The Influence of Social Environment on Morbidity, Mortality, and Reproductive Success in Free-Ranging Cercopithecine Primates

  • Marnie G. Silverstein-MetzlerEmail author
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)


An understanding of the consequences of the socioeconomic gradient is paramount to addressing public health concerns. It has been well documented in Westernized societies that there is an association between low socioeconomic status (SES) and increased risk of adverse health outcomes; however, it is unknown whether the predominant cause of the health gradient is differences in lifestyle risk factors or psychophysiological responses to one’s social environment or both. Studying free-ranging cercopithecine primates provides a unique opportunity to study the effects of social environment on health. This review details effects of SES and other attributes of social environment on morbidity, mortality, and reproductive success in several of the best-studied free-ranging cercopithecine primate species—including olive baboons (Papio anubis), yellow baboons (Papio cynocephalus), chacma baboons (Papio ursinus), cynomolgus macaques (Macaca fascicularis), and rhesus macaques (Macaca mulatta). In these species, animals that occupy a low social status tend to be hypercortisolemic, slower to recover from injury and illness, experience increased mortality rates, and have decreased reproductive success. Rank effects seem to be most pronounced during times when allocation of resources—including food, water, and spacial positioning—became priorities such as for reproducing or surviving environmental threats. The development of strong and consistent social bonds may partially offset adverse health outcomes associated with low dominance rank and was found to independently predict survivorship. Overall, studies in free-ranging cercopithecine primates suggest that social environment, including psychophysiological stressors, influence the social inequalities observed in human health.


Reproductive Success Dominance Rank Social Connectedness Dominant Female Rank Effect 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


  1. 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(1):67–82PubMedCrossRefGoogle Scholar
  2. Adler NE, Epel ES, Castellazzo G, Ickovics JR (2000) Relationship of subjective and objective social status with psychological and physiological functioning: preliminary data in healthy white women. Health Psychol 19(6):586–592PubMedCrossRefGoogle Scholar
  3. Allen J, Balfour R, Bell R, Marmot M (2014) Social determinants of mental health. Int Rev Psychiatry 26(4):392–407. doi: 10.3109/09540261.2014.928270 PubMedCrossRefGoogle Scholar
  4. Altmann SA (1962) A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Ann N Y Acad Sci 102:338–345PubMedCrossRefGoogle Scholar
  5. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49(3/4):227–267. doi: 10.2307/4533591 PubMedCrossRefGoogle Scholar
  6. Altmann J (1980) Baboon mothers and infants. Harvard University Press, CambridgeGoogle Scholar
  7. Altmann J, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons. Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 405–418Google Scholar
  8. Altmann J, Alberts SC, Haines SA, Dubach J, Muruthi P, Coote T, Geffen E, Cheesman DJ, Mututua RS, Saiyalele SN, Wayne RK, Lacey RC, Bruford MW (1996) Behavior predicts genetic structure in a wild primate group. Proc Natl Acad Sci USA 93:5797–5801PubMedPubMedCentralCrossRefGoogle Scholar
  9. Archie EA, Altmann J, Alberts SC (2012) Social status predicts wound healing in wild baboons. Proc Natl Acad Sci USA 109(23):9017–9022. doi: 10.1073/pnas.1206391109 PubMedPubMedCentralCrossRefGoogle Scholar
  10. 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 Biol Sci 281(1793):20141261. doi: 10.1098/rspb.2014.1261 PubMedPubMedCentralCrossRefGoogle Scholar
  11. Avitsur R, Padgett DA, Sheridan JF (2006) Social interactions, stress, and immunity. Neurol Clin 24(3):483–491. doi: 10.1016/j.ncl.2006.03.005 PubMedCrossRefGoogle Scholar
  12. Bartz JA, Hollander E (2006) The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior. Horm Behav 50(4):518–528. doi: 10.1016/j.yhbeh.2006.06.018 Google Scholar
  13. Beehner JC, Onderdonk DA, Alberts SC, Altmann J (2006) The ecology of conception and pregnancy failure in wild baboons. Behav Ecol 17(5):741–750. doi: 10.1093/beheco/arl006 CrossRefGoogle Scholar
  14. Belzung C, Anderson JR (1986) Social rank and responses to feeding competition in Rhesus-monkeys. Behav Processes 12(4):307–316PubMedCrossRefGoogle Scholar
  15. Bensyl DM, Iuliano DA, Carter M, Santelli J, Gilbert BC (2005) Contraceptive use–United States and territories, behavioral risk factor surveillance system, 2002. MMWR Surveill Summ 54(6):1–72PubMedGoogle Scholar
  16. Berga SL (2011) Disorders of gonadotropin secretion. In: Wass JAH, Stewart PM, Amiel SA, Davies MC (eds) Oxford textbook of endocrinology and diabetes, 2nd edn. Oxford University Press, Oxford, pp 1212–1223Google Scholar
  17. Berga SL, Yen SSC (2004) Reproductive failure due to central nervous system-hypothalamic-pituitary dysfunction. In: Reproductive endocrinology. Physiology, pathophysiology, and clinical management, 5th edn. Elsevier Saunders, PhiladelphiaGoogle Scholar
  18. Berglund A, Widemo MS, Rosenqvist G (2005) Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish. Behav Ecol 16(3):649–655. doi: 10.1093/beheco/ari038 CrossRefGoogle Scholar
  19. Bernstein IS (1976) Dominance, aggression and reproduction in primate societies. J Theor Biol 60(2):459–472PubMedCrossRefGoogle Scholar
  20. Bjorntorp P, Holm G, Rosmond R (1999) Hypothalamic arousal, insulin resistance and type 2 diabetes mellitus. Diabet Med 16(5):373–383PubMedCrossRefGoogle Scholar
  21. Blomquist GE, Sade DS, Berard JD (2011) Rank-related fitness differences and their demographic pathways in semi-free-ranging Rhesus Macaques (Macaca mulatta). Int J Primatol 32(1):193–208CrossRefGoogle Scholar
  22. Brandtstadter J, Baltes-Gotz B, Kirschbaum C, Hellhammer D (1991) Developmental and personality correlates of adrenocortical activity as indexed by salivary cortisol: observations in the age range of 35 to 65 years. J Psychosom Res 35(2–3):173–185Google Scholar
  23. Buchan JC, Alberts SC, Silk JB, Altmann J (2003) True paternal care in a multi-male primate society. Nature 425(6954):179–181PubMedCrossRefGoogle Scholar
  24. Chapman C, Rothman J (2009) Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints. Primates 50(1):12–22. doi: 10.1007/s10329-008-0123-0 PubMedCrossRefGoogle Scholar
  25. Charpentier MJ, Tung J, Altmann J, Alberts SC (2008a) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17(8):2026–2040. doi: 10.1111/j.1365-294X.2008.03724.x PubMedCrossRefGoogle Scholar
  26. Charpentier MJ, Van Horn RC, Altmann J, Alberts SC (2008b) Paternal effects on offspring fitness in a multimale primate society. Proc Natl Acad Sci USA 105(6):1988–1992. doi: 10.1073/pnas.0711219105 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Cheney DL, Seyfarth RM (1997) Reconciliatory grunts by dominant female baboons influence victims’ behavior. Anim Behav 54:409–418PubMedCrossRefGoogle Scholar
  28. Cheney DL, Seyfarth RM, Andelman SJ, Lee PC (1988) Reproductive success in vervet monkeys. In: Clutton-Brock TH (ed) Reproductive success. University of Chicago Press, Chicago, pp 384–402Google Scholar
  29. Cheney DL, Seyfarth RM, Silk JB (1995) The role of grunts in reconciling opponents and facilitating interactions among adult female baboons. Anim Behav 50:249–257CrossRefGoogle Scholar
  30. Cheney DL, Seyfarth RM, Fischer J, Beehner J, Bergman T, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2004) Factors affecting reproduction and mortality among baboons in the Okavango delta, Botswanna. Int J Primatol 25(2):401–428CrossRefGoogle Scholar
  31. Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298(14):1685–1687. doi: 10.1001/jama.298.14.1685 PubMedCrossRefGoogle Scholar
  32. Cole SW, Mendoza SP, Capitanio JP (2009) Social stress desensitizes lymphocytes to regulation by endogenous glucocorticoids: insights from in vivo cell trafficking dynamics in rhesus macaques. Psychosom Med 71(6):591–597. doi: 10.1097/PSY.0b013e3181aa95a9 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Crockford C, Wittig RM, Whitten PL, Seyfarth RM, Cheney DL (2008) Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm Behav 53(1):254–265. doi: 10.1016/j.yhbeh.2007.10.007 PubMedCrossRefGoogle Scholar
  34. Dhabhar FS (2009) Enhancing versus suppressive effects of stress on immune function: implications for immunoprotection and immunopathology. NeuroImmunoModulation 16(5):300–317. doi: 10.1159/000216188 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Dittus W (1977) The social regulation of population density and age-sex distribution in the toque monkey. Behaviour 63:281–321CrossRefGoogle Scholar
  36. Dittus WPJ (1980) The social regulation of primate populations: a synthesis. In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold Company, New York, pp 263–286Google Scholar
  37. Domb LG, Pagel M (2001) Sexual swellings advertise female quality in wild baboons. Nature 410(6825):204–206PubMedCrossRefGoogle Scholar
  38. Drews C (1993) The concept and definition of dominance in animal behaviour. Behaviour 125(3):283–313CrossRefGoogle Scholar
  39. Dribe M, Oris M, Pozzi L (2014) Socioeconomic status and fertility before, during, and after the demographic transition: an introduction. Demographic Res S14(7):161–182CrossRefGoogle Scholar
  40. Dunbar RIM (1986) Demography and reproduction. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. University of Chicago Press, Chicago and London, pp 240–249Google Scholar
  41. Fieder M, Huber S (2007) The effects of sex and childless on the association between status and reproductive output in modern society. Evolution and Human Behavior 28:392–398CrossRefGoogle Scholar
  42. Fieder M, Huber S, Bookstein FL, Iber K, Schafer K, Winckler G, Wallner B (2005) Status and reproduction in humans: new evidence for the validity of evolutionary explanations on basis of a university sample. Ethology 111:940–950CrossRefGoogle Scholar
  43. Fitzpatrick CL, Altmann J, Alberts SC (2014) Sources of variance in a female fertility signal: exaggerated estrous swellings in a natural population of baboons. Behav Ecol Sociobiol 68(7):1109–1122. doi: 10.1007/s00265-014-1722-y PubMedPubMedCentralCrossRefGoogle Scholar
  44. Fitzpatrick CL, Altmann J, Alberts SC (2015) Exaggerated sexual swellings and male mate choice in primates: testing the reliable indicator hypothesis in the Amboseli baboons. Anim Behav 104:175–185. doi: 10.1016/j.anbehav.2015.03.019 PubMedPubMedCentralCrossRefGoogle Scholar
  45. Foerster S, Cords M, Monfort SL (2011) Social behavior, foraging strategies, and fecal glucocorticoids in female blue monkeys (Cercopithecus mitis): potential fitness benefits of high rank in a forest guenon. Am J Primatol 73(9):870–882. doi: 10.1002/ajp.20955 PubMedCrossRefGoogle Scholar
  46. Fox JG, Anderson LC, Loew FM, Quimby FW (2002) Laboratory animal medicine. Elsevier, AmsterdamGoogle Scholar
  47. Frank LG, Weldele ML, Glickman SE (1995) Masculinization costs in hyaenas. Nature 377(6550):584–585PubMedCrossRefGoogle Scholar
  48. 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(6040):357–360PubMedPubMedCentralCrossRefGoogle Scholar
  49. Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602CrossRefGoogle Scholar
  50. Hajat A, Kaufman JS, Rose KM, Siddiqi A, Thomas JC (2011) Long-term effects of wealth on mortality and self-rated health status. Am J Epidemiol 173(2):192–200. doi: 10.1093/aje/kwq348 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Hansel A, Hong S, Camara RJ, von Kanel R (2010) Inflammation as a psychophysiological biomarker in chronic psychosocial stress. Neurosci Biobehav Rev 35(1):115–121. doi: 10.1016/j.neubiorev.2009.12.012 PubMedCrossRefGoogle Scholar
  52. Hausfater G (1975) Dominance and reproduction in baboons (Papio cynocephalus). Karger, BaselGoogle Scholar
  53. Hausfater G, Watson DF (1976) Social and reproductive correlates of parasite ova emissions by baboons. Nature 262(5570):688–689PubMedCrossRefGoogle Scholar
  54. Hausfater G, Altmann J, Altmann S (1982) Long-term consistency of dominance relations among female baboons (Papio cynocephalus). Science 217:752–755PubMedCrossRefGoogle Scholar
  55. He X, Akil L, Aker WG, Hwang HM, Ahmad HA (2015) Trends in infant mortality in United States: a brief study of the southeastern States from 2005–2009. Int J Environ Res Public Health 12(5):4908–4920. doi: 10.3390/ijerph120504908 PubMedPubMedCentralCrossRefGoogle Scholar
  56. Higham JP, Heistermann M, Maestripieri D (2013) The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses. Behav Ecol Sociobiol 67(1):19–30Google Scholar
  57. Hoffman CL, Higham JP, Heistermann M, Coe CL, Prendergast BJ, Maestripieri D (2011) Immune function and HPA axis activity in free-ranging Rhesus macaques. Physiol Behav 104(3):507–514. doi: 10.1016/j.physbeh.2011.05.021 PubMedPubMedCentralCrossRefGoogle Scholar
  58. Holt-Lunstad J, Smith TB, Layton JB (2010) Social relationships and mortality risk: a meta-analytic review. PLoS Med 7(7):e1000316. doi: 10.1371/journal.pmed.1000316 PubMedPubMedCentralCrossRefGoogle Scholar
  59. Hopcroft RL (2006) Sex, status, and reproductive success in the contemporary United States. Evol Hum Behav 27:104–120CrossRefGoogle Scholar
  60. Hori H, Ozeki Y, Teraishi T, Matsuo J, Kawamoto Y, Kinoshita Y, Suto S, Terada S, Higuchi T, Kunugi H (2010) Relationships between psychological distress, coping styles, and HPA axis reactivity in healthy adults. J Psychiatr Res 44(14):865–873. doi: 10.1016/j.jpsychires.2010.02.007 PubMedCrossRefGoogle Scholar
  61. Hrdy SB (1981) The woman that never evolved. Harvard University Press, CambridgeGoogle Scholar
  62. Huber S, Bookstein FL, Fieder M (2010) Socioeconomic status, education, and reproduction in modern women: an evolutionary perspective. Am J Hum Biol 22(5):578–587. doi: 10.1002/ajhb.21048 PubMedCrossRefGoogle Scholar
  63. Kaplan GA, Keil JE (1993) Socioeconomic factors and cardiovascular disease: a review of the literature. Circulation 88(4 Pt 1):1973–1998PubMedCrossRefGoogle Scholar
  64. Kaplan JR, Chen H, Appt SE, Lees CJ, Franke AA, Berga SL, Wilson ME, Manuck SB, Clarkson TB (2010) Impairment of ovarian function and associated health-related abnormalities are attributable to low social status in premenopausal monkeys and not mitigated by a high-isoflavone soy diet. Hum Reprod 25(12):3083–3094. doi: 10.1093/humrep/deq288 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Kerhoas D, Perwitasari-Farajallah D, Agil M, Widdig A, Engelhardt A (2014) Social and ecological factors influencing offspring survival in wild macaques. Behav Ecol 25(5):1164–1172. doi: 10.1093/beheco/aru099 PubMedPubMedCentralCrossRefGoogle Scholar
  66. Kleindorfer S, Wasser SK (2004) Infant handling and mortality in yellow baboons (Papio cynocephalus): evidence for female reproductive competition? Behav Ecol Sociobiol 56(4):328–337. doi: 10.1007/s00265-004-0798-1 CrossRefGoogle Scholar
  67. Kunz-Ebrecht SR, Kirschbaum C, Steptoe A (2004) Work stress, socioeconomic status and neuroendocrine activation over the working day. Soc Sci Med 58(8):1523–1530. doi: 10.1016/s0277-9536(03)00347-2 Google Scholar
  68. Lantz PM, Golberstein E, House JS, Morenoff J (2010) Socioeconomic and behavioral risk factors for mortality in a national 19-year prospective study of US adults. Soc Sci Med 70(10):1558–1566. doi: 10.1016/j.socscimed.2010.02.003 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Lawson DW, Mace R (2010) Optimizing modern family size: trade-offs between fertility and the economic costs of reproduction. Human Nat (Hawthorne, NY) 21(1):39–61. doi: 10.1007/s12110-010-9080-6:Google Scholar
  70. Loisel DA, Rockman MV, Wray GA, Altmann J, Alberts SC (2006) Ancient polymorphism and functional variation in the primate MHC-DQA1 5′ cis-regulatory region. Proc Natl Acad Sci USA 103(44):16331–16336. doi: 10.1073/pnas.0607662103 PubMedPubMedCentralCrossRefGoogle Scholar
  71. Loucks AB, Verdun M, Heath EM (1998) Low energy availability, not stress of exercise, alters LH pulsatility in exercising women. J Appl Physiol 84(1):37–46PubMedGoogle Scholar
  72. Loucks EB, Pilote L, Lynch JW, Richard H, Almeida ND, Benjamin EJ, Murabito JM (2010) Life course socioeconomic position is associated with inflammatory markers: the Framingham offspring study. Soc Sci Med 71(1):187–195. doi: 10.1016/j.socscimed.2010.03.012 PubMedCrossRefGoogle Scholar
  73. Maestripieri D (1994) Social structure, infant handling, and mothering styles in group-living old world monkeys. Int J Primatol 15(4):531–553. doi: 10.1007/BF02735970 CrossRefGoogle Scholar
  74. Maestripieri D, Georgiev AV (2015) What cortisol can tell us about the costs of sociality and reproduction among free-ranging rhesus macaque females on Cayo Santiago. Am J Primatol. doi: 10.1002/ajp.22368 PubMedPubMedCentralGoogle Scholar
  75. Majolo B, Lehmann J, de Bortoli Vizioli A, Schino G (2012) Fitness-related benefits of dominance in primates. Am J Phys Anthropol 147(4):652–660. doi: 10.1002/ajpa.22031 PubMedCrossRefGoogle Scholar
  76. McEwen BS (1998) Protective and damaging effects of stress mediators. N Engl J Med 338(3):171–179. doi: 10.1056/nejm199801153380307 PubMedCrossRefGoogle Scholar
  77. Michopoulos V, Higgins M, Toufexis D, Wilson ME (2012a) Social subordination produces distinct stress-related phenotypes in female rhesus monkeys. Psychoneuroendocrinology 37(7):1071–1085. doi: 10.1016/j.psyneuen.2011.12.004 PubMedPubMedCentralCrossRefGoogle Scholar
  78. Michopoulos V, Reding KM, Wilson ME, Toufexis D (2012b) Social subordination impairs hypothalamic-pituitary-adrenal function in female rhesus monkeys. Horm Behav 62(4):389–399. doi: 10.1016/j.yhbeh.2012.07.014 PubMedPubMedCentralCrossRefGoogle Scholar
  79. Modolo L, Martin RD (2008) Reproductive success in relation to dominance rank in the absence of prime-age males in Barbary macaques. Am J Primatol 70(1):26–34. doi: 10.1002/ajp.20452 PubMedCrossRefGoogle Scholar
  80. Mosher WD, Bachrach CA (1996) Understanding US fertility: continuity and change in the National Survey of Family Growth, 1988–1995. Fam Plann Perspect 28(1):4–12PubMedCrossRefGoogle Scholar
  81. Munck A, Guyre PM (1986) Glucocorticoid physiology, pharmacology and stress. Adv Exp Med Biol 196:81–96PubMedCrossRefGoogle Scholar
  82. National Center for Health Statistics (1975) Infant mortality rates: socioeconomic factors. In: Vital and health statistics, vol 21. Department of Health, Education, and Welfare Publications, Rockville, MCGoogle Scholar
  83. National Center for Health Statistics (2011) Health, United States, 2011: with special feature on socioeconomic status and health.
  84. Nguyen N, Van Horn RC, Alberts SC, Altmann J (2009) “Friendships” between new mothers and adult males: adaptive benefits and determinants in wild baboons. Behav Ecol Sociobiol 63(9):1331–1344. doi: 10.1007/s00265-009-0786-6 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pace TW, Hu F, Miller AH (2007) Cytokine-effects on glucocorticoid receptor function: relevance to glucocorticoid resistance and the pathophysiology and treatment of major depression. Brain Behav Immun 21(1):9–19. doi: 10.1016/j.bbi.2006.08.009 PubMedPubMedCentralCrossRefGoogle Scholar
  86. Packer C (1979) Male dominance and reproductive activity in Papio anubis. Anim Behav 27:37–45PubMedCrossRefGoogle Scholar
  87. Packer C, Collins DA, Sindimwo A, Goodall J (1995) Reproductive constraints on aggressive competition in female baboons. Nature 373(6509):60–63. doi: 10.1038/373060a0 PubMedCrossRefGoogle Scholar
  88. Padgett DA, Marucha PT, Sheridan JF (1998) Restraint stress slows cutaneous wound healing in mice. Brain Behav Immun 12(1):64–73. doi: 10.1006/brbi.1997.0512 PubMedCrossRefGoogle Scholar
  89. Palombit RA, Cheney DL, Seyfarth RM (2001) Female–female competition for male ‘friends’ in wild chacma baboons (Papio cynocephalus ursinus). Anim Behav 61(6):1159–1171. doi: 10.1006/anbe.2000.1690 CrossRefGoogle Scholar
  90. Paul A, Kuester J (1996) Differential reproduction in male and female Barbary macaques. In: Fa JE, Lindburg DG (eds) Evolution and ecology of macaque species. Cambridge University Press, Cambridge, pp 293–317Google Scholar
  91. Pollitt RA, Kaufman JS, Rose KM, Diez-Roux AV, Zeng D, Heiss G (2008) Cumulative life course and adult socioeconomic status and markers of inflammation in adulthood. J Epidemiol Community Health 62(6):484–491. doi: 10.1136/jech.2006.054106 PubMedCrossRefGoogle Scholar
  92. Ray O (2004) The revolutionary health science of psychoneuroimmunology: a new paradigm for understanding health and treating illness. Ann N Y Acad Sci 1032:35–51PubMedCrossRefGoogle Scholar
  93. Ray JC, Sapolsky RM (1992) Styles of male social-behavior and their endocrine correlates among high-ranking wild baboons. Am J Primatol 28(4):231–250CrossRefGoogle Scholar
  94. Recognition and Alleviation of Pain in Laboratory Animals (2009) National Academy of Sciences, Washington, DCGoogle Scholar
  95. Rosmond R, Bjorntorp P (2000) The hypothalamic-pituitary-adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. J Intern Med 247(2):188–197PubMedCrossRefGoogle Scholar
  96. Samuels A, Altmann J (1991) Baboons of the Amboseli basin: demographic stability and change. Int J Primatol 12(1):1–19. doi: 10.1007/BF02547555 CrossRefGoogle Scholar
  97. Sapolsky RM (1982) The endocrine stress-response and social status in the wild baboon. Horm Behav 16(3):279–292PubMedCrossRefGoogle Scholar
  98. Sapolsky R (1983) Individual differences in cortisol secretory patterns in the wild baboon: role of negative feedback sensitivity. Endocrinology 113:2263–2269PubMedCrossRefGoogle Scholar
  99. Sapolsky RM (2004) Social status and health in humans and other animals. Annu Rev Anthropol 33:393–418CrossRefGoogle Scholar
  100. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648–652. doi: 10.1126/science.1106477 PubMedCrossRefGoogle Scholar
  101. Sapolsky RM, Ray JC (1989) Styles of dominance and their endocrine correlates among wild olive baboons (Papio anubis). Am J Primatol 18:1–13CrossRefGoogle Scholar
  102. Sapolsky RM, Alberts SC, Altmann J (1997) Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatry 54(12):1137–1143PubMedCrossRefGoogle Scholar
  103. Shively CA (1998) Social subordination stress, behavior and central monoaminergic function in female cynomolgus monkeys. Biol Psychiatry 44(9):882–891PubMedCrossRefGoogle Scholar
  104. Shively CA, Kaplan JR (1991) Stability of social-status rankings of female cynomolgus monkeys, of varying reproductive condition, in different social-groups. Am J Primatol 23(4):239–245CrossRefGoogle Scholar
  105. Shively CA, Willard SL (2012) Behavioral and neurobiological characteristics of social stress versus depression in nonhuman primates. Exp Neurol 233(1):87–94. doi: 10.1016/j.expneurol.2011.09.026 PubMedPubMedCentralCrossRefGoogle Scholar
  106. Shively CA, Laber-Laird K, Anton RF (1997) Behavior and physiology of social stress and depression in female cynomolgus monkeys. Biol Psychiatry 41(8):871–882. doi: 10.1016/S0006-3223(96)00185-0 PubMedCrossRefGoogle Scholar
  107. Shively CA, Register TC, Clarkson TB (2009) Social stress, visceral obesity, and coronary artery atherosclerosis: product of a primate adaptation. Am J Primatol 71(9):742–751. doi: 10.1002/ajp.20706 PubMedPubMedCentralCrossRefGoogle Scholar
  108. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302(5648):1231–1234. doi: 10.1126/science.1088580 PubMedCrossRefGoogle Scholar
  109. 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 Biol Sci 276(1670):3099–3104. doi: 10.1098/rspb.2009.0681 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Silk JB, Beehner JC, Bergman 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(15):1359–1361. doi: 10.1016/j.cub.2010.05.067 PubMedCrossRefGoogle Scholar
  111. Sjors A, Ljung T, Jonsdottir IH (2014) Diurnal salivary cortisol in relation to perceived stress at home and at work in healthy men and women. Biol Psychol 99:193–197. doi: 10.1016/j.biopsycho.2014.04.002 Google Scholar
  112. Skirbekk V (2008) Fertility trends by social status. Demographic Res 18(5):145–180CrossRefGoogle Scholar
  113. Small CM, Manatunga AK, Klein M, Dominguez CE, Feigelson HS, McChesney R, Marcus M (2010) Menstrual cycle variability and the likelihood of achieving pregnancy. Rev Environ Health 25(4):369–378Google Scholar
  114. Smuts BB (1985) Sex and friendship in baboons. Aldine, New YorkGoogle Scholar
  115. Steptoe A, Kunz-Ebrecht S, Owen N, Feldman PJ, Willemsen G, Kirschbaum C, Marmot M (2003) Socioeconomic status and stress-related biological responses over the working day. Psychosom Med 65(3):461–470Google Scholar
  116. Stevens VC, Sparks SJ, Powell JE (1970) Levels of estrogens, progestogens and luteinizing hormone during the menstrual cycle of the baboon. Endocrinology 87(4):658–666PubMedCrossRefGoogle Scholar
  117. Stewart CB, Disotell TR (1998) Primate evolution—in and out of Africa. Curr Biol 8(16):R582–R588PubMedCrossRefGoogle Scholar
  118. Strier KB (2003) Primate behavioral ecology, 2nd edn. Allyn and Bacon, BostonGoogle Scholar
  119. Stringhini S, Tabak AG, Akbaraly TN, Sabia S, Shipley MJ, Marmot MG, Brunner EJ, Batty GD, Bovet P, Kivimaki M (2012) Contribution of modifiable risk factors to social inequalities in type 2 diabetes: prospective Whitehall II cohort study. BMJ 345:e5452. doi: 10.1136/bmj.e5452 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Szekely T, Reynolds JD (1995) Evolutionary transitions in parental care in shorebirds. Proc R Soc Lond: Biol Sci 262:1363. doi: 10.1098/rspb.1995.0176 CrossRefGoogle Scholar
  121. Taub DM (1980) Female choice and mating strategies among wild Barbary macaques. In: Lindburg DG (ed) The macaques: studies in ecology, behavior and evolution. Van Nostrand Reinhold Company, New York, pp 287–344Google Scholar
  122. Tung J, Barreiro LB, Johnson ZP, Hansen KD, Michopoulos V, Toufexis D, Michelini K, Wilson ME, Gilad Y (2012) Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proc Natl Acad Sci USA 109(17):6490–6495. doi: 10.1073/pnas.1202734109 PubMedPubMedCentralCrossRefGoogle Scholar
  123. van Noordwijk MA, van Schaik CP (1987) Competition among female long-tailed macaques, Macaca fascicularis. Anim Behav 35:577–589CrossRefGoogle Scholar
  124. van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40(1):105–130. doi: 10.1007/BF02557705 PubMedCrossRefGoogle Scholar
  125. van Schaik CP (1983) Why are diurnal primates living in groups? Behaviour 87:120–144CrossRefGoogle Scholar
  126. Van Schaik CP (2000) Infanticide by male primates: the sexual selection hypothesis revisited. In: Van Schaik CP, Janson PC (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 27–60CrossRefGoogle Scholar
  127. van Schaik CP, van Noordwijk MA, de Boer RJ, den Tonkelaar I (1983) The effect of group size on time budgets and social behavior in wild long-tailed macaques (Macaca fascicularis). Behav Ecol Sociobiol 13:173–181CrossRefGoogle Scholar
  128. van Schaik CP, Van Noordwijk MA, van Bragt T, Blankenstein MA (1991) A pilot study of the social correlates of levels of urinary cortisol, prolactin, and testosterone in wild long-tailed macaques (Macaca fascicularis). Primates 32:345–356CrossRefGoogle Scholar
  129. Vandenheede H, Vikhireva O, Pikhart H, Kubinova R, Malyutina S, Pajak A, Tamosiunas A, Peasey A, Simonova G, Topor-Madry R, Marmot M, Bobak M (2014) Socioeconomic inequalities in all-cause mortality in the Czech Republic, Russia, Poland and Lithuania in the 2000s: findings from the HAPIEE study. J Epidemiol Community Health 68(4):297–303. doi: 10.1136/jech-2013-203057 PubMedPubMedCentralCrossRefGoogle Scholar
  130. Virgin CE, Sapolsky RM (1997) Styles of male social behavior and their endocrine correlates among low-ranking baboons. Am J Primatol 42:25–39PubMedCrossRefGoogle Scholar
  131. Walker BR (2007) Glucocorticoids and cardiovascular disease. Eur J Endocrinol 157(5):545–559. doi: 10.1530/eje-07-0455 PubMedCrossRefGoogle Scholar
  132. Wasser SK (1996) Reproductive control in wild baboons measured by fecal steroids. Biol Reprod 55:393–399PubMedCrossRefGoogle Scholar
  133. Wasser SK, Norton GW, Rhine RJ, Klein N, Kleindorfer S (1998) Ageing and social rank effects on the reproductive system of free-ranging yellow baboons (Papio cynocephalus) at Mikumi National Park, Tanzania. Hum Reprod Update 4(4):430–438PubMedCrossRefGoogle Scholar
  134. Wasser SK, Norton GW, Kleindorfer S, Rhine RJ (2004) Population trend alters the effects of maternal dominance rank on lifetime reproductive success in yellow baboons (Papio cynocephalus). Behav Ecol Sociobiol 56(4):338–345. doi: 10.1007/s00265-004-0797-2 CrossRefGoogle Scholar
  135. Weeden J, Abrams MJ, Green MC, Sabini J (2006) Do high-status people really have fever children? Hum Nat 17:377–392PubMedCrossRefGoogle Scholar
  136. Weiss JM (1968) Effects of coping responses on stress. J Comp Physiol Psychol 65:251–260PubMedCrossRefGoogle Scholar
  137. Whirledge S, Cidlowski JA (2010) Glucocorticoids, stress, and fertility. Minerva Endocrinol 35(2):109–125PubMedPubMedCentralGoogle Scholar
  138. Whitten PL (1986) Infants and adult males. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT (eds) Primate societies. The University of Chicago Press, Chicago and London, pp 343–357Google Scholar
  139. Wilson ME, Gordon TP, Bernstein IS (1978) Timing of births and reproductive success in rhesus monkey social groups. J Med Primatol 7(4):202–212PubMedGoogle Scholar
  140. Zuberi SK, Salman SH, Virji RN, Sana S, Kumari S, Zehra N (2015) A hospital-based comparative study of the knowledge, attitudes and practices of family planning among women belonging to different socio-economic status. J Pak Med Assoc 65(5):579–584PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Wake Forest School of MedicineWinston-SalemUSA

Personalised recommendations