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Identifying Proximate and Ultimate Causation in the Development of Primate Sex-Typed Social Behavior

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Building Babies

Part of the book series: Developments in Primatology: Progress and Prospects ((DIPR,volume 37))

Abstract

Much like adult body size dimorphism (Leigh 1992; Leigh and Terranova 1998; O’Mara et al. 2012), the diversity of sex differences in social behavior that characterize adult primates must develop during the postnatal period because primate infants are only subtly sexually differentiated in behavior at birth (e.g., Chlorocebus aethiops, Lee 1984; Papio anubis, Bentley-Condit 2003; Papio cynocephalus, Nguyen et al. 2010, 2012). To the extent that adult sex-typed social behaviors are an important element of adult behavioral competence and to the extent that adult behavioral competence translates into reproductive success, the proximate mechanisms underlying the development of sex-typed social behaviors will be targets of selection. Understanding how those proximate mechanisms function to produce sex-typed adult social behaviors will clarify the adaptive nature of adult sex roles by yielding insight into the factors that influence and/or constrain their development (Beaupre et al. 1998; Duvall and Beaupre 1998).

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References

  • Agostini I, Visalberghi E (2005) Social influences on the acquisition of sex-typical foraging patterns by juveniles in a group of wild tufted capuchin monkeys (Cebus nigritus). Am J Primatol 65:335–351

    PubMed  Google Scholar 

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

    Google Scholar 

  • Altmann SA (1991) Diets of yearling female primates (Papio cynocephalus) predict lifetime fitness. Proc Natl Acad Sci USA 88:420–423

    PubMed  CAS  Google Scholar 

  • Altmann J, Alberts S (1987) Body mass and growth rates in a wild primate population. Oecologia 72:15–18

    Google Scholar 

  • Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501

    Google Scholar 

  • Altmann J, Altmann S (1981) Physical maturation and age estimates of yellow baboons, Papio cynocephalus, in Amboseli National Park, Kenya. Am J Primatol 1:389–399

    Google Scholar 

  • Altmann J, Pereira M (1985) Development of social behavior in free-living nonhuman primates. In: Watts E (ed) Nonhuman primate models for human growth and development. Alan R. Liss, New York, pp 217–309

    Google Scholar 

  • Altmann J, Lynch JW, Nguyen N, Alberts SC, Gesquiere LR (2004) Life-history correlates of steroid concentrations in wild peripartum baboons. Am J Primatol 64:95–106

    PubMed  Google Scholar 

  • Andrews M, Rosenblum L (1991) Security of attachment in infants raised in variable- or low-demand environments. Child Dev 62:686–693

    PubMed  CAS  Google Scholar 

  • Andrews MW, Rosenblum LA (1994) The development of affiliative and agonistic social patterns in differentially reared monkeys. Child Dev 65:1398–1404

    PubMed  CAS  Google Scholar 

  • Anestis SF (2006) Testosterone in juvenile and adolescent male chimpanzees (Pan troglodytes): effects of dominance rank, aggression, and behavioral style. Am J Phys Anthropol 130:536–545

    PubMed  Google Scholar 

  • Baldellou M, Adan ANA (1997) Time, gender, and seasonality in vervet activity: a chronobiological approach. Primates 38:31–43

    Google Scholar 

  • Bard KA, Gardner KH (1996) Influences on development in infant chimpanzees: enculturation, temperament, and cognition. In: Russon AE, Bard KA (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, Cambridge, pp 235–256

    Google Scholar 

  • Barthold J, Fichtel C, Kappeler P (2009) What is it going to be? Pattern and potential function of natal coat change in sexually dichromatic redfronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol 138:1–10

    PubMed  Google Scholar 

  • Beaupre S, Duvall D, O’Leile J (1998) Ontogenetic variation in growth and sexual size dimorphism in a central Arizona population of the western diamondback rattlesnake (Crotalus atrox). Copeia 1:40–47

    Google Scholar 

  • Becker JB (2009) Sexual differentiation of motivation: a novel mechanism? Horm Behav 55:646–654

    PubMed  CAS  Google Scholar 

  • Beehner JC, Phillips-Conroy JE, Whitten PL (2005) Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons. Am J Primatol 67:101–119

    PubMed  CAS  Google Scholar 

  • Beehner JC, Nguyen N, Wango EO, Alberts SC, Altmann J (2006) The endocrinology of pregnancy and fetal loss in wild baboons. Horm Behav 49:688–699

    PubMed  CAS  Google Scholar 

  • Beehner JC, Gesquiere L, Seyfarth RM, Cheney DL, Alberts SC, Altmann J (2009) Testosterone related to age and life-history stages in male baboons and geladas. Horm Behav 56:472–480

    PubMed  CAS  Google Scholar 

  • Bentley-Condit VK (2003) Sex differences in captive olive baboon behavior during the first fourteen days of life. Int J Primatol 24:1093–1112

    Google Scholar 

  • Boesch C, Boesch H (1981) Sex differences in the use of natural hammers by wild chimpanzees: a preliminary report. J Hum Evol 10:585–593

    Google Scholar 

  • Borries C, Lu A, Ossi-Lupo K, Larney E, Koenig A (2011) Primate life histories and dietary adaptations: a comparison of Asian colobines and macaques. Am J Phys Anthropol 144:286–299

    PubMed  Google Scholar 

  • Brockman D, Whitten P (1996) Reproduction in free-ranging Propithecus verreauxi: estrus and the relationship between multiple partner matings and fertilization. Am J Phys Anthropol 100:57–69

    PubMed  CAS  Google Scholar 

  • Brockman DK, Cobden AK, Whitten PL (2009) Birth season glucocorticoids are related to the presence of infants in sifaka (Propithecus verreauxi). Proc R Soc B Biol Sci 276:1855–1863

    CAS  Google Scholar 

  • Brown GR, Dixson AF (1999) Investigation of the role of postnatal testosterone in the expression of sex differences in behavior in infant rhesus macaques (Macaca mulatta). Horm Behav 35:186–194

    PubMed  CAS  Google Scholar 

  • Capitanio J (1984) Early experience and social processes in rhesus macaques (Macaca mulatta): I. Dyadic social interaction. J Comp Psychol 98:35–44

    Google Scholar 

  • Castracane VD, Copeland KC, Reyes P, Kuehl TJ (1986) Pubertal endocrinology of yellow baboon (Papio cynocephalus): plasma testosterone, testis size, body weight, and crown-rump length in males. Am J Primatol 11:263–270

    Google Scholar 

  • Cavigelli SA, Pereira ME (2000) Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm Behav 37:246–255

    PubMed  CAS  Google Scholar 

  • Chamove A, Harlow HF, Mitchell G (1967) Sex differences in the infant-directed behavior of preadolescent rhesus monkeys. Child Dev 38:329–335

    PubMed  CAS  Google Scholar 

  • Champoux M, Coe C, Schanberg S, Kuhn C, Suomi S (1989) Hormonal effects of early rearing conditions in the infant rhesus monkey. Am J Primatol 19:111–117

    Google Scholar 

  • Champoux M, Metz B, Suomi S (1991) Behavior of nursery/peer-reared and mother-reared rhesus monkeys from birth through 2 years of age. Primates 32:509–514

    Google Scholar 

  • Cheney D (1978) The play partners of immature baboons. Anim Behav 26:1038–1050

    Google Scholar 

  • Clarke MR (1990) Behavioral development and socialization of infants in a free-ranging group of howling monkeys. Folia Primatol 54:1–15

    PubMed  CAS  Google Scholar 

  • Clarke MR, Glander KE, Zucker EL (1998) Infant-nonmother interactions of free-ranging mantled howlers (Alouatta palliata) in Costa Rica. Int J Primatol 19:451–472

    Google Scholar 

  • Clarke M, Zucker E, Ford R, Harrison R (2007) Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata). Am J Primatol 69:477–484

    PubMed  CAS  Google Scholar 

  • Cords M (2000) Grooming partners of immature blue monkeys (Cercopithecus mitis) in the Kakamega Forest, Kenya. Int J Primatol 21:239–254

    Google Scholar 

  • Cords M, Sheehan MJ, Ekernas LS (2010) Sex and age differences in juvenile social priorities in female philopatric, nondespotic blue monkeys. Am J Primatol 72:193–205

    PubMed  Google Scholar 

  • Crockett CM, Pope TR (2002) Consequences of sex differences in dispersal for juvenile red howler monkeys. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. University of Chicago Press, Chicago, pp 104–118

    Google Scholar 

  • de A. Moura AC, Lee PC (2010) Wild capuchins show male-biased feeding tool use. Int J Primatol 31:457–470

    Google Scholar 

  • Deputte BL, Goy R (1991) Development of behavioral sexual differences: experimental study of prenatal Diethylstilbestrol (D.E.S.) female rhesus macaque infants. In: Ehara A, Kimura T, Takenaka O, Iwamoto M (eds) Primatology today. Elsevier, Amsterdam, pp 465–468

    Google Scholar 

  • Dittami J, Katina S, Möstl E, Eriksson J, Machatschke IH, Hohmann G (2008) Urinary androgens and cortisol metabolites in field-sampled bonobos (Pan paniscus). Gen Comp Endocrinol 155:552–557

    PubMed  CAS  Google Scholar 

  • Dixson AF (1993) Effects of testosterone propionate upon the sexual and aggressive behavior of adult male marmosets (Callithrix jacchus) castrated as neonates. Horm Behav 27:216–230

    PubMed  CAS  Google Scholar 

  • Dixson A, Nevison C (1997) The socioendocrinology of adolescent development in male rhesus monkeys (Macaca mulatta). Horm Behav 31:126–135

    PubMed  CAS  Google Scholar 

  • Duvall D, Beaupre S (1998) Sexual strategy and size dimorphism in rattlesnakes: integrating proximate and ultimate causation. Am Zool 38:152–165

    Google Scholar 

  • Eisler JA, Tannenbaum PL, Mann DR, Wallen K (1993) Neonatal testicular suppression with a GnRH agonist in rhesus monkeys – effects on adult endocrine function and behavior. Horm Behav 27:551–567

    PubMed  CAS  Google Scholar 

  • Ekernas L, Cords M (2007) Social and environmental factors influencing natal dispersal in blue monkeys, Cercopithecus mitis stuhlmanni. Anim Behav 73(6):1009–1018

    Google Scholar 

  • Förster S, Cords M (2002) Development of mother-infant relationships and infant behavior in wild blue monkeys (Cercopithecus mitis stuhlmanni). In: Glenn M, Cords M (eds) The guenons: diversity and adaptation in African monkeys. Klewer Academic/Plenum, New York, pp 245–272

    Google Scholar 

  • Förster S, Cords M (2005) Socialization of infant blue monkeys (Cercopithecus mitis stuhlmanni): allomaternal interactions and sex differences. Behaviour 142:869–896

    Google Scholar 

  • Gesquiere LR, Altmann J, Khan MZ, Couret J, Yu JC, Endres CS, Lynch JW, Ogola P, Ea F, Alberts SC (2005) Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus). Am J Primatol 67:83–100

    PubMed  CAS  Google Scholar 

  • Gesquiere LR, Khan M, Shek L, Wango TL, Wango EO, Alberts SC, Altmann J (2008) Coping with a challenging environment: effects of seasonal variability and reproductive status on glucocorticoid concentrations of female baboons (Papio cynocephalus). Horm Behav 54:410–416

    PubMed  CAS  Google Scholar 

  • Gesquiere LR, Onyango PO, Alberts SC, Altmann J (2010) Endocrinology of year-round ­reproduction in a highly seasonal habitat: environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 176:169–176

    Google Scholar 

  • Gesquiere LR, Learn NH, Simao MCM, Onyango PO, Alberts SC, Altmann J (2011) Life at the top: rank and stress in wild male baboons. Science 333:357–360

    PubMed  CAS  Google Scholar 

  • Ginther AJ, Carlson AA, Ziegler TE, Snowdon CT (2002) Neonatal and pubertal development in males of a cooperatively breeding primate, the cotton-top tamarin (Saguinus oedipus oedipus). Biol Reprod 66:282–290

    PubMed  CAS  Google Scholar 

  • Goldfoot DA (1977) Rearing conditions which support or inhibit later sexual potential of laboratory-born rhesus monkeys: hypotheses and diagnostic behaviors. Lab Anim Sci 27:548–556

    PubMed  CAS  Google Scholar 

  • Gould L (1990) The social development of free-ranging infant Lemur catta at Berenty Reserve, Madagascar. Int J Primatol 11:297–318

    Google Scholar 

  • Gould L (1997) Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta). Am J Phys Anthropol 103:163–171

    PubMed  CAS  Google Scholar 

  • Gould L, Ziegler TE (2007) Variation in fecal testosterone levels, inter-male aggression, dominance rank and age during mating and post-mating periods in wild adult male ring-tailed lemurs (Lemur catta). Am J Primatol 1339:1325–1339

    Google Scholar 

  • Gould L, Sussman RW, Sauther ML (2003) Demographic and life-history patterns in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly Reserve, Madagascar: a 15-year perspective. Am J Phys Anthropol 120:182–194

    PubMed  Google Scholar 

  • Goy R, Phoenix C (1971) The effects of testosterone propionate administered before birth on the development of behavior in genetic female rhesus monkeys. In: Geist V, Walther F (eds) Steroid hormones and brain function. University of California Press, Berkeley, pp 193–201

    Google Scholar 

  • Goy R, Wallen K (1979) Experiential variables influencing play, foot-clasp mounting and adult sexual competence in male rhesus monkeys. Psychoneuroendocrinology 4:1–12

    PubMed  CAS  Google Scholar 

  • Harlow HF (1962) The heterosexual affectional system in monkeys. Am Psychol 17:1–19

    Google Scholar 

  • Harlow HF (1965) Sexual behavior in the rhesus monkeys. In: Beach F (ed) Sex and behavior. Wiley, New York, pp 234–265

    Google Scholar 

  • Harrison M (1983) Age and sex differences in the diet and feeding strategies of the green monkey, Cercopithecus sabaeus. Anim Behav 31:969–977

    Google Scholar 

  • Herman R, Measday M, Wallen K (2003) Sex differences in interest in infants in juvenile rhesus monkeys: relationship to prenatal androgen. Horm Behav 43:573–583

    PubMed  CAS  Google Scholar 

  • Hoppitt W, Laland K (2008) Social processes influencing learning in animals: a review of the evidence. Adv Stud Behav 38:105–165

    Google Scholar 

  • Huck M, Lottker P, Heymann EW, Heistermann M (2005) Characterization and social correlates of fecal testosterone and cortisol excretion in wild male Saguinus mystax. Int J Primatol 26:159–179

    Google Scholar 

  • Johnson SE (2003) Life history and the competitive environment: trajectories of growth, maturation, and reproductive output among chacma baboons. Am J Phys Anthropol 120:83–98

    PubMed  Google Scholar 

  • Jolly A (1966) Lemur behavior. University of Chicago Press, Chicago

    Google Scholar 

  • Lee PC (1984) Early infant development and maternal care in free-ranging vervet monkeys. Primates 25:36–47

    Google Scholar 

  • Leigh S (1992) Patterns of variation in the ontogeny of primate body size dimorphism. J Hum Evol 23:27–50

    Google Scholar 

  • Leigh SR, Terranova CJ (1998) Comparative perspectives on bimaturism, ontogeny, and dimorphism in Lemurid primates. Int J Primatol 19:723–749

    Google Scholar 

  • Lonsdorf E (2004) Sex differences in learning in chimpanzees. Nature 428:715–716

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Lonsdorf E (2012) The role of mothers in the development of complex skills in chimpanzees. In: Clancy K, Hinde K, Rutherford J (eds) Building babies: primate development in proximate and ultimate perspective. Springer, New York

    Google Scholar 

  • MacKinnon KC (2012) Ontogeny of social behavior in the genus cebus and the application of an integrative framework for examining plasticity and complexity in evolution. In: Clancy K, Hinde K, Rutherford J (eds) Building babies: primate development in proximate and ultimate perspective. Springer, New York

    Google Scholar 

  • Maestripieri D (2005) Early experience affects the intergenerational transmission of infant abuse in rhesus monkeys. Proc Natl Acad Sci USA 102:9726–9729

    PubMed  CAS  Google Scholar 

  • Maestripieri D, Zehr J (1998) Maternal responsiveness increases during pregnancy and after estrogen treatment in macaques. Horm Behav 34:223–230

    PubMed  CAS  Google Scholar 

  • Mason W (1978) Social experience and primate cognitive development. In: Burghardt G, Beckoff M (eds) The development of behavior: comparative and evolutionary aspects. Garland STPM Press, New York, pp 233–251

    Google Scholar 

  • McCormack K, Sanchez MM, Bardi M, Maestripieri D (2006) Maternal care patterns and behavioral development of rhesus macaque abused infants in the first 6 months of life. Dev Psychobiol 48:537–550

    PubMed  CAS  Google Scholar 

  • McGraw WS, Vick AE, Daegling DJ (2010) Sex and age differences in the diet and ingestive behaviors of sooty mangabeys (Cercocebus atys) in the Tai forest, Ivory coast. Am J Phys Anthropol 153:140–153

    Google Scholar 

  • McGrew WC (1979) Evolutionary implications of sex differences in chimpanzee predation and tool use. In: Hamburg DA, McCown ER (eds) The great apes. B. Cummings, London, pp 441–463

    Google Scholar 

  • Meredith S (2012) Social influences on the development of sex-typed social behavior in Lemur catta [dissertation]. Arizona State University: Tempe, Available from: ProQuest Dissertations and Theses

    Google Scholar 

  • Meredith S, Fritz J (2005) Sex-differential rearing effects in Pan troglodytes. Am J Phys Anthropol Suppl. 40:151–152

    Google Scholar 

  • Milton K (2002) Diet and social organization of a free-ranging spider monkey population: the development of species-typical behavior in the absence of adults. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. University of Chicago Press, Chicago, pp 173–181

    Google Scholar 

  • Mondragón-Ceballos R, Chiappa P, Mayagoitia L, Lee P (2010) Sex differences in learning the allocation of social grooming in infant stumptailed macaques. Behaviour 147:1073–1099

    Google Scholar 

  • Muehlenbein MP, Campbell BC, Phillippi KM, Murchison MA, Richards RJ, Svec F, Myers L (2001) Reproductive maturation in a sample of captive male baboons. J Med Primatol 30:273

    PubMed  CAS  Google Scholar 

  • Muller M, Wrangham R (2004) Dominance, aggression, and testosterone in wild chimpanzees: a test of the ‘challenge hypothesis’. Anim Behav 67:113–123

    Google Scholar 

  • Nakagawa N (2000) Seasonal, sex, and interspecific differences in activity time budgets and diets of patas monkeys (Erythrocebus patas) and tantalus monkeys (Cercopithecus aethiops tantalus), living sympatrically in northern Cameroon. Primates 41:161–174

    Google Scholar 

  • Nash L (1978) The development of the mother-infant relationship in wild baboons (Papio anubis). Anim Behav 26:746–759

    Google Scholar 

  • Nguyen N, Gesquiere L, Wango E, Alberts S, Altmann J (2008) Late pregnancy glucocorticoid levels predict responsiveness in wild baboon mothers (Papio cynocephalus). Anim Behav 75:1747–1756

    Google Scholar 

  • Nguyen N, Gesquiere L, Alberts S, Altmann J (2010) Sex differences in the mother-infant relationship in wild baboons (Papio cynocephalus): social, experiential, and hormonal correlates. Am J Phys Anthropol Suppl. 50:177

    Google Scholar 

  • Nguyen N, Gesquiere L, Alberts S, Altmann J (2012) Sex differences in the mother-neonate relationships in wild baboons: social, experiential and hormonal correlates. Anim Behav (in press) doi:10.1016/j.anbehav.2012.01.003

  • Nikolei J, Borries C (1997) Sex differential behavior of immature Hanuman langurs (Presbytis entellus) in Ramnagar, South Nepal. Int J Primatol 18:415–437

    Google Scholar 

  • Nunn C (2011) The comparative method in evolutionary anthropology and biology. University of Chicago Press, Chicago, p 392

    Google Scholar 

  • O’Malley RC, Fedigan L (2005) Variability in food-processing behavior among white-faced capuchins (Cebus capucinus) in Santa Rosa National Park, Costa Rica. Am J Phys Anthropol 128:63–73

    PubMed  Google Scholar 

  • O’Mara M (2008) The influence of habitat quality on juvenile ring-tailed lemur (Lemur catta) feeding ecology and glucocorticoid levels. Am J Phys Anthropol Suppl. 46:165

    Google Scholar 

  • O’Mara MT (2012) Development of feeding in ring-tailed lemurs (Lemur catta) [dissertation]. Arizona State University: Tempe, Available from: ProQuest Dissertations and Theses

    Google Scholar 

  • O’Mara MT, Gordon AD, Catlett KK, Terranova CJ, Schwartz GT (2012) Growth and the development of sexual size dimorphism in lorises and galagos. Am J Phys Anthropol 147:11–18

    PubMed  Google Scholar 

  • Onyango PO, Gesquiere LR, Wango EO, Alberts SC, Altmann J (2008) Persistence of maternal effects in baboons: mother’s dominance rank at son’s conception predicts stress hormone levels in subadult males. Horm Behav 54:319–324

    PubMed  CAS  Google Scholar 

  • Ostner J, Heistermann M (2003) Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus). Gen Comp Endocrinol 131:274–283

    PubMed  CAS  Google Scholar 

  • Ostner J, Kappeler P, Heistermann M (2002) Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 52:485–495

    Google Scholar 

  • Ostner J, Kappeler P, Heistermann M (2008) Androgen and glucocorticoid levels reflect seasonally occurring social challenges in male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 62:627–638

    PubMed  Google Scholar 

  • Owens N (1975) Social play behaviour in free-living baboons. Anim Behav 23:387–408

    Google Scholar 

  • Palagi E, Gregorace A, Tarli SMB (2002) Development of olfactory behavior in captive ring-tailed lemurs (Lemur catta). Int J Primatol 23:587–599

    Google Scholar 

  • Pasterski VL, Geffner ME, Brain C, Hindmarsh P, Brook C, Hines M (2005) Prenatal hormones and postnatal socialization by parents as determinants of male-typical toy play in girls with congenital adrenal hyperplasia. Child Dev 76:264–278

    PubMed  Google Scholar 

  • Pereira M (1988) Effects of age and sex on intra-group spacing behaviour in juvenile savannah baboons, Papio cynocephalus cynocephalus. Anim Behav 36:184–204

    Google Scholar 

  • Pereira M (1993) Seasonal adjustment of growth rate and adult body weight in ring-tailed lemurs. In: Kappeler P, Ganzhorn J (eds) Lemur social systems and their ecological basis. Plenum Press, New York, pp 205–221

    Google Scholar 

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

    Google Scholar 

  • Pereira M (2002) Agonistic interaction, dominance relation, and ontogenetic trajectories in ringtailed lemurs. In: Pereira M, Fairbanks L (eds) Juvenile primates. University of Chicago Press, Chicago, pp 285–305

    Google Scholar 

  • Phoenix C, Goy R, Gerall A, Young W (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369–382

    PubMed  CAS  Google Scholar 

  • Pomerantz SM, Goy RW, Roy MM (1986) Expression of male-typical behavior in adult female pseudohermaphroditic rhesus: comparisons with normal males and neonatally gonadectomized males and females. Horm Behav 20:483–500

    PubMed  CAS  Google Scholar 

  • Pusey AE (1983) Mother-offspring relationships in chimpanzees after weaning. Anim Behav 31:363–377

    Google Scholar 

  • Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115:203–246

    Google Scholar 

  • Ranson E, Beach FA (1985) Effects of testosterone on ontogeny of urinary behavior in male and female dogs. Horm Behav 19:36–51

    PubMed  CAS  Google Scholar 

  • Robinson JG (1981) Structure in foraging groups of wedge-capped capuchin monkeys Cebus olivaceus. Anim Behav 29:1036–1056

    Google Scholar 

  • Rose LM (1994) Sex differences in diet and foraging behavior in white-faced capuchins (Cebus capucinus). Int J Primatol 15:95–114

    Google Scholar 

  • Rosenblum LA, Paully GS (1984) The effects of varying environmental demands on maternal and infant behavior. Child Dev 55:305–314

    PubMed  CAS  Google Scholar 

  • Rosenblum L, Coplan J, Friedman S, Bassoff T, Gorman J, Andrews M (1994) Adverse early experiences affect noradrenergic and serotonergic functioning in adult primates. Biol Psychiatry 35:221–227

    PubMed  CAS  Google Scholar 

  • Sackett GP (1972) Exploratory behavior of rhesus monkeys as a function of rearing experiences and sex. Dev Psychol 6:260–270

    Google Scholar 

  • Samuels A, Altmann J (1992) Costs of maternal care: infant-carrying in baboons. Behav Ecol 29:391–398

    Google Scholar 

  • Sapolsky RM (1985) Stress-induced suppression of testicular function in the wild baboon: role of glucocorticoids. Endocrinology 116:2273–2278

    PubMed  CAS  Google Scholar 

  • Sapolsky RM (1986) Endocrine and behavioral correlates of drought in wild olive baboons (Papio anubis). Am J Primatol 11:217–227

    CAS  Google Scholar 

  • Sapolsky R (1991) Testicular function, social rank and personality among wild baboons. Psychoneuroendocrinology 16:281–293

    PubMed  CAS  Google Scholar 

  • Sauther M, Cuozzo F (2008) Somatic variation in living, wild ring-tailed lemurs (Lemur catta). Folia Primatol 79:55–78

    PubMed  Google Scholar 

  • Sauther ML, Sussman RW, Gould L (1999) The socioecology of the ringtailed lemur: thirty-five years of research. Evol Anthropol Issues News Rev 8:120–132

    Google Scholar 

  • Sauther ML, Sussman RW, Cuozzo F (2002) Dental and general health in a population of wild ring-tailed lemurs: a life history approach. Am J Phys Anthropol 117:122–132

    PubMed  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  CAS  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 

  • Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 55:597–604

    PubMed  CAS  Google Scholar 

  • Scordato E, Drea C (2007) Scents and sensibility: information content of olfactory signals in the ringtailed lemur, Lemur catta. Anim Behav 73:301–314

    Google Scholar 

  • Seraphin SB, Whitten PL, Reynolds V (2008) The influence of age on fecal steroid hormone levels in male Budongo Forest chimpanzees (Pan troglodytes schweinfurthii). Am J Primatol 70:661–669

    PubMed  CAS  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91:2983–2994

    PubMed  Google Scholar 

  • Silk J (1999) Why are infants so attractive to others? The form and function of infant handling in bonnet macaques. Anim Behav 57:1021–1032

    PubMed  Google Scholar 

  • Smith A, Birnie A, French J (2012) Prenatal steroids affect development and behavior in primates. In: Clancy K, Hinde K, Rutherford J (eds) Building babies: primate development in proximate and ultimate perspective. Springer, New York

    Google Scholar 

  • Stavisky R, Russell E, Stallings J, Smith EO, Worthman C, PL W (1995) Fecal steroid analysis of ovarian cycles in free-ranging baboons. Am J Primatol 36:285–297

    CAS  Google Scholar 

  • Strier KB (2002) Growing up in a patrifocal society: sex differences in the spatial relations of immature muriquis. In: Pereira ME, Fairbanks LA (eds) Juvenile primates. University of Chicago Press, Chicago, pp 138–147

    Google Scholar 

  • Suomi SJ (1987) Genetic and maternal contributions to individual differences in rhesus monkey biobehavioral development. In: Krasnegor N, Blass E, Hofer M, Smotherman W (eds) Perinatal development. Academic, Orlando, pp 397–416

    Google Scholar 

  • Thornton J, Goy RW (1986) Female-typical sexual behavior of rhesus and defeminization by androgens given prenatally. Horm Behav 20:129–147

    PubMed  CAS  Google Scholar 

  • Thornton J, Zehr JL, Loose MD (2009) Effects of prenatal androgens on rhesus monkeys: a model system to explore the organizational hypothesis in primates. Horm Behav 55:633–645

    PubMed  CAS  Google Scholar 

  • Tomaszycki M, Davis J, Gouzoules H, Wallen K (2001) Sex differences in infant rhesus macaque separation-rejection vocalizations and effects of prenatal androgens. Horm Behav 39:267–276

    PubMed  CAS  Google Scholar 

  • van Noordwijk MA, Hemelrijk CK, Herremans L, Sterck EHM (1993) Spatial position and behavioral sex differences in juvenile long-tailed macaques. In: Pereira M, Fairbanks L (eds) Juvenile primates. University of Chicago Press, Chicago, pp 77–85

    Google Scholar 

  • van Schaik CP, Pandit SA, Vogel ER (2004) A model for within-group coalitionary aggression among males. Behav Ecol Sociobiol 57:101–109

    Google Scholar 

  • Wallen K (1996) Nature needs nurture: the interaction of hormonal and social influences on the development of behavioral sex differences in rhesus monkeys. Horm Behav 30:364–378

    PubMed  CAS  Google Scholar 

  • Wallen K (2001) Sex and context: hormones and primate sexual motivation. Horm Behav 40:339–357

    PubMed  CAS  Google Scholar 

  • Wallen K (2005) Hormonal influences on sexually differentiated behavior in nonhuman primates. Front Neuroendocrinol 26:7–26

    PubMed  CAS  Google Scholar 

  • Wallen K, Hassett JM (2009) Sexual differentiation of behaviour in monkeys: role of prenatal hormones. J Neuroendocrinol 21:421–426

    PubMed  CAS  Google Scholar 

  • Wallen K, Bielert C, Slimp J (1977) Foot clasp mounting in the prepubertal rhesus monkey: social and hormonal influences. In: Chevalier-Skolnikoff S, Poirier F (eds) Primate bio-social development. Garland Publishing, New York, pp 439–461

    Google Scholar 

  • Wallen K, Goldfoot DA, Goy R (1981) Peer and maternal influences on the expression of foot-clasp mounting by juvenile male rhesus monkeys. Dev Psychol 14:299–309

    CAS  Google Scholar 

  • Wallen K, Eisler JA, Tannenbaum PL, Nagell K, Mann DR (1991) Antide (Nal-Lys GnRH antagonist) suppression of pituitary-testicular function and sexual behavior in group-living rhesus monkeys. Physiol Behav 50:429–435

    PubMed  CAS  Google Scholar 

  • Whitten PL, Turner TR (2009) Endocrine mechanisms of primate life history trade-offs: growth and reproductive maturation in vervet monkeys. Am J Hum Biol 21:754–761

    PubMed  Google Scholar 

  • Yamamoto ME, Albuquerque FS, Na L, Ferreira ES (2008) Differential infant carrying in captive and wild common marmosets (Callithrix jacchus). Acta Ethologica 11:95–99

    Google Scholar 

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Acknowledgements

I thank the editors, especially Katie Hinde, two anonymous reviewers, and Kristi Lewton for their comments on earlier versions of this chapter. I thank Teague O’Mara for access to his unpublished data. My work on ring-tailed lemurs at Beza Mahafaly Special Reserve was supported by a Leakey Foundation Research Grant and was conducted under Arizona State University IACUC protocol 08-990R. I thank Michelle Sauther and Frank Cuozzo for their logistical help in pursuing that research and the local staff of Beza for seeing me through it.

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Authors and Affiliations

  1. School of Human Evolution and Social Change, Arizona State University, Tempe, AZ, 85287, USA

    Stephanie L. Meredith

  2. Department of Human Evolutionary Biology, Harvard University, Peabody Museum, 11 Divinity Avenue, Cambridge, MA, 02138, USA

    Stephanie L. Meredith

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  1. Stephanie L. Meredith
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Correspondence to Stephanie L. Meredith .

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Editors and Affiliations

  1. , Department of Anthropology, University of Illinois, 109 Davenport Hall, M/C 148, Urbana, 61801, Illinois, USA

    Kathryn B.H. Clancy

  2. , Department of HUman Evolutionary Biology, Harvard University, 11 Divinity Ave, Cambridge, 02138, Massachusetts, USA

    Katie Hinde

  3. , Comparative Primate Biology Laboratory, University of Illinois at Chicago, Chicago, 60612, Illinois, USA

    Julienne N. Rutherford

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Meredith, S.L. (2013). Identifying Proximate and Ultimate Causation in the Development of Primate Sex-Typed Social Behavior. In: Clancy, K., Hinde, K., Rutherford, J. (eds) Building Babies. Developments in Primatology: Progress and Prospects, vol 37. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-4060-4_18

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