Testosterone predicts future dominance rank and mating activity among male chacma baboons

Behavioral Ecology and Sociobiology

Volumn 59, Issue 4, 2006, Pages 469-479

  Beehner, J C ^a,b   Bergman, T J ^a   Cheney, D L ^a   Seyfarth, R M ^a   Whitten, P L ^c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

Aggression; Baboon; Challenge hypothesis; Dominance rank; Testosterone

Indexed keywords

AGGRESSION; DOMINANCE; MALE BEHAVIOR; MATING BEHAVIOR; PRIMATE; TESTOSTERONE;

PAPIO HAMADRYAS; PAPIO URSINUS;

EID: 30944431725     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-005-0071-2     Document Type: Article

References (87)

1. 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
2. Alberts S, Watts H, Altmann J (2003) Queuing and queue-jumping: long-term patterns of reproductive skew in male savannah baboons, Papio cynocephalus. Anim Behav 65:821-840
3. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:229-267
4. Bardin CW (1996) The anabolic action of testosterone. N Engl J Med 335:52-53
5. Beehner JC, Whitten PL (2004) Modifications of a field method for fecal steroid analysis in baboons. Physiol Behav 82:269-277
6. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM (2005) Interactions in male baboons: the importance of both males' testosterone. Behav Ecol Sociobiol
7. Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL Social instability and social stress in male chacma baboons. Anim Behav (in press)
8. Bernstein IS, Rose RM, Gordon TP (1974) Behavioral and environmental events influencing primate testosterone levels. J Hum Evol 3:517-525
9. Bernstein IS, Rose RM, Gordon TP (1977) Behavioural and hormonal responses of male rhesus monkeys introduced to females in the breeding and nonbreeding seasons. Anim Behav 25:609-614
10. Bernstein IS, Rose RM, Gordon TP, Grady CL (1979) Agonistic rank, aggression, social context, and testosterone in male pigtail monkeys. Aggress Behav 5:329-339
11. Bhasin D, Storer T, Berman N, Callegari C, Clevenger D, Phillips J, Bunnell T, Tricker R, Shirazi A, Casaburi R (1996) The effects of supraphysiologic doses of testosterone on muscle size and strength or normal men. N Engl J Med 335:1-7
12. Bribiescas RG (1996) Testosterone levels among Ache hunter/gatherer men: a functional interpretation of population variation among adult males. Hum Nat 7:163-188
13. Brockman DK, Whitten PL, Richard AF, Schneider A (1998) Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. Am J Phys Anthropol 105:137-151
14. Buck CL, Barnes BM (2003) Androgen in free-living arctic ground squirrels: seasonal changes and influence of staged male-male aggressive encounters. Horm Behav 43:318-326
15. Bulger JB (1993) Dominance rank and access to estrous females in male savanna baboons. Behaviour 127:67-103
16. Bulger JB, Hamilton WJ (1987) Rank and density correlates of inclusive fitness measures in a natural chacma baboon (Papio ursinus) population. Int J Primatol 8:635-650
17. Bulger JB, Hamilton WJ (1988) Inbreeding and reproductive success in a natural chacma baboon, Papio cynocephalus ursinus. Anim Behav 36:574-578
18. Cavigelli SA, Pereira ME (2000) Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm Behav 37:246-255
19. 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
20. Creel S, Wildt DE, Monfort SL (1993) Aggression, reproduction, and androgens in wild dwarf mongooses: a test of the challenge hypothesis. Am Nat 141:816-825
21. Dabbs JM, Mohammed S (1992) Male and female salivary testosterone concentrations before and after sexual activity. Physiol Behav 52:195-197
22. Dixson AF (1998) Primate sexuality. Oxford University Press, Oxford
23. Eberhardt JA, Keverne EB, Meller RE (1980) Social influences on plasma testosterone levels in male talapoin monkeys. Horm Behav 14:251-259
24. Ellis L (1995) Dominance and reproductive success among non-human animals: a cross-species comparison. Ethol Sociobiol 16:257-333
25. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603-622
26. Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257-261
27. Grossman CJ, Roselle GA, Mendenhall CL (1991) Sex steroid regulation of autoimmunity. J Steroid Biochem Mol Biol 40:649-659
28. Hamilton WJ (1984) Significance of paternal investment by primates to the evolution of male-female associations. In: Taub DM (ed) Primate paternalism. Van Nostrand Reinhold, New York, pp 309-335
29. Hamilton WJ, Bulger JB (1990) Natal male baboon rank rises and successful challenges to resident alpha males. Behav Ecol Sociobiol 26:357-363
30. Harding CF, Feder HH (1976) Relation between individual differences in sexual behavior and plasma testosterone levels in the guinea pig. Endocrinology 98:1198-1205
31. Hart BL (1974) Gonadal androgen and sociosexual behavior of male mammals: a comparative analysis. Psychol Bull 81:383-400
32. Hews DK, Moore MC (1995) Influence of androgens on differentiation of secondary sex characteristics in tree lizards, Urosaurus ornatus. Gen Comp Endocrinol 97:86-102
33. Higely JD, Mehlman PT, Poland RE, Taub DM, Vickers J, Suomi SJ, Linnoila M (1996) CSF testosterone and 5-HIAA correlate with different types of aggressive behaviors. Biol Psychiatry 40:1067-1082
34. Holekamp KE, Smale L (1998) Dispersal status influences hormones and behavior in the male spotted hyena. Horm Behav 33:205-216
35. Holekamp KE, Smale L, Simpson HB, Holekamp NA (1984) Hormonal influences on natal dispersal in free-living Belding's ground squirrels (Spermophilus beldingi). Horm Behav 18:465-483
36. Ketterson ED, Nolan JV (1992) Hormones and life histories: an integrative approach. Am Nat 140:S33-S62
37. Kitchen DM, Seyfarth RM, Fischer J, Cheney DL (2003) Loud calls as an indicator of dominance in male baboons (Papio cynocephalus ursinus). Behav Ecol Sociobiol 53:374-384
38. Klein SL (2000) Hormones and mating system affect sex and species differences in immune function among vertebrates. Behav Proc 51:149-166
39. Klinkova E, Heistermann M, Hodges JK (2004) Social parameters and urinary testosterone level in male chimpanzees. Horm Behav 46:474-481
40. Klukowski M, Nelson CE (1998) The challenge hypothesis and seasonal changes in aggression and steroids in male northern fence lizards (Sceloporus undulatus hyacinthinus). Horm Behav 33:197-204
41. 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
42. Macrides F, Bartke A, Dalterio S (1975) Strange females increase plasma testosterone levels in mice. Science 189:1104-1106
43. Marler CA, Moore MC (1988) Evolutionary costs of aggression revealed by testosterone manipulations in free-living male lizards. Behav Ecol Sociobiol 23:21-26
44. Marler CA, Walsberg G, White ML, Moore M (1995) Increased energy expenditure due to increased territorial defense in male lizards after phenotypic manipulation. Behav Ecol Sociobiol 37:225-231
45. Marshall AJ, Hohmann G (2005) Urinary testosterone levels of wild male bonobos (Pan paniscus) in the Lomako Forest, Democratic Republic of Congo. Am J Primatol 65:87-92
46. Mazur A, Booth A (1998) Testosterone and dominance in men. Behav Brain Sci 21:353-397
47. McCaul KD, Gladue BA, Joppa M (1992) Winning, losing, mood, and testosterone. Horm Behav 26:486-504
48. 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. Psychiatry Res 72:89-102
49. 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
50. Muller MN, Wrangham RW (2004) Dominance, aggression and testosterone in wild chimpanzees: a test of the 'challenge hypothesis'. Anim Behav 67:113-123
51. Nakagawa S (2004) A farewell to Bonferroni: the problems of low statistical power and publication bias. Behav Ecol 16:1044-1045
52. Nieuwenhuijsen K, de Neef J, van der Werff J, Bosch T, Slob A (1987) Testosterone, testis size, seasonality, and behavior in group-living stumptail macaques (Macaca arctoides). Horm Behav 21:153-169
53. Nunes S, Duniec TR, Schweppe SA, Holekamp KE (1999) Energetic and endocrine mediation of natal dispersal behavior in Belding's ground squirrels. Horm Behav 35:113-124
54. Olsen NJ, Kovacs W (1996) Gonadal steroids and immunity. Endocr Rev 17:369-384
55. Ostner J, Kappeler PM, Heistermann M (2002) Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav Ecol Sociobiol 52:485-495
56. Owens D, Owens M (1996) Social dominance and reproductive patterns in brown hyaenas, Hyaena brunnea, of the central Kalahari desert. Anim Behav 51:535-551
57. Palombit RA, Seyfarth RM, Cheney DL (1997) The adaptive value of friendships to female baboons: experimental and observational evidence. Anim Behav 54:599-614
58. Palombit RA, Cheney DL, Fischer J, Johnson S, Rendall D, Seyfarth RM, Silk JB (2000) Male infanticide and defense of infants in wild chacma baboons. In: van Schaik CP, Janson CH (eds) Infanticide by males and its implications. Cambridge University Press, Cambridge, pp 123-152
59. Phoenix CH, Goy RW, Gerrall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369-382
60. Purvis K, Haynes NB (1974) Short-term effects of copulation, human chorionic gonadotrophin injection and non-tactile association with a female on T levels in the male rat. J Endocrinol 60:429-439
61. Reyer HU, Dittami JP, Hall MR (1986) Avian helpers at the nest: are they psychologically castrated? Ethology 71:216-228
62. Ruiz de Elvira MC, Herndon JG, Wilson ME (1982) Influence of estrogen-treated females on sexual behavior and male testosterone levels of a social group of rhesus monkeys during the nonbreeding season. Biol Reprod 26:825-834
63. Sapolsky RM (1982) The endocrine stress-response and social status in the wild baboon. Horm Behav 16:279-292
64. Sapolsky RM (1983) Endocrine aspects of social instability in the olive baboon (Papio anubis). Am J Primatol 5:365-379
65. Sapolsky RM (1993) The physiology of dominance in stable versus unstable social hierarchies. In: Mason WA, Mendoza SP (eds) Primate social conflict. State University of New York Press, Albany, pp 171-204
66. Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR (2005) Testosterone and group size in cliff swallows: testing the "challenge hypothesis" in a colonial bird. Horm Behav 47:76-82
67. Smuts BB (1985) Sex and friendship in baboons. Aldine, New York
68. Soliman AT, Khadir MMA, Asfour M (1995) Testosterone treatment in adolescent boys with constitutional delay of growth and development. Metabolism 44:1013-1015
69. Steklis HD, Brammer GL, Raleigh MJ, McGuire MT (1985) Serum testosterone, male dominance and aggression in captive groups of male vervet monkeys (Cercopithecus aethiops sabaeus). Horm Behav 19:154-163
70. Storey JD (2002) A direct approach to false discovery rates. J R Stat Soc B 64:479-498
71. Storey JD, Tibshirani R (2001) Estimating false discovery rates under dependence, with applications to DNA microarrays. In: Technical Report, vol 2001-28. Department of Statistics, Stanford University
72. Strier KB, Ziegler TE, Wittwer DJ (1999) Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm Behav 35:125-134
73. Taitt MJ, Krebs CJ (1982) Manipulation of female behaviour in field populations of Microtus townsendii. J Anim Ecol 51:681-690
74. Takahashi H (2004) Do males have a better chance of mating when the number of estrous females is equal to or greater than the males' ordinal rank? Testing the hypothesis in Japanese macaques. Am J Primatol 63:95-102
75. Tanriverdi F, Silveira L, MacColl G, Bouloux P (2003) The hypothalamic-pituitary-gonadal axis: immune function and autoimmunity. J Endocrinol 176:293-304
76. Terasawa E, Fernandez DL (2001) Neurobiological mechanisms of the onset of puberty in primates. Endocr Rev 22:111-151
77. Wasser SK, Monfort SL, Southers J, Wildt DE (1994) Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fertil 101:213-220
78. Whitten PL (2000) Evolutionary endocrinology of the cercopithecoids. In: Whitehead PF, Jolly CJ (eds) Old world monkeys. Cambridge University Press, Cambridge, pp 269-297
79. Wickings EJ, Dixson AF (1992) Testicular function, secondary sexual development, and social-status in male mandrills (Mandrillus-Sphinx). Physiol Behav 52:909-916
80. Wikelski M, Lynn S, Breuner C, Wingfield JC, Kenagy GC (1999) Energy metabolism, testosterone and corticosterone in white-crowned sparrows. J Comp Biochem A 185:463-470
81. Wiley CJ, Goldizen AW (2003) Testosterone is correlated with courtship but not aggression in the tropical buff-banded rail, Gallirallus philippensis. Horm Behav 43:554-560
82. Wingfield JC, Farner DS (1993) Endocrinology of reproduction in wild species. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol IX. Academic, New York, pp 163-327
83. Wingfield JC, Hegner RE, Dufty Jr AM, Ball GF (1990) The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829-846
84. Wingfield JC, Jacobs JD, Hillgarth N (1997) Ecological constraints and the evolution of hormone/behavior inter-relationships. Ann NY Acad Sci 807:22-41
85. Wingfield JC, Jacobs JD, Tramontin AD, Perfito N, Meddle S, Maney DL, Soma K (1999) Toward an ecological basis of hormone-behavior interactions in reproduction of birds. In: Wallen K, Schneider J (eds) Reproduction in context. MIT Press, Cambridge, MA, pp 85-128
86. Woodley SK (1994) Plasma androgen levels, spermatogenesis, and secondary sexual characteristics in two species of plethodontid salamanders with dissociated reproductive patterns. Gen Comp Endocrinol 96:206-214
87. Woodroffe R, MacDonald DW, Dasilva J (1995) Dispersal and philopatry in the European badger, Meles meles. J Zool 237:227-239