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The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses

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Abstract

Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high-ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10-month period in relation to rank, age, natal status, and group tenure length, including during a socially unstable period in which coalitions of lower ranked males attacked higher ranked males. Androgen, but not GC, levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High-ranking male targets had the highest GC levels of all males when targeted and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.

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References

  • Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Medoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82

    Article  PubMed  CAS  Google Scholar 

  • Aujard F, Perret M (1998) Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiol Behav 64:513–519

    Article  PubMed  CAS  Google Scholar 

  • Bales KL, French JA, McWilliams J, Lake RA, Dietz JM (2006) Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia). Horm Behav 49:88–95

    Article  PubMed  CAS  Google Scholar 

  • Barrett GM, Shimizu K, Bardi M, Asaba S, Mori A (2002) Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm Behav 42:85–96

    Article  PubMed  CAS  Google Scholar 

  • Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2005) Effects of male social instability of female glucocorticoid levels in chacma baboons. Anim Behav 69:1211–1221

    Article  Google Scholar 

  • Beehner JC, Bergman TJ, Cheney DL, Seyfarth RM, Whitten PL (2006) Testosterone predicts future dominance rank and mating activity among male chacma baboons. Behav Ecol Sociobiol 59:469–479

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Berard JD, Nürnberg P, Epplen JT, Schmidtke J (1994) Alternative reproductive tactics and reproductive success in male rhesus macaques. Behaviour 129:177–201

    Article  Google Scholar 

  • Bercovitch FB, Clarke AS (1995) Dominance rank, cortisol concentrations, and reproductive maturation in male rhesus macaques. Physiol Behav 58:215–221

    Article  PubMed  CAS  Google Scholar 

  • Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL (2005) Correlates of stress in free-ranging male chacma baboons. Anim Behav 70:703–713

    Article  Google Scholar 

  • Bernstein IS, Ruehlmann TE, Judge PG, Lindquist T, Weed JL (1991) Testosterone changes during the period of adolescence in male rhesus monkeys (Macaca mulatta). Am J Primatol 24:29–38

    Article  CAS  Google Scholar 

  • Bribiescas RG (2006) On the evolution, life history, and proximate mechanisms of human male reproductive senescence. Evol Anthropol 15:132–141

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Chambers KC, Hess DL, Phoenix CH (1981) Relationship of free and bound testosterone to sexual behavior in old rhesus males. Physiol Behav 27:615–620

    Article  PubMed  CAS  Google Scholar 

  • Chambers KC, Resko JA, Phoenix CH (1982) Correlation of diurnal changes in hormones with sexual behavior and age in male rhesus macaques. Neurobiol Aging 3:37–42

    Article  PubMed  CAS  Google Scholar 

  • Charpentier M, Peignot P, Hossaert-McKey M, Gimenez O, Setchell JM, Wickings EJ (2005) Constraints on control: factors influencing reproductive success in male mandrills. Behav Ecol 16:614–623

    Article  Google Scholar 

  • Cheney DL, Seyfarth RM, Fischer J, Beehner JC, Bergman TJ, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2004) Factors affecting reproduction and mortality among baboons in the Okavango Delta, Botswana. Int J Primatol 25:401–428

    Article  Google Scholar 

  • Darwin C (1871) The descent of man and selection in relation to sex. J Murray, London

    Book  Google Scholar 

  • de Ruiter JR, Van Hooff JARAM, Scheffrahn W (1994) Social and genetic aspects of paternity in wild long-tailed macaques (Macaca fascicularis). Behaviour 129:203–224

    Article  Google Scholar 

  • Dubuc C, Muniz L, Heistermann M, Engelhardt A, Widdig A (2011) Testing the priority-of-access model in a seasonally breeding primate species (Macaca mulatta). Behav Ecol Sociobiol 65:1615–1627

    Article  PubMed  Google Scholar 

  • Eaton GG, Resko JA (1974) Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males. Horm Behav 5:251–259

    Article  PubMed  CAS  Google Scholar 

  • Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333

    Article  Google Scholar 

  • Ellison PT, Bribiescas RG, Bentley GR, Campbell BC, Lipson SF, Panter-Brick C, Hill K (2002) Population variation in age-related decline in male salivary testosterone. Hum Reprod 17:3251–3253

    Article  PubMed  CAS  Google Scholar 

  • Engelhardt A, Heistermann M, Hodges JK, Nürnberg P, Niemitz C (2006) Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)—male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol 59:740–52

    Article  Google Scholar 

  • Fichtel C, Kraus C, Ganswindt A, Heistermann M (2007) Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Horm Behav 51:640–648

    Article  PubMed  CAS  Google Scholar 

  • Ganswindt A, Palme R, Heistermann M, Borragan S, Hodges JK (2003) Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol 134:156–166

    Article  PubMed  CAS  Google Scholar 

  • Gesquiere LR, Wango EO, Alberts SC, Altmann J (2007) Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons. Horm Behav 51:114–125

    Article  PubMed  CAS  Google Scholar 

  • Girard-Buttoz C, Heistermann M, Krummel S, Engelhardt A (2009) Seasonal and social influences on fecal androgen and glucocorticoid excretion in wild male long-tailed macaques (Macaca fascicularis). Physiol Behav 98:168–175

    Article  PubMed  CAS  Google Scholar 

  • Gordon TP, Rose RM, Bernstein IS (1976) Seasonal rhythm in plasma testosterone levels in the rhesus monkey (Macaca mulatta): a three-year study. Horm Behav 7:229–243

    Article  PubMed  CAS  Google Scholar 

  • Gordon TP, Bernstein IS, Rose RM (1978) Social and seasonal influences on testosterone secretion in the male rhesus monkey. Physiol Behav 21:623–627

    Article  PubMed  CAS  Google Scholar 

  • Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602

    Article  Google Scholar 

  • Guibert F, Richard-Yris M-A, Lumineau S, Kotrschal K, Guémené D, Bertin A, Möstl E, Houdelier C (2010) Social instability in laying quail: consequences on yolk steroids and offspring's phenotype. PLoS ONE 5:e14069

    Article  PubMed  Google Scholar 

  • Hamlin HJ, Lowers RH, Guillette LJ (2011) Seasonal androgen cycles in adult male American alligators (Alligator mississippiensis) from a barrier island population. Biol Reprod 85:1108–1113

    Article  PubMed  CAS  Google Scholar 

  • Heistermann M, Finke M, Hodges JK (1995) Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am J Primatol 37:275–284

    Article  CAS  Google Scholar 

  • Heistermann M, Ademmer C, Kaumanns W (2004) Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus. Int J Primatol 25:689–708

    Article  Google Scholar 

  • Heistermann M, Palme R, Ganswindt A (2006) Comparison of different enzyme immunoassays for assessment of adrenocortical activity in primates based on fecal analysis. Am J Primatol 68:257–273

    Article  PubMed  CAS  Google Scholar 

  • Herndon JG, Bein ML, Nordmeyer DL, Turner JJ (1996) Seasonal testicular function in male rhesus monkeys. Horm Behav 30:266–271

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Higham JP, MacLarnon AM, Heistermann M, Ross C, Semple S (2009) Self-directed behaviours and faecal glucocorticoid levels are not correlated in female wild olive baboons. Stress 12:526–532

    Google Scholar 

  • Higham JP, Heistermann M, Maestripieri D (2011) The energetics of male-male endurance rivalry in rhesus macaques. Anim Behav 81:1001–1007

    Google Scholar 

  • Hirschenhauser K, Oliveira RF (2006) Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis. Anim Behav 71:265–277

    Article  Google Scholar 

  • Hirschenhauser K, Winkler H, Oliveira RF (2003) Comparative analyses of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation. Horm Behav 43:508–519

    Article  PubMed  CAS  Google Scholar 

  • Hodges JK, Heistermann M (2011) Field Endocrinology: monitoring hormonal changes in free-ranging primates. In: Setchell J, Curtis D (eds) Field and laboratory methods in primatology, 2nd edn. Cambridge University Press, Cambridge, pp 282–294

    Google Scholar 

  • Hoffman CL, Ruiz-Lambides AV, Davila E, Maldonado E, Gerald MS, Maestripieri D (2008) Sex differences in survival costs of reproduction in a promiscuous primate. Behav Ecol Sociobiol 62:1711–1718

    Article  Google Scholar 

  • Hoffman CL, Higham JP, Heistermann M, Prendergast B, Coe C, Maestripieri D (2011) Immune function and HPA axis activity in free-ranging rhesus macaques. Physiol Behav 104:507–514

    Article  PubMed  CAS  Google Scholar 

  • Kraus C, Heistermann M, Kappeler PM (1999) Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxii)? Physiol Behav 66:855–861

    Article  PubMed  CAS  Google Scholar 

  • Kuemmerli R, Martin RD (2005) Male and female reproductive success in Barbary macaques (Macaca sylvanus) in Gibraltar: no evidence for rank dependence. Int J Primatol 26:1229–1249

    Article  Google Scholar 

  • Landys MM, Goymann W, Scwabl I, Trapschuh M, Slagsvold T (2010) Impact of seasonal and social challenge on testosterone and corticosterone levels in a year-round territorial bird. Horm Behav 58:317–325

    Article  PubMed  CAS  Google Scholar 

  • Lynch JW, Ziegler TE, Strier KB (2002) Individual and seasonal variation in fecal testosterone and cortisol levels of wild male tufted capuchin monkeys, Cebus apella nigritus. Horm Behav 41:275–287

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Mann DR, Akinbami MA, Gould KG, Wallen K (1998) Sexual maturation in male rhesus monkeys: importance of neonatal testosterone exposure and social rank. J Endocrinol 156:493–501

    Article  PubMed  CAS  Google Scholar 

  • Manson JH (1995) Do female rhesus macaques choose novel males? Am J Primatol 37:285–296

    Article  Google Scholar 

  • Mehlman PT, Higley JD, Fernald BJ, Sallee FR, Suomi SJ, Linnoila M (1997) CSF 5-HIAA, testosterone, and sociosexual behaviors in free-ranging male rhesus macaques in the mating season. Psychiat Res 72:89–102

    Article  CAS  Google Scholar 

  • Möhle U, Heistermann M, Palme R, Hodges JK (2002) Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen Comp Endocrinol 129:135–145

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Ostner J, Heistermann M, Schülke O (2011) Male competition and its hormonal correlates in wild Assamese macaques (Macaca assamensis). Horm Behav 59:105–113

    Article  PubMed  CAS  Google Scholar 

  • Palme R, Möstl E (1994) Biotin-straptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In: Görög S (ed) Advances in steroid analysis. Akadémiai Kiadó, Budapest, pp 11–117

    Google Scholar 

  • Paul A, Kuester J, Timme A, Arnemann J (1993) The association between rank, mating effort, and reproductive success in male Barbary macaques (Macaca sylvanus). Primates 34:491–502

    Article  Google Scholar 

  • Plant TM, Zumpe D, Sauls M, Michael RP (1974) An annual rhythm in the plasma testosterone of adult male rhesus monkeys maintained in the laboratory. J Endocrinol 62:403–404

    Article  PubMed  CAS  Google Scholar 

  • Plavcan JM (2001) Sexual dimorphism in primate evolution. Am J Phys Anthropol 116:25–53

    Article  Google Scholar 

  • Rawlins RG, Kessler MJ (eds) (1986) The Cayo Santiago Macaques: history, behavior & biology. SUNY Press, Albany, New York

  • Robinson JA, Scheffler G, Eisele SG, Goy RW (1975) Effects of age and season on sexual behavior and plasma testosterone and dihdrotestosterone concentrations of laboratory-housed male rhesus monkeys (Macaca mulatta). Biol Reprod 13:203–210

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Rose RM, Holaday JW, Bernstein IS (1971) Plasma testosterone, dominance rank and aggressive behaviour in male rhesus monkeys. Nature 231:366–368

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM (1983) Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 5:365–379

    Article  CAS  Google Scholar 

  • Sapolsky RM (1992) Cortisol concentrations and the social significance of rank instability among wild baboons. Psychoneuroendocrinology 17:701–709

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652

    Article  PubMed  CAS  Google Scholar 

  • Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticosteroids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55–89

    Article  PubMed  CAS  Google Scholar 

  • Schradin C (2008) Seasonal changes in testosterone and corticosterone levels in four social categories of a desert dwelling sociable rodent. Horm Behav 53:573–579

    Article  PubMed  CAS  Google Scholar 

  • Schülke O, Ostner J (2008) Male reproductive skew, paternal relatedness and female social relationships. Am J Primatol 70:1–4

    Article  Google Scholar 

  • Schülke O, Ostner J (2012) Ecological and social influences on sociality. In: Mitani J, Call J, Kappeler P, Palombit R, Silk J (eds) The evolution of primate societies. In press

  • Setchell JM, Charpentier M, Wickings EJ (2005) Mate-guarding and paternity in mandrills (Mandrillus sphinx): factors influencing monopolisation of females by the alpha male. Anim Behav 70:1105–1120

    Article  Google Scholar 

  • Setchell JM, Smith T, Wickings EJ, Knapp LA (2010) Stress, social behaviour and secondary sexual traits in a male primate. Horm Behav 58:720–728

    Article  PubMed  CAS  Google Scholar 

  • Shutt K, MacLarnon A, Heistermann M, Semple S (2007) Grooming in Barbary macaques: better to give than receive? Biol Lett 3:231–233

    Article  PubMed  Google Scholar 

  • Thierry B, Iwaniuk AN, Pellis SM (2000) The influence of phylogeny on the social behaviour of macaques (Primates: Cercopithecidae, genus Macaca). Ethology 106:713–728

    Article  Google Scholar 

  • van Meter PE, French JA, Dloniak SM, Watts HE, Kolowski JM, Holekamp KE (2009) Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm Behav 55:329–337

    Article  PubMed  Google Scholar 

  • van Noordwijk MA, van Schaik CP (2004) Sexual selection and the careers of primate males: paternity concentration, dominance-acquisition tactics and transfer decisions. In: Kappeler P, van Schaik CP (eds) Sexual selection in primates. Cambridge University Press, Cambridge, pp 208–229

    Chapter  Google Scholar 

  • Weingrill T, Willems EP, Zimmermann N, Steinmetz H, Heistermann M (2011) Species-specific patterns in fecal glucocorticoid and androgen levels in zoo-living orangutans (Pongo spp.). Gen Comp Endocrinol 172:446–457

    Article  PubMed  CAS  Google Scholar 

  • Widdig A, Bercovitch FB, Streich WJ, Nürnberg P, Krawczak M (2004) A longitudinal analysis of reproductive skew in male rhesus macaques. Proc R Soc Lond B 271:819–826

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wynne-Edwards KE (2001) Hormonal changes in mammalian fathers. Horm Behav 40:139–145

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Doreen Hess, Jenna Goldfein, Maria Rakhovskaya, and the staff of the CPRC for logistical support in the field and assistance with animal capturing and handling. We are extremely grateful to Andrea Heistermann and Petra Kiesel for analyzing the fecal samples and to Tara Mandalaywala and the CPRC for assisting with their transportation to Germany. We are deeply indebted to John Addicott for helping us to set up our Access database. JH also thanks Antje Engelhardt and Constance Dubuc for general discussion on macaque social styles and competitive regimes. We would also like to thank Thore Bergman for providing raw data from his 2005 animal behavior study. Finally, the MS was improved by comments from Joan Silk and two anonymous reviewers. This research was supported by NIH grant R21-AG029862 to D.M. This publication was made possible by grant number CM-5-P40RR003640 from the NIH National Center for Research Resources (NCRR) to the CPRC of the University of Puerto Rico. Its contents are solely the responsibility of the authors and do not necessarily represent the official views of NCRR or NIH.

Ethical standards

This study was conducted in accordance with the NIH Guide for the Care and Use of Laboratory Animals and conformed to all laws of Puerto Rico, the United States, and Germany. The protocol for this study was approved by the Institutional Animal Care and Use Committee, Medical Sciences Department, University of Puerto Rico.

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Authors and Affiliations

  1. Institute for Mind and Biology, University of Chicago, 940 East 57th Street, Chicago, IL, 60637, USA

    James P. Higham & Dario Maestripieri

  2. Department of Anthropology, New York University, 25 Waverly Place, New York, NY, 10003, USA

    James P. Higham

  3. Reproductive Biology Unit, German Primate Centre, Kellnerweg 4, 37077, Göttingen, Germany

    Michael Heistermann

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  1. James P. Higham
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Correspondence to James P. Higham.

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Communicated by J. B. Silk

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Higham, J.P., Heistermann, M. & Maestripieri, D. The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67, 19–30 (2013). https://doi.org/10.1007/s00265-012-1420-6

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