Social status predicts wound healing in wild baboons

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 23, 2012, Pages 9017-9022

  Archie, Elizabeth A ^a   Altmann, Jeanne ^b,c,d   Alberts, Susan C ^c,e  

^a UNIVERSITY OF NOTRE DAME   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c INSTITUTE OF PRIMATE RESEARCH   (Kenya)

^d UNIVERSITY OF NAIROBI   (Kenya)

^e DUKE UNIVERSITY   (United States)

Author keywords

Dominance rank; Ecoimmunology; Glucocorticoid hormones; Papio cynocephalus; Savanna baboon

Indexed keywords

GLUCOCORTICOID; IMMUNOSUPPRESSIVE AGENT; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; BABOON; DISEASES; FEEDING; FEMALE; HEALTH CARE COST; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOSUPPRESSIVE TREATMENT; INJURY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REPRODUCTION; SEASON; SOCIAL ENVIRONMENT; SOCIAL STATUS; SURVIVAL; WOUND HEALING;

AGE FACTORS; ANIMALS; GLUCOCORTICOIDS; INCIDENCE; KENYA; MALE; MONKEY DISEASES; OBSERVER VARIATION; PAPIO; REPRODUCTION; SOCIAL DOMINANCE; TESTOSTERONE; WOUND HEALING;

ANIMALIA; PAPIO; PAPIO CYNOCEPHALUS; VERTEBRATA;

EID: 84861880588     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206391109     Document Type: Article

References (82)

1. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308: 648-652.
2. McEwen BS, Gianaros PJ (2010) Central role of the brain in stress and adaptation: Links to socioeconomic status, health, and disease. Ann N Y Acad Sci 1186:190-222.
3. Sapolsky RM (2004) Social status and health in humans and other animals. Annu Rev Anthropol 33:393-418.
4. Adler NE, et al. (1994) Socioeconomic status and health. The challenge of the gradient. Am Psychol 49:15-24. (Pubitemid 24976661)
5. Fairbanks B, Hawley DM (2012) Interactions between host social behavior, physiology, and disease susceptibility. Ecoimmunology, eds Demas GE, Nelson RJ (Oxford Univ Press, New York), pp 440-467.
6. Cohen S, et al. (1997) Chronic social stress, social status, and susceptibility to upper respiratory infections in nonhuman primates. Psychosom Med 59:213-221.
7. Lindstrom KM (2004) Social status in relation to Sindbis virus infection clearance in greenfinches. Behav Ecol Sociobiol 55:236-241.
8. Nunn CL, Altizer S (2006) Infectious Diseases in Primates: Behavior, Ecology, and Evolution (Oxford Univserity Press, Oxford, UK).
9. Lloyd-Smith JO, Schreiber SJ, Kopp PE, GetzWM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359. (Pubitemid 41643951)
10. Davidson RS, Marion G, Hutchings MR (2008) Effects of host social hierarchy on disease persistence. J Theor Biol 253:424-433.
11. Cohen S, Janicki-Deverts D, Miller GE (2007) Psychological stress and disease. JAMA 298:1685-1687. (Pubitemid 47606658)
12. McEwen BS (1998) Stress, adaptation, and disease. Allostasis and allostatic load. Ann N Y Acad Sci 840:33-44.
13. Creel S (2001) Social dominance and stress hormones. Trends Ecol Evol 16: 491-497.
14. Abbott DH, et al. (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67-82. (Pubitemid 36293276)
15. Muehlenbein MP, Bribiescas RG (2005) Testosterone-mediated immune functions and male life histories. Am J Hum Biol 17:527-558. (Pubitemid 41684269)
16. Stearns SC (1992) The Evolution of Life Histories (Oxford Univ Press, Oxford, UK).
17. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603-622.
18. Mills SC, et al. (2010) Fitness trade-offs mediated by immunosuppression costs in a small mammal. Evolution 64:166-179.
19. Norris K, Anwar M, Read AF (1994) Reproductive effort influences the prevalence of haematozoan parasites in great tits. J Anim Ecol 63:601-610.
20. Muehlenbein MP, Alger J, Cogswell F, James M, Krogstad D (2005) The reproductive endocrine response to Plasmodium vivax infection in Hondurans. Am J Trop Med Hyg 73:178-187. (Pubitemid 41278769)
21. Mills SC, et al. (2009) Testosterone-mediated effects on fitness-related phenotypic traits and fitness. Am Nat 173:475-487.
22. Roberts ML, Buchanan KL, Hasselquist D, Evans MR (2007) Effects of testosterone and corticosterone on immunocompetence in the zebra finch. Horm Behav 51:126-134. (Pubitemid 44838638)
23. HauM (2007) Regulation of male traits by testosterone: Implications for the evolution of vertebrate life histories. Bioessays 29:133-144.
24. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257-261.
25. Casto JM, Nolan V, Jr., Ketterson ED (2001) Steroid hormones and immune function: Experimental studies in wild and captive dark-eyed juncos (Junco hyemalis). Am Nat 157:408-420. (Pubitemid 32235239)
26. Negro SS, Caudron AK, Dubois M, Delahaut P, Gemmell NJ (2010) Correlation between male social status, testosterone levels, and parasitism in a dimorphic polygynous mammal. PLoS ONE 5:e12507.
27. Roberts ML, Buchanan KL, Evans MR, Marin RH, Satterlee DG (2009) The effects of testosterone on immune function in quail selected for divergent plasma corticosterone response. J Exp Biol 212:3125-3131.
28. Padgett DA, Marucha PT, Sheridan JF (1998) Restraint stress slows cutaneous wound healing in mice. Brain Behav Immun 12:64-73. (Pubitemid 29012195)
29. Kiecolt-Glaser JK, Marucha PT, Malarkey WB, Mercado AM, Glaser R (1995) Slowing of wound healing by psychological stress. Lancet 346:1194-1196.
30. Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: A review of the evidence. Anim Behav 68:227-239. (Pubitemid 38946557)
31. Nunn CL, Lindenfors P, Pursall ER, Rolff J (2009) On sexual dimorphism in immune function. Philos Trans R Soc Lond B Biol Sci 364:61-69.
32. Duckworth RA, Mendonça MT, Hill GE (2001) A condition dependent link between testosterone and disease resistance in the house finch. Proc Biol Sci 268:2467-2472. (Pubitemid 33151455)
33. Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21:55-89. (Pubitemid 32266068)
34. Dhabhar FS (2009) Enhancing versus suppressive effects of stress on immune function: Implications for immunoprotection and immunopathology. Neuroimmunomodulation 16:300-317.
35. Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: When and how. J Neuroendocrinol 15:711-724. (Pubitemid 36874367)
36. Detillion CE, Craft TK, Glasper ER, Prendergast BJ, DeVries AC (2004) Social facilitation of wound healing. Psychoneuroendocrinology 29:1004-1011. (Pubitemid 38833527)
37. Demas GE, Zysling DA, Beechler BR, Muehlenbein MP, French SS (2011) Beyond phytohaemagglutinin: Assessing vertebrate immune function across ecological contexts. J Anim Ecol 80:710-730.
38. Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61:681-692. (Pubitemid 23397926)
39. Wilson BS (1992) Tail injuries increase the risk of mortality in free-living lizards (Uta stansburiana). Oecologia 92:145-152.
40. Alberts SC, Watts HE, Altmann J (2003) Queuing and queue-jumping: Long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821-840. (Pubitemid 36453601)
41. Alberts SC, Buchan JC, Altmann J (2006) Sexual selection in wild baboons: From mating opportunities to paternity success. Anim Behav 72:1177-1196. (Pubitemid 44634363)
42. Sapolsky RM, Alberts SC, Altmann J (1997) Hypercortisolism associated with social subordinance or social isolation among wild baboons. Arch Gen Psychiatry 54: 1137-1143. (Pubitemid 27524379)
43. Altmann J, Gesquiere L, Galbany J, Onyango PO, Alberts SC (2010) Life history context of reproductive aging in a wild primate model. Ann N Y Acad Sci 1204:127-138.
44. Gesquiere LR, Onyango PO, Alberts SC, Altmann J (2011) Endocrinology of year-round reproduction in a highly seasonal habitat: Environmental variability in testosterone and glucocorticoids in baboon males. Am J Phys Anthropol 144:169-176.
45. Gesquiere L, et al. (2011) Life at the top: Energetic and psychological stress in wild male primates. Science 333:357-360.
46. Rasmussen KLR (1985) Changes in the activity budgets of yellow baboons (Papio cynocephalus) during sexual consortships. Behav Ecol Sociobiol 17:161-170.
47. Alberts SC, Altmann J, WilsonML (1996) Mate guarding constrains foraging activity of male baboons. Anim Behav 51:1269-1277.
48. Hausfater G, Watson DF (1976) Social and reproductive correlates of parasite ova emissions by babonns. Nature 262:688-689.
49. Alberts SC, Sapolsky RM, Altmann J (1992) Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm Behav 26:167-178.
50. McFarlane D, Wolf RF, McDaniel KA, White GL (2011) Age-associated alteration in innate immune response in captive baboons. J Gerontol A Biol Sci Med Sci 66: 1309-1317.
51. Post DG, Hausfater G, McCuskey SA (1980) Feeding behavior of yellow baboons (Papio cynocephalus): Relationship to age, gender and dominance rank. Folia Primatol (Basel) 34:170-195.
52. Sapolsky RM (1993) Endocrinology alfresco: Psychoendocrine studies of wild baboons. Recent Prog Horm Res 48:437-468.
53. Sapolsky RM, Spencer EM (1997) Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol 273:R1346-R1351.
54. MacCormick HA, et al. Male and female aggression: Lessons from sex, rank, age, and injruy in olive baboons. Behav Ecol, 23:684-691.
55. Drews C (1996) Contexts and patterns of injuries in free-ranging male baboons (Papio cynocephalus). Behaviour 133:443-474.
56. Banks WA, Altmann J, Sapolsky RM, Phillips-Conroy JE, Morley JE (2003) Serum leptin levels as a marker for a syndrome X-like condition in wild baboons. J Clin Endocrinol Metab 88:1234-1240. (Pubitemid 36337783)
57. Altmann J, Muruthi P (1988) Differences in daily life between semi-provisioned and wild-feeding baboons. Am J Primatol 15:213-222.
58. Juster RP, McEwen BS, Lupien SJ (2010) Allostatic load biomarkers of chronic stress and impact on health and cognition. Neurosci Biobehav Rev 35:2-16.
59. Norris K, Evans MR (2000) Ecological immunology: Life history trade-offs and immune defense in birds. Behav Ecol 11:19-26. (Pubitemid 30146972)
60. Muehlenbein MP, Watts DP, Whitten PL (2004) Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Am J Primatol 64:71-82. (Pubitemid 39428851)
61. Wedekind C, Folstad I (1994) Adaptive or nonadaptive immunosuppression by sex hormones. Am Nat 143:936-938.
62. Gilliver SC, Ashworth JJ, Ashcroft GS (2007) The hormonal regulation of cutaneous wound healing. Clin Dermatol 25:56-62. (Pubitemid 46177465)
63. Martin LB, 2nd, Weil ZM, Nelson RJ (2007) Immune defense and reproductive pace of life in Peromyscus mice. Ecology 88:2516-2528. (Pubitemid 351345109)
64. Martin LB, 2nd, Hasselquist D, Wikelski M (2006) Investment in immune defense is linked to pace of life in house sparrows. Oecologia 147:565-575.
65. Sheldon BC, Verhulst S (1996) Ecological immunology: Costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 11:317-321.
66. Olsson M, Wapstra E, Madsen T, Silverin B (2000) Testosterone, ticks and travels: A test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc Biol Sci 267:2339-2343.
67. Granger DA, Booth A, Johnson DR (2000) Human aggression and enumerative measures of immunity. Psychosom Med 62:583-590. (Pubitemid 30604803)
68. Singh AB, et al. (2002) The effects of varying doses of T on insulin sensitivity, plasma lipids, apolipoproteins, and C-reactive protein in healthy young men. J Clin Endocrinol Metab 87:136-143. (Pubitemid 34084682)
69. Muehlenbein MP (2006) Intestinal parasite infections and fecal steroid levels in wild chimpanzees. Am J Phys Anthropol 130:546-550.
70. Muller MN, Wrangham RW (2004) Dominance, aggression and testosterone in wild chimpanzees: A test of the 'challenge hypothesis'. Anim Behav 67:113-123. (Pubitemid 38204046)
71. Martin LB, Weil ZM, Kuhlman JR, Nelson RJ (2006) Trade-offs within the immune systems of female White-footed Mice, Peromyscus leucopus. Funct Ecol 20:630-636. (Pubitemid 44035842)
72. Koski KG, Su Z, Scott ME (1999) Energy deficits suppress both systemic and gut immunity during infection. Biochem Biophys Res Commun 264:796-801.
73. Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000-1015.
74. Kiecolt-Glaser JK, et al. (2005) Hostile marital interactions, proinflammatory cytokine production, and wound healing. Arch Gen Psychiatry 62:1377-1384. (Pubitemid 41746615)
75. Bauer ME, Jeckel CMM, Luz C (2009) The role of stress factors during aging of the immune system. Ann N Y Acad Sci 1153:139-152.
76. Hoffman CL, et al. (2011) Immune function and HPA axis activity in free-ranging rhesus macaques. Physiol Behav 104:507-514.
77. Smuts BB (1985) Sex and Friendship in Baboons (Aldine Transaction, New York).
78. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of 'friendships' to female baboons: Experimental and observational evidence. Anim Behav 54:599-614. (Pubitemid 27413941)
79. Manson JH (1994) Mating patterns, mate choice, and birth season heterosexual relationships in free-ranging rhesus macaques. Primates 35:417-433.
80. Hausfater G (1975) Dominance and Reproduction in Baboons: A Quantitative Analysis (S. Karger, Basel).
81. Alberts SC, Altmann J (1995) Preparation and activation: Determinants of age at reproductive maturity in male baboons. Behav Ecol Sociobiol 36:397-406. (Pubitemid 26448298)
82. Alberts SC, Altmann J (1995) Balancing costs and opportunities: Dispersal in male baboons. Am Nat 145:279-306.