Sex and seasonal differences in aggression and steroid secretion in Lemur catta: Are socially dominant females hormonally 'masculinized'?

Hormones and Behavior

Volumn 51, Issue 4, 2007, Pages 555-567

  Drea, Christine M ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Aggression; Androstenedione; Estradiol; Female dominance; Lemur; Masculinization; Seasonality; Spotted hyena; Testosterone

Indexed keywords

ANDROGEN; ANDROSTENEDIONE; ESTRADIOL; STEROID; TESTOSTERONE;

AGGRESSION; ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ESTRADIOL BLOOD LEVEL; FEMALE; GENETIC TRAIT; INHERITANCE; MALE; MASCULINITY; NONHUMAN; PRIORITY JOURNAL; PROSIMIAN; SEASONAL VARIATION; SEX DIFFERENCE; SOCIAL DOMINANCE; SOCIAL INTERACTION; STEROID RELEASE; TESTOSTERONE BLOOD LEVEL;

AGGRESSION; ANALYSIS OF VARIANCE; ANDROSTENEDIONE; ANIMALS; ESTRADIOL; FEMALE; HIERARCHY, SOCIAL; LEMUR; MALE; MENSTRUAL CYCLE; SEASONS; SEX CHARACTERISTICS; SOCIAL DOMINANCE; TESTOSTERONE;

EID: 34147111255     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2007.02.006     Document Type: Article

References (96)

1. Albert D.J., Jonik R.H., and Walsh M.L. Hormone-dependent aggression in male and female rats: experimental, hormonal, and neural foundations. Neurosci. Biobehav. Rev. 16 (1992) 177-192
2. Aujard F. Effect of vomeronasal organ removal on male socio-sexual responses to female in a prosimian primate (Microcebus murinus). Physiol. Behav. 62 (1997) 1003-1008
3. Aujard F., and Perret M. Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus. Physiol. Behav. 64 (1998) 513-519
4. Baker, M.G., 1990. Effects of ovariectomy on dyadic aggression and submission in a colony of peripubertal spotted hyaenas (Crocuta crocuta). M.A. thesis, University of California, Berkeley.
5. Beatty W.W. Gonadal hormones and sex differences in non-reproductive behaviors in rodents: organizational and activational influences. Horm. Behav. 12 (1979) 112-163
6. Billiar R.B., Richardson D., Anderson E., Mahajan D., and Little B. The effect of chronic and acyclic elevation of circulating androstenedione or estrone concentrations on ovarian function in the rhesus monkey. Endocrinology 116 (1985) 2209-2220
7. Bogart M.H., Kumamoto A.T., and Lasley B.L. A comparison of the reproductive cycle of three species of Lemur. Folia Primatol. 28 (1977) 134-143
8. Brockman D.K., Whitten P.L., Richard A.F., and Schneider A. Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. Am. J. Phys. Anthropol. 105 (1998) 137-151
9. Brockman D.K., Whitten P.L., Richard A.F., and Benander B. Birth season testosterone levels in male Verreaux's sifaka, Propithecus verreauxi: insights into socio-demographic factors mediating seasonal testicular function. Behav. Ecol. Sociobiol. 49 (2001) 117-127
10. Cashdan E. Hormones and competitive aggression in women. Aggress. Behav. 29 (2003) 107-115
11. Cavigelli S.A., and Pereira M.E. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37 (2000) 246-255
12. Concannon P.W., and Castracane V.D. Serum androstenedione and testosterone concentrations during pregnancy and nonpregnant cycles in dogs. Biol. Reprod. 33 (1985) 1078-1083
13. Davison S.L., and Bell R. Androgen physiology. Semin. Reprod. Med. 24 (2006) 71-77
14. Dloniak S.M., French J.A., Place N.J., Weldele M.L., Glickman S.E., and Holekamp K.E. Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta). Gen. Comp. Endocrinol. 135 (2004) 51-61
15. Dloniak S.M., French J.A., and Holekamp K.E. Rank-related effects of androgens on behaviour in wild spotted hyenas. Nature 440 (2006) 1190-1193
16. Drea C.M., and Frank L.G. The social complexity of spotted hyenas. In: de Waal F.B.M., and Tyack P.L. (Eds). Animal Social Complexity: Intelligence, Culture, and Individualized Societies (2003), Harvard Univ. Press, Cambridge, MA 121-148
17. Drea C.M., and Wallen K. Female sexuality and the myth of male control. In: Travis C.B. (Ed). Evolution, Gender, and Rape (2003), MIT Press, Cambridge, MA 29-60
18. Drea, C.M., Scordato, E.S. in press. Olfactory communication in the ringtailed lemur (Lemur catta): form and function of multimodal signals. In: Beynon, R., Hurst, J., Roberts, C., Wyatt T. (Eds.), Chemical Signals in Vertebrates 11. Springer Press, New York.
19. Drea, C.M., Weil, A., submitted for publication. External genital morphology of the ringtailed lemur (Lemur catta): are females 'masculinized'?
20. Drea C.M., Weldele M.L., Forger N.G., Coscia E.M., Frank L.G., Licht P., and Glickman S.E. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti-androgens. J. Reprod. Fertil. 113 (1998) 117-127
21. Drea C.M., Coscia E.M., and Glickman S.E. Hyenas. In: Knobil E., Neill J., and Licht P. (Eds). Encyclopedia of Reproduction vol. 2 (1999), Academic Press, San Diego 718-725
22. Drea C.M., Place N.J., Weldele M.L., Coscia E.M., Licht P., and Glickman S.E. Exposure to naturally circulating androgens in fetal life is prerequisite for male mating but incurs direct reproductive costs in female spotted hyaenas. Proc. R. Soc. Lond., B 269 (2002) 1981-1987
23. East M.L., Hofer H., and Wickler W. The erect 'penis' is a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behav. Ecol. Sociobiol. 33 (1993) 355-370
24. Evans C.S., and Goy R.W. Social behaviour and reproductive cycles in captive ring-tailed lemurs (Lemur catta). J. Zool. 156 (1968) 181-197
25. Feder H.H. Peripheral plasma levels of gonadal steroids in adult male and adult, nonpregnant female mammals. In: Adler N., Pfaff D., and Goy R.W. (Eds). Handbook of Behavioral Neurobiology. Reproduction vol. 7 (1985), Plenum Press, New York 299-370
26. Frank L.G. Social organization of the spotted hyaena Crocuta crocuta. II. Dominance and reproduction. Anim. Behav. 34 (1986) 1510-1527
27. Frank L.G., Davidson J.M., and Smith E.R. Androgen levels in the spotted hyaena Crocuta crocuta: the influence of social factors. J. Zool. 206 (1985) 525-531
28. Frank L.G., Glickman S.E., and Powch I. Sexual dimorphism in the spotted hyaena (Crocuta crocuta). J. Zool. 221 (1990) 308-313
29. Glickman S.E., Frank L.G., Davidson J.M., Smith E., and Siiteri P.K. Androstenedione may organize or activate sex-reversed traits in female spotted hyaenas. Proc. Natl. Acad. Sci. U. S. A. 84 (1987) 3444-3447
30. Glickman S.E., Frank L.G., Pavgi S., and Licht P. Hormonal correlates of 'masculinization' in female spotted hyaenas (Crocuta crocuta): I. Infancy through sexual maturity. J. Reprod. Fertil. 95 (1992) 451-462
31. Glickman S.E., Coscia E.M., Frank L.G., Licht P., Weldele M.L., and Drea C.M. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 3. Effects of juvenile gonadectomy. J. Reprod. Fertil. 113 (1998) 129-135
32. Glickman S.E., Cunha J.R., Drea C.M., Conley A.J., and Place N.J. Mammalian sexual differentiation: lessons from the spotted hyena. Trends Endocrinol. Metab. 17 (2006) 349-356
33. Goss, R.A. 1986. The influence of food source on the behavioural ecology of brown hyaenas Hyaena brunnea in the Namib desert. M.Sc. University of Pretoria, South Africa.
34. Goy R.W., and McEwen B.S. Sexual Differentiation of the Brain (1980), MIT Press, Cambridge, MA
35. Goy R.W., and Robinson J.A. Prenatal exposure of rhesus monkeys to patent androgens: morphological, behavioral, and physiological consequences. In: Hunt V.R., Smith M.K., and Worth D. (Eds). Environmental Factors in Human Growth and Development. Banbury Report 11 (1982), Cold Spring Harbor Laboratory, Plainview, NY 355-378
36. Goymann W., East M.L., and Hofer H. Androgens and the role of female "hyperaggressiveness" in spotted hyenas (Crocuta crocuta). Horm. Behav. 39 (2001) 83-92
37. Hill W.C.O. Primates: Comparative Anatomy and Taxonomy. I-Strepsirhini (1953), The Edinburgh Univ. Press, London
38. Hrdy S.B. The Woman That Never Evolved (1981), Harvard Univ. Press, Cambridge
39. Inoff-Germain G., Arnold G., Nottelmann E., Susman E., Cutler Jr. G., and Chrousos G. Relations between hormone levels and observational measures of aggressive behavior of young adolescents in family interactions. Dev. Psychol. 24 (1988) 129-139
40. Ioannou J.M. Female reproductive organs. In: Hafez E.S.E. (Ed). Comparative Reproduction of Nonhuman Primates (1971), Charles C. Thomas Publisher, Springfield, IL 131-159
41. Izard M.K. Social influences on prosimian endocrinology. In: Ziegler T.E., and Bercovitch F.B. (Eds). Socioendocrinology of Primate Reproduction (1990), Wiley-Liss, New York 159-186
42. Jolly A. Lemur Behavior (1966), University of Chicago Press, Chicago
43. Jolly A. The puzzle of female feeding priority. In: Small M.F. (Ed). Female Primates: Studies by Women Primatologists (1984), Liss, New York 197-215
44. Jost A. Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Prog. Horm. Res. 8 (1953) 379-418
45. Kappeler P.M. Female dominance in Lemur catta: more than just female feeding priority. Folia Primatol. 55 (1990) 92-95
46. Kappeler P.M. The evolution of sexual size dimorphism in prosimian primates. Am. J. Primatol. 21 (1990) 201-214
47. Kruuk H. The Spotted Hyena: A Study of Predation and Social Behavior (1972), The University of Chicago Press, Chicago
48. Leigh S.R., and Terranova C.J. Comparative perspectives on bimaturism, ontogeny, and dimorphism in lemurid primates. Int. J. Primatol. 19 (1998) 723-749
49. Licht P., Frank L.G., Pavgi S., Yalcinkaya T., Siiteri P.K., and Glickman S.E. Hormonal correlates of "masculinization" in female spotted hyaenas (Crocuta crocuta). II. Maternal and fetal steroids. J. Reprod. Fertil. 95 (1992) 463-474
50. Licht P., Hayes T., Tsai P., Cunha G., Kim H., Golbus M., Hayward S., Martin M., Jaffe R.B., and Glickman S.E. Androgens and masculinization of genitalia in the spotted hyena (Crocuta crocuta). 1. Urogenital morphology and placental androgen production during fetal life. J. Reprod. Fertil. 113 (1998) 105-116
51. Lindeque M., Skinner J.D., and Millar R.P. Adrenal and gonadal contribution to circulating androgens in spotted hyaenas (Crocuta crocuta) as revealed by LHRH, hCG and ACTH stimulation. J. Reprod. Fertil. 78 (1986) 211-217
52. Lonstein J.S., and Gammie S.C. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci. Biobehav. Rev. 26 (2002) 869-888
53. Lovejoy J., and Wallen K. Adrenal suppression and sexual initiation in group-living female rhesus monkeys. Horm. Behav. 24 (1990) 256-269
54. MacLusky N.J., and Naftolin F. Sexual differentiation of the central nervous system. Science 211 (1981) 1294-1303
55. Matthews L.H. Reproduction in the spotted hyaena, Crocuta crocuta (Erxleben). Philos. Trans. R. Soc. Lond., B Biol. Sci. 230 (1939) 1-78
56. Mills M.G.L. Kalahari Hyenas: Comparative Behavioural Ecology of Two Species (1990), Unwin Hyman, London
57. Monaghan E.P., and Glickman S.E. Hormones and aggressive behavior. In: Becker J.B., Breedlove S.M., and Crews D. (Eds). Behavioral Endocrinology (1992), MIT Press, Cambridge, MA 261-285
58. Neaves W.B., Griffin J.E., and Wilson J.D. Sexual dimorphism of the phallus in spotted hyaena (Crocuta crocuta). J. Reprod. Fertil. 59 (1980) 509-513
59. Ostner J., Kappeler P.M., and Heistermann M. Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus). Behav. Ecol. Sociobiol. 52 (2002) 485-495
60. Owens M.J., and Owens D.D. Feeding ecology and its influence on social organization in brown hyenas (Hyaena brunnea, Thunberg) of the central Kalahari Desert. East Afr. Wildl. J. 16 (1978) 113-135
61. Owens D.D., and Owens M.J. Social dominance and reproductive patterns in brown hyaenas, Hyaena brunnea, of the central Kalahari desert. Anim. Behav. 51 (1996) 535-551
62. Pazol K., Kaplan J.R., Abbott D.H., Appt S.E., and Wilson M.E. Practical measurement of total and bioavailable estradiol in female macaques. Clin. Chim. Acta 340 (2004) 117-126
63. Pereira M.E. Asynchrony within estrous synchrony among ringtailed lemurs (Primates: Lemuridae). Physiol. Behav. 49 (1991) 47-52
64. Pereira M.E., and Weiss M.L. Female mate choice, male migrations, and the threat of infanticide in ringtailed lemurs. Behav. Ecol. Sociobiol. 28 (1991) 141-152
65. Pereira M.E., Kaufman R., Kappeler P.M., and Overdorff D.J. Female dominance does not characterize all of the Lemuridae. Folia Primatol. 55 (1990) 96-103
66. Perret M. Environmental and social determinants of sexual function in the male lesser mouse lemur (Microcebus murinus). Folia Primatol. 59 (1992) 1-25
67. Petter-Rousseaux A. Reproductive physiology and behavior of the Lemuroidea. In: Buettner-Janusch J. (Ed). Evolutionary and Genetic Biology of Primates vol. 2 (1964), Academic Press, New York 91-132
68. Place N.J., and Glickman S.E. Masculinization of female mammals: lessons from nature. Adv. Exp. Med. Biol. 545 (2004) 243-253
69. Racey P.A., and Skinner J.D. Endocrine aspects of sexual mimicry in spotted hyaenas Crocuta crocuta. J. Zool. 187 (1979) 315-326
70. Ralls K. Mammals in which females are larger than males. Q. Rev. Biol. 51 (1976) 245-276
71. Richard A.F. Malagasy prosimians: female dominance. In: Smuts B.B., Cheney D.L., Seyfarth R.M., Wrangham R.W., and Struhsaker T.T. (Eds). Primate Societies (1987), University of Chicago Press, Chicago 25-33
72. Richard A.F., and Nicoll M.E. Female social dominance and basal metabolism in a Malagasy primate, Propithecus verreauxi. Am. J. Primatol. 12 (1987) 309-314
73. Rubenstein D.R., and Wikelski M. Steroid hormones and aggression in female Galápagos marine iguanas. Horm. Behav. 48 (2005) 329-341
74. Sauther M.L. Reproductive behavior of free-ranging Lemur catta at Beza Mahafaly Special Reserve, Madagascar. Am. J. Phys. Anthropol. 84 (1991) 463-477
75. Sauther M.L. Resource competition in wild populations of ringtailed lemurs (Lemur catta): implications for female dominance. In: Kappeler P.M., and Ganzhorn J.U. (Eds). Lemur Social Systems and Their Ecological Basis (1993), Plenum Press, New York
76. Schilling A., and Perret M. Removal of the olfactory bulbs modifies the gonadal responses to photoperiod in the lesser mouse lemur (Microcebus murinus). Biol. Reprod. 49 (1993) 58-65
77. Schilling A., Perret M., and Predine J. Sexual inhibition in a prosimian primate: a pheromone-like effect. J. Endocrinol. 102 (1984) 143-151
78. Sherwin B.B. A comparative analysis of the role of androgen in human male and female sexual behavior: Behavioral specificity, critical thresholds, and sensitivity. Psychobiology 16 (1988) 416-425
79. Simon N.G., and Whalen R.E. Sexual differentiation of androgen-sensitive and estrogen-sensitive regulatory systems for aggressive behavior. Horm. Behav. 21 (1987) 493-500
80. Smale L., Frank L.G., and Holekamp K.E. Ontogeny of dominance in free-living spotted hyaenas, juvenile rank relations with adult females and immigrant males. Anim. Behav. 46 (1993) 467-477
81. Sokal R.R., and Rohlf F.J. Biometry: The Principles and Practice of Statistics in Biological Research. 2nd Ed. (1981), W.H. Freeman and Company, New York
82. Staub N.L., and De Beer M. The role of androgens in female vertebrates. Gen. Comp. Endocrinol. 108 (1997) 1-24
83. Sussman R.W. Demography and social organization of free-ranging Lemur catta in the Beza Mahafaly Reserve, Madagascar. Am. J. Phys. Anthropol. 84 (1991) 43-58
84. Tilden C., and Oftedal O. The bioenergetics of reproduction in prosimian primates: is it related to female dominance?. In: Altermann L., Doyle G.A., and Izard M.K. (Eds). Creatures of the Dark (1995), Plenum Press, New York 119-131
85. Van de Poll N.E., Van Zanten S., and De Jonge F.H. Effects of testosterone, estrogen, and dihydrotestosterone upon aggressive and sexual behavior of female rats. Horm. Behav. 20 (1986) 418-431
86. Van Horn R.N. Primate breeding season: photoperiodic regulation in captive Lemur catta. Folia Primatol. 24 (1975) 203-220
87. Van Horn R.N., and Resko J.A. The reproductive cycle of the ringtailed lemur (Lemur catta): sex steroid levels and sexual receptivity under controlled photoperiods. Endocrinology 101 (1977) 1579-1586
88. Van Horn R.N., Beamer N.B., and Dixson A.F. Diurnal variations of plasma testosterone in two prosimian primates (Galago crassicaudatus and Lemur catta). Biol. Reprod. 15 (1976) 523-528
89. Vick L.G., and Pereira M.E. Episodic targeting aggression and the histories of Lemur social groups. Behav. Ecol. Sociobiol. 25 (1989) 3-12
90. Von Engelhardt N., Kappeler P.M., and Heistermann M. Androgen levels and female social dominance in Lemur catta. Proc. R. Soc. Lond., B 267 (2000) 1533-1539
91. Wichmann U., Wichmann G., and Krause W. Serum levels of testosterone precursors, testosterone and estradiol in 10 animal species. Exp. Clin. Endocrinol. 83 (1984) 283-290
92. Wingfield J.C., Hegner R.E., Dufty Jr. A.M., and Ball G.F. The "challenge hypothesis": Theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136 (1990) 829-846
93. Woodley S.K., and Moore M.C. Female territorial aggression and steroid hormones in mountain spiny lizards. Anim. Behav. 57 (1999) 1083-1089
94. Yalcinkaya T.M., Siiteri P.K., Vigne J.-L., Licht P., Pavgi S., Frank L.G., and Glickman S.E. A mechanism for virilization of female spotted hyenas in utero. Science 260 (1993) 1929-1931
95. Yost R.A. The nocturnal behavior of captive brown hyaenas (Hyaena brunnea). Mammalia 44 (1980) 27-34
96. Young A.L., Richard A.F., and Aiello L.C. Female dominance and maternal investment in strepsirhine primates. Am. Nat. 135 (1990) 473-488