Environmental and social influences on neuroendocrine puberty and behavior in macaques and other nonhuman primates

This article is part of a Special Issue "Puberty and Adolescence". Puberty is the developmental period when the hypothalamic-pituitary-gonadal (HPG) axis is activated, following a juvenile quiescent period, and reproductive capacity matures. Although pubertal events occur in a consistent sequence, there is considerable variation between individuals in the onset and timing of pubertal events, with puberty onset occurring earlier in girls than in boys. Evidence in humans demonstrates that social and environmental context influences the timing of puberty onset and may account for some of the observed variation. This review analyzes the nonhuman primate literature, focusing primarily on rhesus macaques (Macaca mulatta), to examine the social and environmental influences on puberty onset, how these factors influence puberty in males and females, and to review the relationship between puberty onset of adult neuroendocrine function and sexual behavior. Social and environmental factors influence the timing of puberty onset and pubertal events in nonhuman primates, as in humans, and the influences of these factors differ for males and females. In nonhuman primates, gonadal hormones are not required for sexual behavior, but modulate the frequency of occurrence of behavior, with social context influencing the relationship between gonadal hormones and sexual behavior. Thus, the onset of sexual behavior is independent of neuroendocrine changes at puberty; however, there are distinct behavioral changes that occur at puberty, which are modulated by social context. Puberty is possibly the developmental period when hormonal modulation of sexual behavior is organized, and thus, when social context interacts with hormonal state to strongly influence the expression of sexual behavior.

[1]  J. Altmann,et al.  Preparation and activation: determinants of age at reproductive maturity in male baboons , 1995, Behavioral Ecology and Sociobiology.

[2]  J M Tanner,et al.  Variations in the Pattern of Pubertal Changes in Boys , 1970, Archives of disease in childhood.

[3]  F. Bercovitch,et al.  Dominance rank, resource availability, and reproductive maturation in female savanna baboons , 1993, Behavioral Ecology and Sociobiology.

[4]  M. Wilson,et al.  Gene-Environment Interactions, Not Neonatal Growth Hormone Deficiency, Time Puberty in Female Rhesus Monkeys1 , 2008, Biology of reproduction.

[5]  A. Dixson,et al.  The Socioendocrinology of Adolescent Development in Male Rhesus Monkeys (Macaca mulatta) , 1997, Hormones and Behavior.

[6]  M. Zencir,et al.  Factors affecting onset of puberty in Denizli province in Turkey. , 2009, The Turkish journal of pediatrics.

[7]  E. Knobil,et al.  The neuroendocrine control of the menstrual cycle. , 1980, Recent progress in hormone research.

[8]  M. Wilson,et al.  Dietary influences on growth and sexual maturation in premenarchial rhesus monkeys , 1988, Hormones and Behavior.

[9]  D. Collins,et al.  Influence of continuous gonadotropin-releasing hormone (GnRH) agonist treatment on luteinizing hormone and testosterone secretion, the response to GnRH, and the testicular response to human chorionic gonadotropin in male rhesus monkeys. , 1984, The Journal of clinical endocrinology and metabolism.

[10]  J. Godfrey,et al.  Social and emotional predictors of the tempo of puberty in female rhesus monkeys , 2013, Psychoneuroendocrinology.

[11]  F. Naftolin,et al.  Age, weight and weight gain in the individual pubertal female rhesus monkey (Macaca mulatta). , 1976, Biology of reproduction.

[12]  J. Flier,et al.  Leptin accelerates the onset of puberty in normal female mice. , 1997, The Journal of clinical investigation.

[13]  F. Bercovitch Dominance rank and reproductive maturation in male rhesus macaques (Macaca mulatta). , 1993, Journal of reproduction and fertility.

[14]  M. Wilson,et al.  Season determines timing of first ovulation in rhesus monkeys (Macaca mulatta) housed outdoors. , 1989, Journal of reproduction and fertility.

[15]  A. Bogaert Age at puberty and father absence in a national probability sample. , 2005, Journal of adolescence.

[16]  K. Bales,et al.  Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia) , 2006, Hormones and Behavior.

[17]  M. Wilson,et al.  Short-day melatonin pattern advances puberty in seasonally breeding rhesus monkeys (Macaca mulatta). , 1989, Journal of reproduction and fertility.

[18]  V. Castracane,et al.  A Longitudinal Study of Leptin During Development in the Male Rhesus Monkey: The Effect of Body Composition and Season on Circulating Leptin Levels1 , 2000, Biology of reproduction.

[19]  E. Knobil On the control of gonadotropin secretion in the rhesus monkey. , 1974, Recent progress in hormone research.

[20]  M. Westerterp-Plantenga,et al.  The relationship between leptin, gonadotropic hormones, and body composition during puberty in a Dutch children cohort. , 2009, European journal of endocrinology.

[21]  D. Hess,et al.  On the sites of the negative and positive feedback actions of estradiol in the control of gonadotropin secretion in the rhesus monkey. , 1978, Endocrinology.

[22]  M. Pelleymounter,et al.  Effects of the obese gene product on body weight regulation in ob/ob mice. , 1995, Science.

[23]  E. Terasawa,et al.  Printed in U.S.A. Copyright © 1999 by The Endocrine Society Effects of Pulsatile Infusion of the GABA A Receptor Blocker Bicuculline on the Onset of Puberty in Female Rhesus Monkeys* , 2022 .

[24]  D. Abbott,et al.  Physical, hormonal and behavioural aspects of sexual development in the marmoset monkey, Callithrix jacchus. , 1978, Journal of reproduction and fertility.

[25]  K. Wallen Desire and ability: Hormones and the regulation of female sexual behavior , 1990, Neuroscience & Biobehavioral Reviews.

[26]  E. Terasawa,et al.  Developmental changes in GnRH release in response to kisspeptin agonist and antagonist in female rhesus monkeys (Macaca mulatta): implication for the mechanism of puberty. , 2012, Endocrinology.

[27]  J. L. Zehr,et al.  Factors Regulating the Timing of Puberty Onset in Female Rhesus Monkeys (Macaca mulatta): Role of Prenatal Androgens, Social Rank, and Adolescent Body Weight1 , 2005, Biology of reproduction.

[28]  C. Snowdon,et al.  The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. , 1987, Biology of reproduction.

[29]  C. Koford Rank of Mothers and Sons in Bands of Rhesus Monkeys , 1963, Science.

[30]  A. Mcneilly,et al.  Inhibition of ovarian function in subordinate female marmoset monkeys (Callithrix jacchus jacchus). , 1981, Journal of Reproduction and Fertility.

[31]  M. Wilson,et al.  Ontogeny of luteinizing hormone secretion and first ovulation in seasonal breeding rhesus monkeys. , 1986, Endocrinology.

[32]  J. Altmann,et al.  Age at maturity in wild baboons: genetic, environmental and demographic influences , 2008, Molecular ecology.

[33]  L. Wildt,et al.  Experimental induction of puberty in the infantile female rhesus monkey. , 1980, Science.

[34]  J. L. Zehr,et al.  Hormones and history: The evolution and development of primate female sexuality , 2004, Journal of sex research.

[35]  A. Mcneilly,et al.  Dynamics of the follicle-stimulating hormone (FSH)-inhibin B feedback loop and its role in regulating spermatogenesis in the adult male rhesus monkey (Macaca mulatta) as revealed by unilateral orchidectomy. , 2000, Endocrinology.

[36]  T. Plant,et al.  Evidence from the rhesus monkey (Macaca mulatta) for the view that negative feedback control of luteinizing hormone secretion by the testis is mediated by a deceleration of hypothalamic gonadotropin-releasing hormone pulse frequency. , 1984, Endocrinology.

[37]  R. Forehand,et al.  Toward a new understanding of early menarche: the role of environmental stress in pubertal timing. , 1993, Adolescence.

[38]  M. E. Yamamoto,et al.  Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups , 2005, American journal of primatology.

[39]  J. Tanner,et al.  Neonatal treatment of male monkeys with a gonadotropin-releasing hormone agonist alters differentiation of central nervous system centers that regulate sexual and skeletal development. , 1993, The Journal of clinical endocrinology and metabolism.

[40]  T. Plant,et al.  Elevating circulating leptin in prepubertal male rhesus monkeys (Macaca mulatta) does not elicit precocious gonadotropin-releasing hormone release, assessed indirectly. , 2002, The Journal of clinical endocrinology and metabolism.

[41]  S. Mccann,et al.  Nitric oxide mediates leptin-induced luteinizing hormone-releasing hormone (LHRH) and LHRH and leptin-induced LH release from the pituitary gland. , 1997, Endocrinology.

[42]  J M Tanner,et al.  Variations in pattern of pubertal changes in girls. , 1969, Archives of disease in childhood.

[43]  R. Frisch,et al.  Menstrual Cycles: Fatness as a Determinant of Minimum Weight for Height Necessary for Their Maintenance or Onset , 1974, Science.

[44]  H. McClure,et al.  Neonatal treatment with luteinizing hormone-releasing hormone analogs alters peripheral lymphocyte subsets and cellular and humorally mediated immune responses in juvenile and adult male monkeys. , 1994, The Journal of clinical endocrinology and metabolism.

[45]  K. Wallen,et al.  Sexual maturation in male rhesus monkeys: importance of neonatal testosterone exposure and social rank. , 1998, The Journal of endocrinology.

[46]  Jean M. Severin,et al.  Escape from Social Suppression of Sexual Behavior and of Ovulation in Female Common Marmosets a , 1997, Annals of the New York Academy of Sciences.

[47]  D. Dierschke,et al.  Positive feedback effect of progesterone on luteinizing hormone (LH) release in cyclic female rhesus monkeys: LH response occurs in two phases. , 1980, The Journal of clinical endocrinology and metabolism.

[48]  J. V. Hooff,et al.  Behavioral aspects of puberty in group-living stumptail monkeys (Macaca arctoides) , 1988, Physiology & Behavior.

[49]  J. Bourguignon,et al.  In VitroStimulation of the Prepubertal Rat Gonadotropin-Releasing Hormone Pulse Generator by Leptin and Neuropeptide Y through Distinct Mechanisms. , 2000, Endocrinology.

[50]  K. Wallen,et al.  Blockade of neonatal activation of the pituitary-testicular axis with continuous administration of a gonadotropin-releasing hormone agonist in male rhesus monkeys. , 1984, The Journal of clinical endocrinology and metabolism.

[51]  C. Sisk,et al.  Back to the future: The organizational–activational hypothesis adapted to puberty and adolescence , 2009, Hormones and Behavior.

[52]  T. Plant,et al.  N-methyl-D,L-aspartate elicits hypothalamic gonadotropin-releasing hormone release in prepubertal male rhesus monkeys (Macaca mulatta). , 1987, Endocrinology.

[53]  K. Nagell,et al.  Antide (NAL-LYS GnRH antagonist) suppression of pituitary-testicular function and sexual behavior in group-living rhesus monkeys , 1991, Physiology & Behavior.

[54]  K. Suter,et al.  The pattern and tempo of the pubertal reaugmentation of open-loop pulsatile gonadotropin-releasing hormone release assessed indirectly in the male rhesus monkey (Macaca mulatta). , 1998, Endocrinology.

[55]  D. Abbott,et al.  Extension of reproductive suppression by pheromonal cues in subordinate female marmoset monkeys, Callithrix jacchus. , 1990, Journal of reproduction and fertility.

[56]  H. Fraser,et al.  Effect of Neonatal Treatment with a GnRH Antagonist on Development of the Cell‐Mediated Immune Response in Marmosets , 1999, American journal of reproductive immunology.

[57]  B. Ellis,et al.  Impact of fathers on daughters' age at menarche: a genetically and environmentally controlled sibling study. , 2008, Developmental psychology.

[58]  J. Hodges,et al.  Social status controls LH secretion and ovulation in female marmoset monkeys (Callithrix jacchus). , 1988, The Journal of endocrinology.

[59]  R. Colman,et al.  Body weight impact on puberty: effects of high-calorie diet on puberty onset in female rhesus monkeys. , 2012, Endocrinology.

[60]  D. Heber,et al.  The stimulatory and down-regulatory effects of a gonadotropin-releasing hormone agonist in man. , 1984, The Journal of clinical endocrinology and metabolism.

[61]  D. Abbott,et al.  Specific Neuroendocrine Mechanisms Not Involving Generalized Stress Mediate Social Regulation of Female Reproduction in Cooperatively Breeding Marmoset Monkeys a , 1997, Annals of the New York Academy of Sciences.

[62]  M. Wilson,et al.  Effects of a natural versus artificial environment on the tempo of maturation in female rhesus monkeys. , 1988, Endocrinology.

[63]  R. Frisch,et al.  Weight at menarche: similarity for well-nourished and undernourished girls at differing ages, and evidence for historical constancy. , 1972, Pediatrics.

[64]  J. Moossy,et al.  The arcuate nucleus and the control of gonadotropin and prolactin secretion in the female rhesus monkey (Macaca mulatta). , 1978, Endocrinology.

[65]  M. Ferin,et al.  A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. , 1992, Endocrinology.

[66]  C. Snowdon,et al.  Reproductive biology of captive male cottontop tamarin monkeys as a function of social environment , 2001, Animal Behaviour.

[67]  Jay Belsky,et al.  Family rearing antecedents of pubertal timing. , 2007, Child development.

[68]  F. Bercovitch,et al.  Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques , 1988, Hormones and Behavior.

[69]  T. P. Gordon,et al.  Age differences in copulatory behavior and serum 17β-estradiol in female rhesus monkeys , 1982, Physiology & Behavior.

[70]  T. Plant,et al.  Operation of the follicle-stimulating hormone (FSH)–inhibin B feedback loop in the control of primate spermatogenesis , 2001, Molecular and Cellular Endocrinology.

[71]  K. Wallen,et al.  Timing of Prenatal Androgen Exposure: Anatomical and Endocrine Effects on Juvenile Male and Female Rhesus Monkeys , 2000, Hormones and Behavior.

[72]  J. French,et al.  Social and Developmental Influences on Reproductive Function in Female Wied's Black Tufted-Ear Marmosets (Callithrix kuhli) , 1997, Hormones and Behavior.

[73]  S. Yen,et al.  Hormonal dynamics at midcycle: a reevaluation. , 1983, The Journal of clinical endocrinology and metabolism.

[74]  E. J. Wickings,et al.  Life history in male mandrills (Mandrillus sphinx): physical development, dominance rank, and group association. , 2006, American journal of physical anthropology.

[75]  Tony M. Plant,et al.  Neurobiological Bases Underlying the Control of the Onset of Puberty in the Rhesus Monkey: A Representative Higher Primate , 2001, Frontiers in Neuroendocrinology.

[76]  K. Wallen Sex and Context: Hormones and Primate Sexual Motivation , 2001, Hormones and Behavior.

[77]  J. Brooks-Gunn,et al.  The antecedents of menarcheal age: heredity, family environment, and stressful life events. , 1995, Child development.

[78]  E. Terasawa,et al.  gamma-Aminobutyric acid is an inhibitory neurotransmitter restricting the release of luteinizing hormone-releasing hormone before the onset of puberty. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[79]  D. Hess,et al.  On the sites of the negative and positive feedback actions of estradiol in the control of gonadotropin secretion in the rhesus monkey. 1978. , 2005, American journal of obstetrics and gynecology.

[80]  K. Wallen,et al.  Blockade of neonatal activation of the pituitary-testicular axis: effect on peripubertal luteinizing hormone and testosterone secretion and on testicular development in male monkeys. , 1989, The Journal of clinical endocrinology and metabolism.

[81]  J. E. Schneider,et al.  Sense and Nonsense in Metabolic Control of Reproduction , 2012, Front. Endocrin..

[82]  C. Snowdon,et al.  Neonatal and Pubertal Development in Males of a Cooperatively Breeding Primate, the Cotton-Top Tamarin (Saguinus oedipus oedipus)1 , 2002, Biology of reproduction.

[83]  M. Wilson,et al.  Timing of sexual maturity in female rhesus monkeys (Macaca mulatta) housed outdoors. , 1984, Journal of reproduction and fertility.

[84]  R. Leibel,et al.  Effect of puberty on the relationship between circulating leptin and body composition. , 2000, The Journal of clinical endocrinology and metabolism.

[85]  T. Plant,et al.  Puberty in monkeys is triggered by chemical stimulation of the hypothalamus. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[86]  E. Nieschlag,et al.  Reversible induction of azoospermia in rhesus monkeys by constant infusion of a gonadotropin-releasing hormone agonist using osmotic minipumps. , 1983, The Journal of clinical endocrinology and metabolism.

[87]  S. Ojeda,et al.  Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[88]  S. Sholl,et al.  Pulsatile luteinizing hormone (LH) release during the progesterone-induced LH surge in the female rhesus monkey. , 1987, Endocrinology.

[89]  Kim Wallen,et al.  Nature Needs Nurture: The Interaction of Hormonal and Social Influences on the Development of Behavioral Sex Differences in Rhesus Monkeys , 1996, Hormones and Behavior.

[90]  F. Chehab,et al.  Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin , 1996, Nature Genetics.

[91]  R. Goy,et al.  Effects of castration and replacement therapy on sexual behavior of adult male rhesuses. , 1973, Journal of comparative and physiological psychology.

[92]  E. Terasawa,et al.  Effects of pulsatile infusion of the GABA(A) receptor blocker bicuculline on the onset of puberty in female rhesus monkeys. , 1999, Endocrinology.

[93]  A. Caspi,et al.  Childhood experience and the onset of menarche: a test of a sociobiological model. , 1992, Child development.

[94]  J. French,et al.  Social and developmental influences on urinary androgen levels in young male white‐faced marmosets (Callithrix geoffroyi) , 2011, American journal of primatology.

[95]  K. Chambers,et al.  Sexual behavior in response to testosterone in old long-term-castrated rhesus males , 1983, Neurobiology of Aging.

[96]  Rebecca R. Pick,et al.  Onset of plural cooperative breeding in common marmoset families following replacement of the breeding male , 2004, Animal Behaviour.

[97]  J. Bourguignon,et al.  In vitro stimulation of the prepubertal rat gonadotropin-releasing hormone pulse generator by leptin and neuropeptide Y through distinct mechanisms. , 2000, Endocrinology.

[98]  M. Grumbach,et al.  N-methyl-D-aspartate (NMDA) receptors mediate the release of gonadotropin-releasing hormone (GnRH) by NMDA in a hypothalamic GnRH neuronal cell line (GT1-1). , 1994, Endocrinology.

[99]  T. Plant,et al.  Sustained intermittent release of gonadotropin-releasing hormone in the prepubertal male rhesus monkey induced by N-methyl-DL-aspartic acid. , 1988, Neuroendocrinology.

[100]  M. Wilson,et al.  Leptin administration increases nocturnal concentrations of luteinizing hormone and growth hormone in juvenile female rhesus monkeys. , 2003, The Journal of clinical endocrinology and metabolism.

[101]  G. Merriam,et al.  Photoperiod-driven changes in reproductive function in male rhesus monkeys. , 1992, The Journal of clinical endocrinology and metabolism.

[102]  D. Rowe,et al.  Environmental and Genetic Influences on Pubertal Development: Evolutionary Life History Traits? , 2000 .

[103]  S. Bloom,et al.  An increase in kisspeptin-54 release occurs with the pubertal increase in luteinizing hormone-releasing hormone-1 release in the stalk-median eminence of female rhesus monkeys in vivo. , 2008, Endocrinology.

[104]  E. Terasawa,et al.  In vivo release of luteinizing hormone releasing hormone increases with puberty in the female rhesus monkey. , 1989, Endocrinology.

[105]  J. L. Zehr,et al.  Prenatal androgen blockade accelerates pubertal development in male rhesus monkeys , 2006, Psychoneuroendocrinology.

[106]  D. Styne,et al.  Puberty : ontogeny, neuroendocrinology, physiology, and disorders , 1998 .

[107]  E. Terasawa,et al.  Negative feedback effects of estrogen on luteinizing hormone-releasing hormone release occur in pubertal, but not prepubertal, ovariectomized female rhesus monkeys. , 1993, Endocrinology.

[108]  K. Wallen Hormonal influences on sexually differentiated behavior in nonhuman primates , 2005, Frontiers in Neuroendocrinology.

[109]  V. Castracane,et al.  Leptin and thyroxine during sexual development in male monkeys: effect of neonatal gonadotropin-releasing hormone antagonist treatment and delayed puberty on the developmental pattern of leptin and thyroxine secretion. , 2002, European journal of endocrinology.