMed  PubMed Central  Google Scholar 

  • Berghänel A, Ostner J, Schröder U, Schülke O (2011a) Social bonds predict future cooperation in male barbary macaques, Macaca sylvanus. Anim Behav 81:1109–1116

    Google Scholar 

  • Berghänel A, Ostner J, Schülke O (2011b) Coalitions destabilize dyadic dominance relationships in male barbary macaques (Macaca sylvanus). Behaviour 148:1256–1274

    Google Scholar 

  • Berghänel A, Schülke O, Ostner J (2015) Locomotor play drives motor skill acquisition at the expense of growth: a life history trade-off. Sci Adv 1:e1500451

    PubMed  PubMed Central  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. https://doi.org/10.1098/rspb.2016.1304

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2003) Hierarchical classification by rank and kinship in baboons. Science 302:1234–1236

    CAS  PubMed  Google Scholar 

  • Bernstein I (1976) Dominance, aggression and reproduction in primate societies. J Theor Biol 60:459–472

    CAS  PubMed  Google Scholar 

  • Biro PA, Stamps JA (2008) Are animal personality traits linked to life-history productivity? Trends Ecol Evol 23:361–368

    PubMed  Google Scholar 

  • Bissonnette A, Perry S, Barrett L, Mitani JC, Flinn M, Gavrilets S, de Waal FBM (2015) Coalitions in theory and reality: a review of pertinent variables and processes. Behaviour 152:1–56

    Google Scholar 

  • Blair C, Kuzawa CW, Willoughby MT (2019) The development of executive function in early childhood is inversely related to change in body mass index: evidence for an energetic tradeoff? Dev Sci 18:e12860

    Google Scholar 

  • Blanc J, Rahill G, Spruill TM, Jean-Louis G, Mouchenik Y (2019) Association between prenatal exposure to the Haiti 2010 earthquake, consequent maternal PTSD and autistic symptoms in offspring. Europ J Trauma Dissociation. https://doi.org/10.1016/j.ejtd.2019.02.001

  • Bradbury J, Vehrencamp SL (1998) Principles of animal communication. Sinauer Press, Sunderland, MA

    Google Scholar 

  • Brent LN, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG, Skene JH, Platt ML (2013) Genetic origins of social networks in rhesus macaques. Sci Rep 3:1042

    PubMed  PubMed Central  Google Scholar 

  • Brent LN, Chang SWC, Gariépy J-F, Platt M (2014) The neuroethology of friendship. Ann N Y Acad Sci 1316:1–17

    CAS  PubMed  Google Scholar 

  • Briseno-Jaramillo M, Ramos-Fernández G, Palacios-Romo TM, Sosa-López JR, Lemasson A (2018) Age and social affinity effects on contact call interactions in free-ranging spider monkeys. Behav Ecol Sociobiol 72:192. https://doi.org/10.1007/s00265-018-2615-2

    Article  Google Scholar 

  • Brunton PJ (2013) Effects of maternal exposure to social stress during pregnancy: consequences for mother and offspring. Reproduction 146:R175–R189

    CAS  PubMed  Google Scholar 

  • Buffa G, Dahan S, Sinclair I, St-Pierre M, Roofigari N, Mutran D, Rondeau JJ, Dancause KN (2018) Prenatal stress and child development: a scoping review of research in low- and middle-income countries. PLoS One 13:e0207235

    CAS  PubMed  PubMed Central  Google Scholar 

  • Careau V, Réale D, Humphries MM, Thomas Donald W (2010) The pace of life under artificial selection: personality, energy expenditure, and longevity are correlated in domestic dogs. Am Nat 175:753–758

    PubMed  Google Scholar 

  • Chang S, Brent LJN, Adams G, Klein J, Pearson J, Watson K, Platt M (2013) Neuroethology of primate social behavior. P Natl Acad Sci USA 110:10387–10394

    CAS  Google Scholar 

  • Chapais B (1995) Alliances as a means of competition in primates: evolutionary, developmental, and cognitive aspects. Yearb Phys Anthropol 38:115–136

    Google Scholar 

  • Cheney DL, Seyfarth RM, Silk JB (1995) The responses of female baboons (Papio cynocephalus ursinus) to anomalous social interactions: evidence for causal reasoning? J Comp Psychol 109:134–141

    CAS  PubMed  Google Scholar 

  • Cheney DL, Silk JB, Seyfarth RM (2016) Network connections, dyadic bonds and fitness in wild female baboons. R Soc Open Sci 3:160255. https://doi.org/10.1098/rsos.160255

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke AS, Schneider ML (1993) Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys. Dev Psychobiol 26:293–304

    CAS  PubMed  Google Scholar 

  • Clarke AS, Schneider ML (1997) Effects of prenatal stress on behavior in adolescent rhesus monkeys. Ann N Y Acad Sci 807:490–491

    CAS  PubMed  Google Scholar 

  • Clarke AS, Bergholz A, Schneider T, Mary L (1996) Maternal gestational stress alters adaptive and social behavior in adolescent rhesus monkey offspring. Infant Behav Dev 19:451–461

    Google Scholar 

  • Coe CL, Lubach GR (2008) Fetal programming - prenatal origins of health and illness. Curr Dir Psychol Sci 17:36–41

    Google Scholar 

  • Coe CL, Lulbach GR, Schneider ML (2002) Prenatal disturbance alters the size of the corpus callosum in young monkeys. Dev Psychobiol 41:178–185

    PubMed  Google Scholar 

  • Coe CL, Kramer M, Czéh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025–1034

    CAS  PubMed  Google Scholar 

  • Connor RC (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philos Trans R Soc B 362:587–602

    Google Scholar 

  • Crockford C, Deschner T, Wittig RM (2018) The role of oxytocin in social buffering: what do primate studies add? Curr Top Behav Neurosci 35:155–173. https://doi.org/10.1007/7854_2017_12

    Article  CAS  PubMed  Google Scholar 

  • Cui J, Mistur EJ, Wei C, Lansford JE, Putnick DL, Bornstein MH (2018) Multilevel factors affecting early socioemotional development in humans. Behav Ecol Sociobiol 72:172. https://doi.org/10.1007/s00265-018-2580-9

    Article  Google Scholar 

  • Dammhahn M, Dingemanse NJ, Niemelä PT, Réale D (2018) Pace-of-life syndromes: a framework for the adaptive integration of behaviour, physiology and life history. Behav Ecol Sociobiol 72:62. https://doi.org/10.1007/s00265-018-2473-y

    Article  Google Scholar 

  • Dantzer R (2004) Cytokine-induced sickness behaviour: a neuroimmune response to activation of innate immunity. Eur J Pharmacol 500:399–411

    CAS  PubMed  Google Scholar 

  • Davis EP, Sandman CA (2010) The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Dev 81:131–148

    PubMed  PubMed Central  Google Scholar 

  • Davis EP, Stout SA, Molet J, Vegetabile B, Glynn LM, Sandman CA, Heins K, Stern H, Baram TZ (2017) Exposure to unpredictable maternal sensory signals influences cognitive development across species. P Natl Acad Sci USA 114:10390–11039

    CAS  Google Scholar 

  • de Rooij SR, Wouters H, Yonker JE, Painter RC, Roseboom TJ (2010) Prenatal undernutrition and cognitive function in late adulthood. P Natl Acad Sci USA 107:16881–16886

    Google Scholar 

  • de Waal FBM (1992) Aggression as a well-integrated part of primate social relationships: a critique of the Seville statement on violence. In: Silverberg J, Gray J (eds) Aggression and peacefulness in humans and other primates. Oxford University Press, Oxford, pp 37–56

    Google Scholar 

  • de Waal FBM, Luttrell LM (1989) Toward a comparative socioecology of the genus Macaca: different dominance styles in rhesus and stumptailed macaques. Am J Primatol 19:83–109

    Google Scholar 

  • De Witt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81

    Google Scholar 

  • Deaner RO, Khera AV, Platt ML (2005) Monkeys pay per view: adaptive valuation of social images by rhesus macaques. Curr Biol 15:543–548

    CAS  PubMed  Google Scholar 

  • Del Giudice M (2014a) Early stress and human behavioral development: emerging evolutionary perspectives. J Dev Orig Hlth Dis 5:270–280

    Google Scholar 

  • Del Giudice M (2014b) Life history plasticity in humans: the predictive value of early cues depends on the temporal structure of the environment. Proc R Soc B 281:20132222

    PubMed  Google Scholar 

  • Dettmer AM, Murphy AM, Guitarra D, Slonecker E, Suomi SJ, Rosenberg KL, Novak MA, Meyer JS, Hinde K (2018) Cortisol in neonatal mother’s milk predicts later infant social and cognitive functioning in rhesus monkeys. Child Dev 89:525–538

    PubMed  Google Scholar 

  • Dingemanse NJ, Kazem AJ, Réale D, Wright J (2010) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89

    PubMed  Google Scholar 

  • Dmitriew CM (2011) The evolution of growth trajectories: what limits growth rate? Biol Rev 86:97–116

    PubMed  Google Scholar 

  • Dodson S (1989) Predator-induced reaction norms: cyclic changes in shape and size can be protective. BioScience 39:447–452

    Google Scholar 

  • Douhard M, Plard F, Gaillard J-M, Capron G, Delorme D, Klein F, Duncan P, Loe LE, Bonenfant C (2014) Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate. Proc R Soc B 281:20140276

    PubMed  Google Scholar 

  • Dunbar RIM (1992) Time: a hidden constraint on the behavioural ecology of baboons. Behav Ecol Sociobiol 31:35–49

    Google Scholar 

  • Duthie L, Reynolds RM (2013) Changes in the maternal hypothalamic-pituitary-adrenal axis in pregnancy and postpartum: influences on maternal and fetal outcomes. Neuroendocrinology 98:106–115

    CAS  PubMed  Google Scholar 

  • Ebenau A, von Borell C, Penke L, Ostner J, Schülke O (2019) Personality homophily affects male social bonding in wild Assamese macaques (Macaca assamensis). Anim Behav (published online, doi:https://doi.org/10.1101/520064) https://doi.org/10.1101/520064)

  • Eisenegger C, Haushofer J, Fehr E (2011) The role of testosterone in social interaction. Trends Cogn Sci 15:263–271

    CAS  PubMed  Google Scholar 

  • Ellis BJ, Del Giudice M (2019) Developmental adaptation to stress: an evolutionary perspective. Annu Rev Psychol 70:111–139

    PubMed  Google Scholar 

  • Frankenhuis W, E., Nettle D, Dall SR (2019) A case for environmental statistics of early-life effects. Philos Trans R Soc B 374:20180110

    Google Scholar 

  • Franz M, McLean E, Tung J, Altmann J, Alberts SC (2015) Self-organizing dominance hierarchies in a wild primate population. Proc R Soc B 282:20151512

    PubMed  Google Scholar 

  • Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc B 367:1785–1801

    Google Scholar 

  • Fröhlich M, Hobaiter C (2018) The development of gestural communication in great apes. Behav Ecol Sociobiol 72:194

    Google Scholar 

  • Fruteau C, Voelkl B, van Damme E, Noë R (2009) Supply and demand determine the market value of food providers in wild vervet monkeys. P Natl Acad Sci USA 106:12007–12012

    CAS  Google Scholar 

  • Garber PA, Dolins FL (2014) Primate spatial strategies and cognition: introduction to this special issue. Am J Primatol 76:393–398

    PubMed  Google Scholar 

  • Gilby IC, Brent LJN, Wroblewski EE, Rudicell RS, Hahn BH, Goodall J, Pusey AE (2013) Fitness benefits of coalitionary aggression in male chimpanzees. Behav Ecol Sociobiol 67:373–381

    PubMed  Google Scholar 

  • Glover V (2011) Prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52:356–367

    PubMed  Google Scholar 

  • Gluckman PD, Hanson MA, Spencer HG (2005) Predictive adaptive responses and human evolution. Trends Ecol Evol 20:527–533

    PubMed  Google Scholar 

  • Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 454–471

    Google Scholar 

  • Groothuis TG, Maestripieri D (2013) Parenatal influneces on offspring personality traits in oviparous and placental vertebrates. In: Carere C, Maestriperi D (eds) Animal personality - behavior, physiology and evolution. University of Chicago Press, Chicago, pp 317–352

    Google Scholar 

  • Groothuis TGG, Taborsky B (2015) Introducing biological realism into the study of developmental plasticity in behaviour. Front Zool 12:S6

    PubMed  PubMed Central  Google Scholar 

  • Gutleb DR, Roos C, Noll A, Ostner J, Schülke O (2017) COMT Val158Met moderates the link between rank and aggression in a non-human primate. Genes Brain Behav 17:e12443

    PubMed  Google Scholar 

  • Hales CN, Barker DJP (2001) The thrifty phenotype hypothesis: type 2 diabetes Brit Med Bull 60:5-20

  • Hämäläinen A, Immonen E, Tarka M, Schuett W (2018) Evolution of sex-specific pace-of-life syndromes: causes and consequences. Behav Ecol Sociobiol 72:50

    Google Scholar 

  • Hanson KN, Gluckman PD (2014) Early developmental conditioning of later health and disease: physiology or pathophysiology? Physiol Rev 94:1027–1076

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hardy ICW, Briffa M (2013) Animal contests. Cambridge University Press, Cambridge

    Google Scholar 

  • Hauser J, Dettling-Artho A, Pilloud S, Maier C, Knapman A, Feldon J, Pryce CR (2007) Effects of prenatal dexamethasone treatment on postnatal physical, endocrine, and social development in the common marmoset monkey. Endocrinology 148:1813–1822

    CAS  PubMed  Google Scholar 

  • Hauser J, Knapmann A, Zürcher NR et al (2008) Effects of prenatal dexamethasone treatment on physical growth, pituitary-adrenal hormones, and performance of motor, motivational, and cognitive tasks in juvenile and adolescent common marmoset monkeys. Endocrinology 149:6343–6355

    CAS  PubMed  Google Scholar 

  • Hendry AP (2015) Key questions on the role of phenotypic plasticity in eco-evolutionary dynamics. J Hered 107:25–41

    PubMed  Google Scholar 

  • Hennessy MB, Deak T, Schiml PA (2014) Sociality and sickness: have cytokines evolved to serve social functions beyond times of pathogen exposure? Brain Behav Immun 37:15–20

    CAS  PubMed  Google Scholar 

  • Hennessy MB, Kaiser S, Tiedtke T, Sachser N (2015) Stability and change: stress responses and the shaping of behavioral phenotypes over the life span. Front Zool 12:S18. https://doi.org/10.1186/1742-9994-12-s1-s18

    Article  PubMed  PubMed Central  Google Scholar 

  • Hinde K, Capitanio JP (2010) Lactational programming? Mother’s milk energy predicts infant behavior and temperament in rhesus macaques (Macaca mulatta). Am J Primatol 72:522–529

    PubMed  PubMed Central  Google Scholar 

  • Hinde K, Skibiel AL, Foster AB, Del Rosso L, Mendoza SP, Capitanio JP (2015) Cortisol in mother’s milk across lactation reflects maternal life history and predicts infant temperament. Behav Ecol 26:269–281

    PubMed  Google Scholar 

  • Hoogenboom MO, Metcalfe NB, Armstrong JD, Groothuis TGG (2012) The growth benefits of aggressive behavior vary with individual metabolism and resource predictability. Behav Ecol 24:253–261

    Google Scholar 

  • Hostinar CE, Gunnar MR (2013) The developmental effects of early life stress: an overview of current theoretical frameworks. Curr Dir Psychol Sci 22:400–406

    PubMed  PubMed Central  Google Scholar 

  • Huebner F, Fichtel C, Kappeler Peter M (2018) Linking cognition with fitness in a wild primate: fitness correlates of problem-solving performance and spatial learning ability. Philos Trans R Soc B 373:20170295

    Google Scholar 

  • Huttunen MO, Niskanen P (1978) Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry 35:429–431

    CAS  PubMed  Google Scholar 

  • Isbell LA, van Vuren D (1996) Differential costs of locational and social dispersal and their consequences for female group-living primates. Behaviour 133:1–36

    Google Scholar 

  • Janson C (2007) Experimental evidence for route integration and strategic planning in wild capuchin monkeys. Anim Cogn 10:341–356

    PubMed  Google Scholar 

  • Joly M, Micheletta J, De Marco A, Langermans JA, Sterck EHM, Waller BM (2017) Comparing physical and social cognitive skills in macaque species with different degrees of social tolerance. Proc R Soc B 284:20162738

    PubMed  Google Scholar 

  • Kaiser S, Sachser N (2009) Effects of prenatal social stress on offspring development: pathology or adaptation? Curr Dir Psychol Sci 18:118–121

    Google Scholar 

  • Kaiser S, Schwerdt B, Siegeler K, Sachser N (2015) Social instability during pregnancy and lactation alters female wild cavy offsprings’ endocrine status and behaviour later in life. Behaviour 152:837–859

    Google Scholar 

  • Kalbitzer U, Bergstrom ML, Carnegie SD, Wikberg EC, Kawamura S, Campos FA, Jack KM, Fedigan LM (2017) Female sociality and sexual conflict shape offspring survival in a Neotropical primate. P Natl Acad Sci USA 114:1892–1897

    CAS  Google Scholar 

  • Kapoor A, Matthews SG (2005) Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring. J Physiol 566:967–977

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB (2008) Higher risk of off-spring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65:146–152

    PubMed  Google Scholar 

  • King S, Dancause K, Turcotte-Tremblay AM, Veru F, Laplante DP (2012) Using natural disasters to study the effects of prenatal maternal stress on child health and development. Birth Defect Res 96:273–288

    CAS  Google Scholar 

  • Kinsella MT, Monk C (2009) Impact of maternal stress, depression and anxiety on fetal neurobehavioral development. Clin Obstet Gynecol 52:425–440

    PubMed  PubMed Central  Google Scholar 

  • Kiyokawa Y, Hennessy MB (2018) Comparative studies of social buffering: a consideration of approaches, terminology, and pitfalls. Neurosci Biobehav Rev 86:131–141

    PubMed  Google Scholar 

  • Konečná M, Lhota S, Weiss A, Urbánek T, Adamová T, Pluháček J (2008) Personality in free-ranging Hanuman langur (Semnopithecus entellus) males: subjective ratings and recorded behavior. J Comp Psychol 122:379–389

    PubMed  Google Scholar 

  • Konečná M, Weiss A, Lhota S, Wallner B (2012) Personality in barbary macaques (Macaca sylvanus): temporal stability and social rank. J Res Pers 46:581–590

    Google Scholar 

  • Korstjens A, Lugo Verhoeckx I, Dunbar R (2006) Time as a constraint on group size in spider monkeys. Behav Ecol Sociobiol 60:683–694

    Google Scholar 

  • Koski SE, Burkart JM (2015) Common marmosets show social plasticity and group-level similarity in personality. Sci Rep 5:8878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kuzawa CW, Quinn EA (2007) Developmental origins of adult function and health: evolutionary hypotheses. Annu Rev Anthropol 38:131–147

    Google Scholar 

  • Laplante DP, Brunet A, Schmitz N, Ciampi A, King S (2008) Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5-year-old children. J Am Acad Child Psy 47:1063–1072

    Google Scholar 

  • Lea AJ, Altmann J, Alberts SC, Tung J (2015) Developmental constraints in a wild primate. Am Nat 185:809–821

    PubMed  PubMed Central  Google Scholar 

  • Lea AJ, Tung J, Archie EA, Alberts SC (2017) Developmental plasticity research in evolution and human health - response to commentaries. Evol Med Public Health 2017:201–205

    PubMed  Google Scholar 

  • Lea AJ, Akinyi MY, Nyakundi R, Mareri P, Nyundo F, Kariuki T, Alberts SC, Archie EA, Tung J (2018) Dominance rank-associated gene expression is widespread, sex-specific, and a precursor to high social status in wild male baboons. P Natl Acad Sci USA 115:E12163–E12171

    CAS  Google Scholar 

  • Lemaître J-F, Berger V, Bonenfant C, Douhard M, Gamelon M, Plard F, Gaillard J-M (2015) Early-late life trade-offs and the evolution of ageing in the wild. Proc R Soc B 282:20150209. https://doi.org/10.1098/rspb.2015.0209

    Article  PubMed  Google Scholar 

  • Li J, Olsen J, Vestergaard M, Oble C (2010) Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. Eur Child Adolesc Psychiatry 10:747–753

    Google Scholar 

  • Li N, Wang Y, Zhao X, Gao Y, Song M, Yu L, Wang L, Li N, Chen Q, Li Y, Cai J, Wang X (2015) Long-term effect of early-life stress from earthquake exposure on working memory in adulthood. Neuropsychiatr Dis Treat 11:2959–2965

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lonsdorf EV, Stanton MA, Murray CM (2018) Sex differences in maternal sibling-infant interactions in wild chimpanzees. Behav Ecol Sociobiol 72:117. https://doi.org/10.1007/s00265-018-2531-5

    Article  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445

    CAS  PubMed  Google Scholar 

  • MacLean EL, Merritt DJ, Brannon EM (2008) Social complexity predicts transitive reasoning in prosimian primates. Anim Behav 76:479–486

    PubMed  PubMed Central  Google Scholar 

  • Madrid JE, Mandalaywala TM, Coyne SP, Ahloy-Dallaire J, Barr CS, Maestripieri D, Parker KJ (2018) Adaptive developmental plasticity in rhesus macaques: the serotonin transporter gene interacts with maternal care to affect juvenile social behaviour. Proc R Soc B 285:20180541

    PubMed  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, Chicago University Press, Chicago, pp 256–291

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

    Article  Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Markham AC, Gesquiere LR (2017) Costs and benefits of group living in primates: an energetic perspective. Philos Trans R Soc B 372:20160239

    Google Scholar 

  • Massen JJM, Sterck EHM, de Vos H (2010) Close social associations in animals and humans - functions and mechanisms of friendship. Behaviour 147:1379–1412

    Google Scholar 

  • Mastorci F, Vicentini M, Viltart O, Manghi M, Graiani G, Quaini F, Meerlo P, Nalivaiko E, Maccari S, Sgoifo A (2009) Long-term effects of prenatal stress: changes in adult cardiovascular regulation and sensitivity to stress. Neurosci Biobehav Rev 33:191–203

    PubMed  Google Scholar 

  • Maynard Smith J, Parker GA (1976) The logic of asymmetric contests. Anim Behav 24:159–175

    Google Scholar 

  • McFarland R, Fuller A, Hetem RS, Mitchell D, Maloney SK, Henzi SP, Barrett L (2015) Social integration confers thermal benefits in a gregarious primate. J Anim Ecol 84:871–878

    PubMed  Google Scholar 

  • McFarland R, Murphy D, Lusseau D, Henzi SP, Parker JL, Pollet TV, Barrett L (2017) The ‘strength of weak ties’ among female baboons: fitness-related benefits of social bonds. Anim Behav 126:101–106

    Google Scholar 

  • McGowan PO, Matthews SG (2018) Prenatal stress, glucocorticoids and developmental programming of the stress response. Endocrinology 159:69–82

    PubMed  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    PubMed  Google Scholar 

  • Meyer JS, Hamel AF (2014) Models of stress in nonhuman primates and their relevance for human psychopathology and endocrine dysfunction. ILAR J 55:347–360

    CAS  PubMed  PubMed Central  Google Scholar 

  • Michaelis T, Abaei A, Boretius S, Tammer R, Frahm J, Schlumbohm C, Fuchs E (2009) Intrauterine hyperexposure to dexamethasone of the common marmoset monkey revealed normal cerebral metabolite concentrations in adulthood as assessed by quantitative proton magnetic resonance spectroscopy in vivo. J Med Primatol 38:213–218

    CAS  PubMed  Google Scholar 

  • Miller LE (2002) Eat or be eaten - risk sensitive foraging among primates. Cambridge University Press, Cambridge

    Google Scholar 

  • Moisiadis VG, Matthews SG (2014a) Glucocorticoids and fetal programming part 1: outcomes. Nat Rev Endocrinol 10:391. https://doi.org/10.1038/nrendo.2014.73

    Article  CAS  PubMed  Google Scholar 

  • Moisiadis VG, Matthews SG (2014b) Glucocorticoids and fetal programming part 2: mechanisms. Nat Rev Endocrinol 10:403. https://doi.org/10.1038/nrendo.2014.74

    Article  CAS  PubMed  Google Scholar 

  • Monaghan P (2008) Early growth conditions, phenotypic development and environmental change. Philos Trans R Soc B 363:1635–1645

    Google Scholar 

  • Montiglio P-O, Dammhahn M, Dubuc Messier G, Réale D (2018) The pace-of-life syndrome revisited: the role of ecological conditions and natural history on the slow-fast continuum. Behav Ecol Sociobiol 72:116. https://doi.org/10.1007/s00265-018-2526-2

    Article  Google Scholar 

  • Müller-Klein N, Heistermann M, Strube C, Morbach ZM, Lilie N, Franz M, Schülke O, Ostner J (2018) Physiological and social consequences of gastrointestinal nematode infection in a nonhuman primate. Behav Ecol 30:322–335

    Google Scholar 

  • 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:R156–R157

    CAS  PubMed  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

    Google Scholar 

  • Mustoe AC, Taylor JH, Birnie AK, Huffman MC, French JA (2014) Gestational cortisol and social play shape development of marmosets' HPA functioning and behavioral responses to stressors. Dev Psychobiol 56:1229–1243

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nettle D, Bateson M (2015) Adaptive developmental plasticity: what is it, how can we recognize it and when can it evolve? Proc R Soc B 282:20151005

    PubMed  Google Scholar 

  • Nettle D, Frankenhuis WE, Rickard IJ (2013) The evolution of predictive adaptive responses in human life history. Proc R Soc B 280:20131343

    PubMed  Google Scholar 

  • Neuenschwander R, Oberlander TF (2017) Developmental origins of self-regulation: prenatal maternal stress and psychobiological development during childhood. In: Deater-Deckard K, Panneton R (eds) Parental stress and early child development: adaptive and maladaptive outcomes. Springer, New York, pp 127–156

    Google Scholar 

  • Noë R, Sluijter AA (1995) Which adult male savanna baboons form coalitions? Int J Primatol 16:77–105

    Google Scholar 

  • O’Connor TG, Heron J, Glover V, the ALSPAC Study Team (2002) Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J Am Acad Child Psy 41:1470–1477

    Google Scholar 

  • Ostner J, Schülke O (2014) The evolution of social bonds in primate males. Behaviour 151:871–906

    Google Scholar 

  • Ostner J, Schülke O (2018) Linking sociality to fitness in primates: a call for mechanisms. Adv Study Behav 50:127–175

    Google Scholar 

  • Ostner J, Nunn CL, Schülke O (2008) Female reproductive synchrony predicts skewed paternity across primates. Behav Ecol 19:1150–1158

    PubMed  PubMed Central  Google Scholar 

  • Palmer AC (2011) Nutritionally mediated programming of the developing immune system. Adv Nutr 2:377–395

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paz-y-Mino-C G, Bond AB, Kamil AC, Balda RP (2004) Pinyon jays use transitive inference to predict social dominance. Nature 430:778–781

    CAS  PubMed  Google Scholar 

  • Pearce E, Wlodarski R, Machin A, Dunbar RIM (2017) Variation in the β-endorphin, oxytocin, and dopamine receptor genes is associated with different dimensions of human sociality. P Natl Acad Sci USA 114:5300–5305

    CAS  Google Scholar 

  • Perry S, Barrett HC, Manson JH (2004) White-faced capuchin monkeys show triadic awareness in their choice of allies. Anim Behav 67:165–170

    Google Scholar 

  • Perry S, Godoy I, Lammers W, Lin A (2017) Impact of personality traits and early life experience on timing of emigration and rise to alpha male status for wild male white-faced capuchin monkeys (Cebus capucinus) at Lomas Barbudal Biological Reserve, Costa Rica. Behaviour 154:195–226

    Google Scholar 

  • Petersen MB, Aarøe L (2015) Birth weight and social trust in adulthood: evidence for early calibration of social cognition. Psychol Sci 26:1681–1692

    PubMed  Google Scholar 

  • Piekarski DJ, Johnson CM, Boivin JR, Thomas AW, Lin WC, Delevich K, M Galarce E, Wilbrecht L (2017) Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? Brain Res 1654B:123–144

    CAS  PubMed  Google Scholar 

  • Piquer B, Fonseca JL, Lara HE (2017) Gestational stress, placental norepinephrine transporter and offspring fertility. Reproduction 153:147–155

    CAS  PubMed  Google Scholar 

  • Pryce CR, Aubert Y, Maier C, Pearce PC, Fuchs E (2011) The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology 214:33–53

    CAS  PubMed  Google Scholar 

  • Pusey A (2012) Magnitude and sources of variation in female reproductive performance. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 343–366

    Google Scholar 

  • Ravelli G-P, Stein ZA, Susser MW (1976) Obesity in young men after famine exposure in utero and early infancy. N Engl J Med 295:349–353

    CAS  PubMed  Google Scholar 

  • Réale D, Garant D, Humphries Murray M, Bergeron P, Careau V, Montiglio P-O (2010) Personality and the emergence of the pace-of-life syndrome concept at the population level. Philos Trans R Soc B 365:4051–4063

    Google Scholar 

  • Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468

    Google Scholar 

  • Rijlaarsdam J, van Ijzendoorn MH, Verhulst FC, Jaddoe VWV, Felix JF, Tiemeier H, Bakermans-Kranenburg MJ (2016) Prenatal stress exposure, oxytocin receptor gene (OXTR) methylation and child autistic traits: the moderating role of OXTR rs53576 genotype. Autism Res 10:430–438

    PubMed  PubMed Central  Google Scholar 

  • Roberts AD, Moore CF, DeJesus OT et al (2004) Prenatal stress, moderate fetal alcohol, and dopamine system function in rhesus monkeys. Neurotoxicol Teratol 26:169–178

    CAS  PubMed  Google Scholar 

  • Rodriguez-Llanes JM, Verbeke G, Finlayson C (2009) Reproductive benefits of high social status in male macaques (Macaca). Anim Behav 78:643–649

    Google Scholar 

  • Romero L (2004) Physiological stress in ecology: lessons from biomedical research. Trends Ecol Evol 19:249–255

    PubMed  Google Scholar 

  • Romero LM, Dickens MJ, Cyr NE (2009) The reactive scope model - a new model integrating homeostasis, allostasis, and stress. Horm Behav 55:375–389

    PubMed  Google Scholar 

  • Rosati AG, Arre AM, Platt ML, Santos LR (2018) Developmental shifts in social cognition: socio-emotional biases across the lifespan in rhesus monkeys. Behav Ecol Sociobiol 72:163

    Google Scholar 

  • Roseboom T, de Rooij S, Painter R (2006) The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82:485–491

    PubMed  Google Scholar 

  • Roseboom TJ, Painter RC, van Abeelen AFM, Veenendaal MVE, de Rooij SR (2011) Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas 70:141–145

    PubMed  Google Scholar 

  • Royauté R, Berdal MA, Garrison CR, Dochtermann NA (2018) Paceless life? A meta-analysis of the pace-of-life syndrome hypothesis. Behav Ecol Sociobiol 72:64

    Google Scholar 

  • Sachser N (1986) Different forms of social organization at high and low population densities in guinea pigs. Behaviour 97:253–272

    Google Scholar 

  • Sachser N, Kaiser S, Hennessy MB (2013) Behavioural profiles are shaped by social experience: when, how and why. Philos Trans R Soc B 368:20120344. https://doi.org/10.1098/rstb.2012.0344

    Article  CAS  Google Scholar 

  • Sachser N, Hennessy MB, Kaiser S (2018) The adaptive shaping of social behavioural phenotypes during adolescence. Biol Lett 14:20180536

    PubMed  Google Scholar 

  • Sandi C, Haller J (2015) Stress and the social brain: behavioural effects and neurobiological mechanisms. Nat Rev Neurosci 16:290–304

    CAS  PubMed  Google Scholar 

  • Sapolsky R (2002) Endocrinology of the stress-response. In: Becker J, Breedlove S, Crews D, McCarthy M (eds) Behavioral endocrinology, 2nd edn. The MIT Press, Cambridge, pp 409–450

    Google Scholar 

  • Schino G, Sciarretta M (2016) Patterns of social attention in mandrills, Mandrillus sphinx. Int J Primatol 37:752–761

    Google Scholar 

  • Schino G, Tiddi B, Polizzi Di Sorrentino E (2006) Simultaneous classification by rank and kinship in Japanese macaques. Anim Behav 71:1069–1074

    Google Scholar 

  • Schmitt CA, Di Fiore A (2015) Predation risk sensitivity and the spatial organization of primate groups: a case study using GIS in lowland woolly monkeys (Lagothrix lagotricha poeppigii). Am J Phys Anthropol 156:158–165

    PubMed  Google Scholar 

  • Schneider ML (1992) Prenatal stress exposure alters postnatal behavioral expression under conditions of novelty challenge in rhesus monkey infants. Dev Psychobiol 25:529–540

    CAS  PubMed  Google Scholar 

  • Schneider ML, Coe C (1993) Repeated social stress during pregnancy impairs neuromotor development of the primate infant. J Dev Behav Pediatr 14:81–87

    CAS  PubMed  Google Scholar 

  • Schneider ML, Suomi SJ (1992) Neurobehavioral assessment in rhesus monkey neonates (Macaca mulatta): developmental changes, behavioral stability, and early experience. Infant Behav Dev 15:155–177

    Google Scholar 

  • Schneider ML, Roughton EC, Koehler AJ, Lubach GR (1999) Growth and development following prenatal stress exposure in primates: an examination of ontogenetic vulnerability. Child Dev 70:263–274

    CAS  PubMed  Google Scholar 

  • Schneider ML, Moore CF, Roberts AD, Dejesus O (2001) Prenatal stress alters early neurobehavior, stress reactivity and learning in non-human primates: a brief review. Int J Biol Stress 4:183–193

    CAS  Google Scholar 

  • Schneider ML, Moore CF, Kraemer GW (2004) Moderate level alcohol during pregnancy, prenatal stress, or both and limbic-hypothalamic-pituitary-adrenocortical axis response to stress in rhesus monkeys. Child Dev 75:96–109

    PubMed  Google Scholar 

  • Schuett W, Dall S, Royle N (2011) Pairs of zebra finches with similar ‘personalities’ make better parents. Anim Behav 81:609–618

    Google Scholar 

  • Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani JC, Call J, Kappeler PM, Palombit RA, Silk JB (eds) The evolution of primate societies. The University of Chicago Press, Chicago, pp 195–219

    Google Scholar 

  • Schülke O, Bhagavatula J, Vigilant L, Ostner J (2010) Social bonds enhance reproductive success in male macaques. Curr Biol 20:2207–2210

    PubMed  Google Scholar 

  • Selye H (1976) The stress of life. McGraw-Hill, New York

    Google Scholar 

  • Seyfarth RM, Cheney DL (2012) The evolutionary origins of friendship. Annu Rev Psychol 63:153–177

    PubMed  Google Scholar 

  • Seyfarth RM, Cheney DL (2015) Social cognition. Anim Behav 103:191–202

    Google Scholar 

  • Shepherd SV, Deaner RO, Platt ML (2006) Social status gates social attention in monkeys. Curr Biology 16:R119–R120

    CAS  PubMed  Google Scholar 

  • Sheriff MJ, Bell A, Boonstra R et al (2017) Integrating ecological and evolutionary context in the study of maternal stress. Integr Comp Biol 57:437–449

    PubMed  PubMed Central  Google Scholar 

  • Silk J (1992) The patterning of intervention among male bonnet macaques: reciprocity, revenge, and loyalty. Curr Anthropol 33:318–325

    Google Scholar 

  • Silk JB (2002) Practice random acts of aggression and senseless acts of intimidation: the logic of status contests in social groups. Evol Anthropol 11:221–225

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2009) The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proc R Soc Lond B 276:3099–3104

    Google Scholar 

  • Silk JB, Beehner JC, Bergamn TJ, Crockford C, Engh AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20:1359–1361

    CAS  PubMed  Google Scholar 

  • Silk JB, Seyfarth RM, Cheney DL (2018) Quality versus quantity: do weak bonds enhance the fitness of female baboons? Anim Behav 140:207–211

    Google Scholar 

  • Simcock G, Kildea S, Elgbeili G, Laplante DP, Stapleton H, Cobham V, King S (2016) Age-related changes in the effects of stress in pregnancy on infant motor development by maternal report: the Queensland Flood Study. Dev Psychobiol 58:640–659

    PubMed  Google Scholar 

  • Simcock G, Kildea S, Elgbeili G, Laplante DP, Cobham V, King S (2017) Prenatal maternal stress shapes children’s theory of mind: the QF2011 Queensland Flood Study. J Dev Orig Hlth Dis 8:483–492

    CAS  Google Scholar 

  • Skoluda N, Nater UM (2013) Consequences of developmental stress in humans: prenatal stress. In: Laviola G, Macrì S (eds) Adaptive and maladaptive aspects of developmental stress. Springer, New York, pp 121–146

    Google Scholar 

  • Snyder-Mackler N, Sanz J, Kohn JN et al (2016) Social status alters immune regulation and response to infection in macaques. Science 354:1041–1045

    CAS  PubMed  PubMed Central  Google Scholar 

  • Snyder-Mackler N, Sanz J, Kohn JN, Voyles T, Pique-Regi R, Wilson ME, Barreiro LB, Tung J (2019) Social status alters chromatin accessibility and the gene regulatory response to glucocorticoid stimulation in rhesus macaques. P Natl Acad Sci USA 116:1219–1228

    CAS  Google Scholar 

  • Spitze K (1992) Predator-mediated plasticity of prey life history and morphology: Chaoborus americanus predation on Daphnia pulex. Am Nat 139:229–247

    Google Scholar 

  • Sullivan EL, Grayson B, Takahashi D, Robertson N, Maier A, Bethea CL, Smith MS, Coleman K, Grove KL (2010) Chronic consumption of a high-fat diet during pregnancy causes perturbations in the serotonergic system and increased anxiety-like behavior in nonhuman primate offspring. J Neurosci 30:3826–3830

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sutherland S, Brunwasser SM (2018) Sex differences in vulnerability to prenatal stress: a review of the recent literature. Curr Psychiatry Rep 20:102

  • Taborsky B (2016) Opening the black box of developmental experiments: behavioural mechanisms underlying long-term effects of early social experience. Ethology 122:1–17

    Google Scholar 

  • Taborsky B (2017) Developmental plasticity: preparing for life in a complex world. Adv Study Behav 49:49–99

    Google Scholar 

  • Talge NM, Neal C, Glover V, the Early Stress, Translational Research and Prevention Science Network Fetal and Neonatal Experience on Child and Adolescent Mental Health (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261

    PubMed  Google Scholar 

  • Tao S, Dahl GE (2013) Heat stress effects during late gestation on dry cows and their calves. J Dairy Sci 96:4079–4093

    CAS  PubMed  Google Scholar 

  • Tauber SC, Schlumbohm C, Schilg L, Fuchs E, Nau R, Gerber J (2006) Intrauterine exposure to dexamethasone impairs proliferation but not neuronal differentiation in the dentate gyrus of newborn common marmoset monkeys. Brain Pathol 16:209–217

    CAS  PubMed  Google Scholar 

  • Tauber SC, Bunkowski S, Schlumbohm C, Rhlmann M, Fuchs E, Nau R, Gerber J (2008) No long-term effect two years after intrauterine exposure to dexamethasone on dentate gyrus volume, neuronal proliferation and differentiation in common marmoset monkeys. Brain Pathol 18:497–503

    CAS  PubMed  Google Scholar 

  • Thompson NA, Cords M (2018) Stronger social bonds do not always predict greater longevity in a gregarious primate. Ecol Evol 8:1604–1614

    PubMed  PubMed Central  Google Scholar 

  • Trillmich F, Günther A, Müller C, Reinhold K, Sachser N (2015) New perspectives in behavioural development: adaptive shaping of behaviour over a lifetime? Front Zool 12:S1. https://doi.org/10.1186/1742-9994-12-S1-S1

    Article  Google Scholar 

  • Tung J, Archie EA, Altmann J, Alberts SC (2016) Cumulative early life adversity predicts longevity in wild baboons. Nat Commun 7:11181. https://doi.org/10.1038/ncomms11181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uller T, Nakagawa S, English S (2013) Weak evidence for anticipatory parental effects in plants and animals. J Evol Biol 26:2161–2170

    CAS  PubMed  Google Scholar 

  • Uno H, Eisele S, Sakai A, Shelton S, Baker E, DeJesus O, Holden J (1994) Neurotoxicity of glucocorticoids in the primate brain. Horm Behav 28:336–348

    CAS  PubMed  Google Scholar 

  • van Hazebroek BCM, Wermink H, van Domburgh L, de Keijser JW, Hoeve M, Popma A (2018) Biosocial studies of antisocial behavior: a systematic review of interactions between peri/prenatal complications, psychophysiological parameters, and social risk factors. Aggress Violent Behav 47:169–188

    Google Scholar 

  • van Noordwijk MA, van Schaik CP (2001) Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour 138:359–395

    Google Scholar 

  • van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144

    Google Scholar 

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

    Google Scholar 

  • van Schaik CP, Aureli F (2000) The natural history of valuable relationships in primates. In: Aureli F, de Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, LA, pp 307–332

    Google Scholar 

  • van Schaik CP, Pandit S, Vogel E (2006) Toward a general model for male-male coalitions in primate groups. In: Kappeler P, van Schaik C (eds) Cooperation in primates and humans. Springer, Heidelberg, pp 151–172

    Google Scholar 

  • Varcin KJ, Alvares GA, Uljarević M, Whitehouse AJO (2017) Prenatal maternal stress events and phenotypic outcomes in autism spectrum disorder. Autism Res 10:1866–1877

    PubMed  Google Scholar 

  • Veru F, Laplante DP, Luheshi G, King S (2014) Prenatal maternal stress exposure and immune function in the offspring. Stress 17:133–148

    CAS  PubMed  Google Scholar 

  • von Borell C, Penke L, Weiss A (2019) Developing individual differences in primate behavior: the role of genes, environment and their interplay. Behav Ecol Sociobiol 73:20

    Google Scholar 

  • Walder JD, Laplante DP, Sousa-Pires A, Veru F, Brunet A, King S (2014) Prenatal maternal stress predicts autism traits in 6½ year-old children: Project Ice Storm. Psychiatry Res 219:353–360

    PubMed  Google Scholar 

  • Watt PJ, Ariyomo TO (2013) Disassortative mating for boldness decreases reproductive success in the guppy. Behav Ecol 24:1320–1326

    Google Scholar 

  • Weinstock M (2008) The longterm behavioural consequences of prenatal stress. Neurosci Biobehav Rev 32:1073–1086

    CAS  PubMed  Google Scholar 

  • Weinstock M (2015) Changes induced by prenatal stress in behavior and brain morphology: can they be prevented or reversed? In: Antonelli M (ed) Perinatal programming of neurodevelopment. Springer, New York, pp 3–25

    Google Scholar 

  • Wells JCK (2003) The thrifty phenotype hypothesis: thrifty offspring or thrifty mother? J Theor Biol 221:143–161

    PubMed  Google Scholar 

  • Wells JCK (2007) Flaws in the theory of predictive adaptive responses. Trends Endocrinol Metab 18:331–337

    CAS  PubMed  Google Scholar 

  • Wells JCK (2010) Maternal capital and the metabolic ghetto: an evolutionary perspective on the transgenerational basis of health inequalities. Am J Hum Biol 22:1–17

    PubMed  Google Scholar 

  • Wells JCK (2019) Developmental plasticity as adaptation: adjusting to the external environment under the imprint of maternal capital. Philos Trans R Soc B 374:20180122

    Google Scholar 

  • West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New York

    Google Scholar 

  • Whiten A, van de Waal E (2018) The pervasive role of social learning in primate lifetime development. Behav Ecol Sociobiol 72:80

    PubMed  PubMed Central  Google Scholar 

  • Widdig A, Streich WJ, Tembrock G (2000) Coalition formation among male barbary macaques (Macaca sylvanus). Am J Primatol 50:37–51

    CAS  PubMed  Google Scholar 

  • Willette AA, Lubach GR, Coe CL (2007) Environmental context differentially affects behavioral, leukocyte, cortisol, and interleukin-6 responses to low doses of endotoxin in the rhesus monkey. Brain Behav Immun 21:807–815

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wingfield JC, Hegner RE, Dufty AMJ, Ball GF (1990) The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Google Scholar 

  • Wittig RM, Crockford C, Weltring A, Langergraber KE, Deschner T, Zuberbühler K (2016) Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations. Nat Commun 7:13361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Young C, Majolo B, Heistermann M, Schülke O, Ostner J (2014a) Responses to social and environmental stress are attenuated by strong male bonds in wild macaques. P Natl Acad Sci USA 111:18195–18200

    CAS  Google Scholar 

  • Young C, Majolo B, Schülke O, Ostner J (2014b) Male social bonds and rank predict supporter selection in cooperative aggression in wild barbary macaques. Anim Behav 95:23–32

    Google Scholar 

  • Young C, Majolo B, Schülke O, Ostner J (2014c) Male social bonds predict partner recruitment in cooperative aggression in wild barbary macaques. Anim Behav 80:675–682

    Google Scholar 

  • Zimmermann TD, Kaiser S, Hennessy MB, Sachser N (2017) Adaptive shaping of the behavioural and neuroendocrine phenotype during adolescence. Proc R Soc B 284:20162784

    PubMed  Google Scholar 

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Acknowledgments

We thank Anja Widdig and Federica Amici for the invitation to contribute to the topical collection on Primate Social Development, Melanie Dammhahn for sharing thoughts on POLS in the context of prenatal stress effects, two anonymous reviewers for very constructive comments, and members of the DFG Research Unit FOR 2136 Sociality and Health in Primates as well as members of the Leibniz Science Campus Primate Cognition for discussion.

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Authors and Affiliations

  1. Department of Behavioral Ecology, University of Goettingen, Kellnerweg 6, 37077, Goettingen, Germany

    Oliver Schülke & Julia Ostner

  2. Research Group Primate Social Evolution, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany

    Oliver Schülke & Julia Ostner

  3. Leibniz Science Campus Primate Cognition, German Primate Center, Leibniz Institute for Primate Research, Goettingen, Germany

    Oliver Schülke & Julia Ostner

  4. Department of Anthropology, University of New Mexico, Albuquerque, NM, USA

    Andreas Berghänel

  5. Konrad Lorenz Institute of Ethology - Domestication Laboratory, Department of Interdisciplinary Life Sciences, University of Veterinary Medicine Vienna, Vienna, Austria

    Andreas Berghänel

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Correspondence to Oliver Schülke.

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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

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Schülke, O., Ostner, J. & Berghänel, A. Prenatal maternal stress effects on the development of primate social behavior. Behav Ecol Sociobiol 73, 128 (2019). https://doi.org/10.1007/s00265-019-2729-1

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