Primate sexual swellings as coevolved signal systems

Primates

Volumn 41, Issue 1, 2000, Pages 1-16

  Stallmann, Robert R ^a   Froehlich, Jeffery W ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Mate choice; Multiple mating; Sexual conflict; Sexual selection; Sexual swellings

Indexed keywords

COEVOLUTION; COMMUNICATION; FUNCTIONAL ROLE; PRIMATE; SEXUAL BEHAVIOR; SEXUAL SELECTION; SIGNAL;

EID: 0034111350     PISSN: 00328332     EISSN: None     Source Type: Journal    
DOI: 10.1007/BF02557457     Document Type: Article

References (91)

1. ALBERTS, S. C.; SAPOLSKY, R. M.; 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. ALTMANN, J. 1997. Mate choice and intrasexual reproductive competition: contributions to reproduction that go beyond acquiring more mates. In: Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers, GOWATY, P. A. (ed.), Chapman & Hall, New York, pp. 320-333.
3. ANDERSSON, M. 1994. Sexual Selection. Princeton Univ. Press, Princeton.
4. ARNQVIST, G.; ROWE, L. 1995. Sexual conflict and arms races between the sexes: a morphological adaptation for control of mating in a female insect. Proc. R. Soc. Lond. B, 261: 123-127.
5. BASOLO, A. L. 1990. Female preference predates the evolution of the sword in swordtail fish. Science, 250: 808-810.
6. BEACH, F. A. 1976. Sexual attractivity, proceptivity, and receptivity in female mammals. Horm. Behav., 7: 105-138.
7. BIELERT, C.; ANDERSON, C. M. 1985. Baboon sexual swellings and male response: a possible operational supernormal stimulus and response interaction. Int. J. Primatol., 6: 377-393.
8. BIRKHEAD, T. R.; FLETCHER, F.; PELLATT, E. J.; STAPLES, A. 1995. Ejaculate quality and the success of extra-pair copulations in the zebra finch. Nature, 377: 422-423.
9. BIRKHEAD, T. R.; MØLLER, A. P. (eds.), 1998a. Sperm Competition and Sexual Selection. Academic Press, New York.
10. BIRKHEAD, T. R.; MØLLER, A. P. 1998b. Sperm competition, sexual selection and different routes to fitness. In: Sperm Competition and Sexual Selection, BIRKHEAD, T. R.: MØLLER, A. P. (eds.), Academic Press, New York, pp. 757-781.
11. CLARK, A. G.; BEGUN, D. J.; PROUT, T. 1999. Female X male interactions in Drosophila sperm competition. Science, 283: 217-220.
12. CLUTTON-BROCK, T. H.; HARVEY, P. H. 1976. Evolutionary rules and primate societies. In: Growing Points in Ethology, BATESON, P. P. G.; HINDE, R. A. (eds.), Cambridge Univ. Press, Cambridge, pp. 195-237.
13. COWLISHAW, G.; O'CONNELL, S. M. 1996. Male-male competition, paternity certainty and copulation calls in female baboons. Anim. Behav., 51: 235-238.
14. COX, C. R.; LEBOEUF, B. J. 1977. Female incitation of male competition: a mechanism in sexual selection. Amer. Naturalist, 111: 317-335.
15. CUNNINGHAM, E. J. A.; BIRKHEAD, T. R. 1998. Sex roles and sexual selection. Anim. Behav., 56: 1311-1321.
16. CURTSINGER, J. W. 1991. Sperm competition and the evolution of multiple mating. Amer. Naturalist, 138: 93-102.
17. DAHL, J. F. 1986. Cyclic perineal swelling during the intermenstrual intervals of captive female pygmy chimpanzees (Pan paniscus). J. Human Evol., 15: 369 -385
18. DEWSBURY, D. A. 1982. Ejaculate cost and mate choice. Amer. Naturalist, 119 601-610.
19. DIXON, A. F. 1998a. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes, and Human Beings. Oxford Univ. Press, Oxford.
20. DIXSON, A. F. 1998b. Sexual selection and evolution of the seminal vesicles in primates. Folia Primatol., 69: 300-306.
21. BERHARD, W. G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton Univ. Press, Princeton.
22. EERHARD, W. G. 1998. Female roles in sperm competition. In: Sperm Competition and Sexual Selection, BIRKHEAD, T. R.; MØLLER, A. P. (eds.), Academic Press, New York, pp. 91-116.
23. ESTEP, D. Q.; NIEUWENHUIJSEN, K.; BRUCE, K. E. M.; DE NEEF, K. J.; WALTERS, P. A.; BAKER, S. C.; SLOB, A. K. 1988. Inhibition of sexual behaviour among subordinate stumptail macaques. Macaca arc-toides, Anim. Behav., 36: 854-864.
24. FLEAGLE, J. G. 1999. Primate Adaptation and Evolution (2nd ed.). Academic Press, San Diego.
25. GAGNEUX, P.; WOODRUFF, D. S.; BOESCH, C. 1997. Furtive mating in female chimpanzees. Nature, 387: 358-359.
26. GLICK, B. B. 1980. Ontogenetic and psychobiological aspects of the mating activities of male Macaca radiata. In: The Macaques: Studies in Ecology, Behavior and Evolution, LlNDBURG, D. G. (ed.), Van Nostrand Reinhold, New York, pp. 345-369.
27. GOLDFOOT, D. A. 1971. Hormonal and social determinants of sexual behavior in pigtail monkeys (Macaca nemestrina). In: Normal and Abnormal Development of Brain and Behavior, STOELINGA, G. B. A.; VAN DER WERFFTEN BOSCH, J. J. (eds.), Leiden Univ. Press, Leiden, pp. 325-342.
28. GOMENDIO, M.; HARCOURT, A. H.; ROLDAN, E. R. S. 1998. Sperm competition in mammals. In: Sperm Competition and Sexual Selection, BIRKHEAD, T. R.; MØLLER, A. P. (eds.), Academic Press, San Diego, pp. 667-756.
29. GOODALL, J. 1986. The Chimpanzees of Gombe: Patterns of Behavior. Harvard Univ. Press, Cambridge, Massachusetts.
30. GOULD, S. J.; LEWONTIN, R. C. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. Lond. B, 205: 581-598.
31. HAMILTON, W. D.; ZUK, M. 1982. Heritable true fitness and bright birds: a role for parasites? Science, 218: 384-387.
32. HAMILTON, W. J. 1984. Significance of paternal investment by primates to the evolution of male-female associations. In: Primate Paternalism, TAUB, D. M. (ed.), Van Nostrand Reinhold, New York, pp. 309-335.
33. HARCOURT, A. H. 1989. Environment, competition and reproductive performance of female monkeys. Trends Ecol. Evol., 4: 101 - 105.
34. HARCOURT, A. H. 1995. Sexual selection and sperm competition in primates: what are male genitalia good for? Evol. Anthropol., 4: 121 - 129.
35. HARVEY, P. H.; MAY, R. M. 1989. Out for the sperm count. Nature, 337: 508-509.
36. HILL, R. A.; DUNBAR, R. I. M. 1998. An evaluation of the roles of predation rate and predation risk as selective pressures on primate grouping behaviour. Behaviour, 135: 411-430.
37. HIRAIWA-HASEGAWA, M. 1988. Adaptive significance of infanticide in primates. Trends Ecol. Evol., 3: 102-105.
38. HIRAIWA-HASEGAWA, M.; HASEGAWA, T. 1994. Infanticide in nonhuman primates: sexual selection and local resource competition. In: Infanticide and Parental Care, PARMIGIANI, S.; VOM SAAL, F. S. (eds.), Harwood, New York, pp. 137-154.
39. HOOGLAND, J. L. 1998. Why do female Gunnison's prairie dogs copulate with more than one male? Anim. Behav., 55: 351-359.
40. HRDY, S. B. 1979. Infanticide among animals: a review, classification and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol., 1: 13-40.
41. HRDY, S. B. 1981. The Woman That Never Evolved. Harvard Univ. Press, Cambridge, Massachusetts
42. . HRDY, S. B.; WHITTEN, P. L. 1987. Patterns of sexual activity. In: Primate Societies. SMUTS, B. B.; CHENEY, D. L.; SEYFARTH, R. M.; WRANGHAM, R. W.; STRUHSAKFR, T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 370-384.
43. JOHNSTONE, R. A. 1995. Sexual selection, honest advertisement and the handicap principle: reviewing the evidence. Biol. Rev., 70: 1-65.
44. KUESTER, J.; PAUL, A. 1996. Female-female competition and male mate choice in Barbary macaques (Macaca sylvanus). Behaviour, 133: 763-790.
45. MADSEN. T.; SHINE, R.; LOMAN, J.; HÅKANSSON, T. 1992. Why do female adders copulate so frequently? Nature, 355: 440-441.
46. MANSON, J. H. 1992. Measuring female male choice in Cayo Santiago rhesus macaques. Anim. Behav., 44: 405-416.
47. MANSON, J. H. 1994. Male aggression: a cost of female choice in Cayo Santiago rhesus macaques. Anim. Behav., 48: 473-475.
48. MANSON, J. H. 1997. Primate consortships: a critical review. Cur: Anthropol., 38: 353-374.
49. MORI, A.; YAMAGUCHI, N.; WATANABE, K.; SHIMIZU, K. 1997. Sexual maturation of female Japanese macaques under poor nutritional conditions and food-enhanced perineal swelling in the Koshima troop. Int. J. Primatol., 18: 553-579.
50. NUNN, C. L. 1996. Male harassment and the evolution of prominent estrous advertisement in primates. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin.
51. O'CONNELL, S. M.; COWLISHAW, G. 1994. Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons. Anim. Behav., 48: 687-694.
52. OI, T. 1987. Sexual behavior of the wild pig-tailed macaques in west Sumatra: Kyoto Univ. Overseas Res. Rep Studies on Asian Non-human Primates, No. 6. Primate Res. Instit., Kyoto Univ., Inuyama, Japan.
53. OI, T. 1996. Sexual behaviour and mating system of the wild pig-tailed macaque in West Sumatra. In: Evolution and Ecology of Macaque Societies. FA, J. E.; LINDBURG, D. G. (eds.), Cambridge Univ. Press, Cambridge, pp. 342-368.
54. OLSSON, M.; MADSEN, T.; SHINE, R. 1997. Is sperm really so cheap?: costs of reproduction in male adders, Vipera berus. Proc. R. Soc. Lond. B, 264: 455-459.
55. OLSSON, M.; SHINE, R.; MADSEN, T.; GULLBERG, A.; TEGELSTROM, H. 1996. Sperm selection by females. Nature, 383: 585.
56. OWENS, I. P. F.; THOMPSON, D. B. A. 1994. Sex differences, sex ratios and sex roles. Proc. R. Soc. Lond. B, 258: 93-99.
57. PAGEL, M. 1994. The evolution of conspicuous oestrous advertisement in Old World monkeys. Anim. Behav. ,47: 1333-1341.
58. PAUL, A. 1989. Determinants of male mating success in a large group of barbary macaques (Macaca syl-vanus) at Affenberg Salem. Primates, 30: 461-476.
59. PERRIGO, G ; BRYANT, W. C.; VOM SAAL, F. S. 1990. A unique neural timing system prevents male mice from harming their own offspring. Anim. Behav., 39: 535-539.
60. PETRIE, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature, 371: 598-599.
61. PROMISLOW, D. E. L.; SMITH, E. A.; PEARSE, L. 1998. Adult fitness consequences of sexual selection in Drosophila melanogaster. Proc. Natl. Acad. Sci. USA, 95: 10687-10692.
62. PUSEY, A.; WILLIAMS, J.; GOODALL, J. 1997. The influence of dominance rank on the reproductive success of female chimpanzees. Science, 277: 828-831.
63. QVARNSTRÖM, A.; FORSGREN, E. 1998. Should females prefer dominant males? Trends Ecol. Evol., 13: 498-501.
64. REYNOLDS, J. D.; GROSS, M. R. 1992. Female mate preference enhances offspring growth and reproduction in a fish, Poecilia reticulata. Proc. R. Soc. Lond. B, 250: 57-62.
65. ROLDAN, E. R. S.; CASSINELLO, J.; ABAIGAR, T.; GOMENDIO, M. 1998. Inbreeding, fluctuating asymmetry, and ejaculate quality in an endangered ungulate. Proc. R. Soc. Lond. B, 265: 243-248.
66. ROLDAN, E. R. S.; GOMENDIO, M. 1995. Sperm length and sperm competition in primates: a rebuttal of criticism. Folia Primatol., 64: 225-230.
67. RYAN, M. J., WAGNER, W. E. 1987. Asymmetries in mating preferences between species: female swordtails prefer heterospecific males. Science, 236: 595-597.
68. RYAN, M. J.; Fox, J. H.; WILCZYNSKI, W.; RAND, A. S. 1990. Sexual selection for sensory exploitation in the frog Physalaemus pustulosus. Nature, 343: 66 -67.
69. SCHWAGMEYER, P. L.; PARKER, G. A. 1990. Male mate choice as predicted by sperm competition in thirteen-lined ground squirrels. Nature, 348: 62-64.
70. SILLEN-TULLBERG, B.; MØLLER, A. P. 1993. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. Amer. Naturalist, 141:1-25.
71. SMALL, M. F. 1989. Female choice in nonhuman primates. Yrbk. Phys. Anthropol., 32: 103-127.
72. SMUTS, B. B. 1985. Sex and Friendship in Baboons. Aldine, Chicago.
73. SMUTS, B. B. 1987a. Sexual competition and mate choice. In: Primate Societies, SMUTS, B. B.; CHENEY, D. L.; SEYFARTH, R. M.; WRANGHAM, R. W.; STRUHSAKER, T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 385-399.
74. SMUTS, B. B. 1987b. Gender, aggression, and influence. In: Primate Societies, SMUTS, B. B.; CHENEY, D. L.; SEYFARTH, R. M; WRANGHAM, R. W.; STRUHSAKER, T. T. (eds.), Univ. of Chicago Press, Chicago, pp. 400-412.
75. THIERRY, B.; AUJARD, F.; HODGES, J. K. 1996a. Correlations between behavioral, hormonal and morphological variations in the menstrual cycle of female Tonkean macaques. Paper presented at the International Primatological Society, American Society of Primatologists Joint Congress, Madison, Wisconsin.
76. THIERRY, B.; HEISTERMANN, M.; AUJARD, F.; HODGES, J. K. 1996b. Long-term data on basic reproductive parameters and evaluation of endocrine, morphological, and behavioral measures for monitoring reproductive status in a group of semifree-ranging Tonkean macaques (Macaca tonkeana). Amer. J. Primatol., 39: 47-62.
77. VAN SCHAIK, C. P. 1983. Why are diurnal primates living in groups? Behaviour, 87: 120-144.
78. VAN VOORHIES, W. A. 1992. Production of sperm reduces nematode lifespan. Nature, 360: 456-458.
79. WATSON, P. J. 1990. Female-enhanced male competition determines the first mate and principle sire in the spider Linyphia litigiosa (Lyniphiidae). Behav. Ecol. Sociobiol., 26: 77-90.
80. WATSON, P. J. 1998. Multi-male mating and female choice increases offspring growth in the spider Neriene litigiosa (Linyphiidae). Anim. Behav., 55: 387-403.
81. WHITTEN, P. L.; RUSSELL, E. 1996. Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys). Amer. J. Primatol., 40: 67-82.
82. WICKLER, W. 1967. Socio-sexual signals and their intra-specific imitation among primates. In: Primate Ethology, MORRIS, D. (ed.), Doubleday, New York, pp. 89-189.
83. WILDT, D. E.; DOYLE, L. L.; STONE, S. C.; HARRISON, R. M. 1977. Correlation of perineal swelling with serum ovarian hormone levels, vaginal cytology, and ovarian follicular development during the baboon reproductive cycle. Primates, 18: 261-270.
84. WILSON, N.; TUBMAN, S. C.; EADY, P. E.; ROBERTSON, G. W. 1997. Female genotype affects male success in sperm competition. Proc. R. Soc. Lond. B, 264: 1491-1495.
85. WOODROFFE, R.; VINCENT, A. 1994. Mother's little helpers: patterns of male care in mammals. Trends Ecol. Evol., 9: 294-297.
86. WRANGHAM, R. W. 1993. The evolution of sexuality in chimpanzees and bonobos. Human Nature, 4: 47-79.
87. YASUI, Y. 1997. A "good-sperm" model can explain the evolution of costly multiple matings by females. Amer. Naturalist, 149: 573-584.
88. ZAHAVI, A. 1975. Mate selection: a selection for a handicap. J. Theor. Biol., 53: 205-214.
89. ZEH, J. A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscor-pion. Behav. Ecol. Sociobiol., 40: 111-118.
90. ZUMPE, D.; MICHAEL, R. P. 1987. Relation between the dominance rank of female rhesus monkeys and their access to males. Amer. J. Primatol., 13: 155-169.
91. ZUMPE, D.; MICHAEL, R. P. 1989. Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta). Amer. J. Primatol., 17: 287 -304.