Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-8448b6f56d-m8qmq Total loading time: 0 Render date: 2024-04-24T17:40:46.878Z Has data issue: false hasContentIssue false

5 - Sexual selection and exaggerated sexual swellings of female primates

Published online by Cambridge University Press:  10 August 2009

By
Dietmar P. Zinner ,
Charles L. Nunn ,
Carel P. van Schaik  and
Peter M. Kappeler
Edited by
Peter M. Kappeler  and
Carel P. van Schaik
Dietmar P. Zinner
Affiliation:
Department of Behaviour and Ecology, German Primate Centre, Göttingen, Germany
Charles L. Nunn
Affiliation:
Department of Biology, University of California, Davis, CA, USA
Carel P. van Schaik
Affiliation:
Department of Biological Anthropology and Anatomy, Duke University, Durham, NC, USA
Peter M. Kappeler
Affiliation:
Department of Behaviour and Ecology, German Primate Centre, Göttingen, Germany
Peter M. Kappeler
Affiliation:
Deutsches Primatenzentrum, Göttingen, Germany
Carel P. van Schaik
Affiliation:
Duke University, North Carolina
Get access

Summary

INTRODUCTION

Females of several species of Old World monkeys and apes exhibit enlarged perineal swellings that include the skin of the anogenital region and rump (see Fig. 5.1). Swellings are normally produced by adult females undergoing ovarian activity and they have stimulated evolutionary biologists since Darwin (1876) to think about their adaptive value and the evolutionary mechanisms responsible for their origin and maintenance. Given the association between sexual swellings and mating activity, it seems likely that some aspect of sexual selection is responsible for the evolution of this exaggerated trait. However, even today the functional significance of exaggerated swellings, as well as the processes responsible for their evolution, remain controversial (Dixson, 1983, 1998; Pagel, 1994, 1995; Radwan, 1995; Wiley & Poston, 1996; Nunn, 1999a; Stallmann & Froehlich, 2000; Domb & Pagel, 2001; Nunn et al., 2001; Domb & Pagel, 2002; Zinner et al., 2002; Snowdon, this volume).

In this chapter, we explore the role of sexual selection in the evolution of exaggerated sexual swellings. Because sexual swellings are associated with mating behaviour and competition among males for access to females, sexual selection has figured prominently among hypotheses for this exaggerated trait. Hypotheses have incorporated the two primary components of sexual selection, sometimes within the same explanation. For example, the best-male hypothesis (Clutton-Brock & Harvey, 1976) states that swellings stimulate male–male competition, improving the ability of females to identify and mate with the highest-quality males.

In recent years, our understanding of the theoretical basis for sexual selection has increased.

Type
Chapter
Information
Sexual Selection in Primates
New and Comparative Perspectives
 , pp. 71 - 89
Publisher: Cambridge University Press
Print publication year: 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aidara, D., Badawi, M., Tahiri-Zagret, C. & Robyn, C. 1981. Changes in concentrations of serum prolactin, FSH, oestradiol and progesterone and of the sex skin during the menstrual cycle in the mangabey monkeys (Cercocebus atys lunulatus). Journal of Reproduction and Fertility, 62, 475–81CrossRefGoogle Scholar
Alberts, S. C., Altmann, J. & Wilson, M. L. 1996. Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269–77CrossRefGoogle Scholar
Amundsen, T., Forsgren, E. & Hansen, L. T. T. 1997. On the function of female ornaments: male bluethroats prefer colourful females. Proceedings of the Royal Society London, Series B, 264, 1579–86CrossRefGoogle Scholar
Anderson, C. M. 1986. Female age: male preferences and reproductive success in primates. International Journal of Primatology, 7, 305–26CrossRefGoogle Scholar
Anderson, C. M. & Bielert, C. F. 1994. Adolescent exaggeration in female catarrhine primates. Primates, 35, 283–300CrossRefGoogle Scholar
Andersson, M. 1982. Female choice selects for extreme tail-length in a widowbird. Nature, 229, 818–20CrossRefGoogle Scholar
Andersson, M. 1994. Sexual Selection. Princeton, NJ: Princeton University Press
Andersson, M. & Iwasa, Y. 1996. Sexual selection. Trends in Ecology and Evolution, 11, 53–9CrossRefGoogle ScholarPubMed
Arnqvist, G. & Rowe, L. 1995. Sexual conflict and arms races between the sexes – a morphological adaptation for control of mating in female insects. Proceedings of the Royal Society London, Series B, 261, 123–7CrossRefGoogle Scholar
Aykroyd, O. E. & Zuckermann, S. 1938. Factors in sexual-skin oedema. The Journal of Physiology, London, 94, 13–25CrossRefGoogle ScholarPubMed
Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity, 2, 349–68CrossRefGoogle ScholarPubMed
Bercovitch, F. B. 1995. Female cooperation, consortship maintenance, and male mating success in savanna baboons. Animal Behaviour, 50, 137–49CrossRefGoogle Scholar
Bernhardt, C. 1993. Änderungen im Verhalten adulter Mantelpavianweibchen (Papio hamadryas hamadryas) in Abhängigkeit vom Östruszustand. Diploma thesis, University of Erlangen–Nürnberg
Bielert, C. & Anderson, C. M. 1985. Baboon sexual swellings and male response: a possible operational mammalian supernormal stimulus and response interaction. International Journal of Primatology, 6, 377–93CrossRefGoogle Scholar
Bielert, C. & Busse, C. 1983. Influences of ovarian hormones on the food intake and feeding of captive and wild female chacma baboons (Papio ursinus). Physiology and Behavior, 30, 103–11CrossRefGoogle Scholar
Bielert, C. & Girolami, L. 1986. Experimental assessments of behavioral and anatomical components of female chacma baboon (Papio ursinus) sexual attractiveness. Psychoneuroendocrinology, 11, 75–90CrossRefGoogle ScholarPubMed
Bielert, C. & Walt, L. A. 1982. Male chacma baboon (Papio ursinus) sexual arousal: mediation by visual cues from female conspecifics. Psychoneuroendocrinology, 7, 31–48CrossRefGoogle ScholarPubMed
Bielert, C., Czaja, J. A., Eisele, S.et al. 1976. Mating in the rhesus monkey (Macaca mulatta) after conception and its relationship to oestradiol and progesterone levels throughout pregnancy. Journal of Reproduction and Fertility, 46, 179–87CrossRefGoogle ScholarPubMed
Bielert, C., Girolami, L. & Jowell, S. 1989. An experimental examination of the colour component in visually mediated sexual arousal of the male chacma baboon (Papio ursinus). Journal of Zoology, London, 219, 569–79CrossRefGoogle Scholar
Clutton-Brock, T. H. & Harvey, P. H. 1976. Evolutionary rules and primate societies. In Growing Points in Ethology, ed. P. Bateson & R. Hinde. Cambridge: Cambridge University Press, pp. 195–237
Clutton-Brock, T. H. & Harvey, P. H. 1977. Primate ecology and social organisation. Journal of Zoology, London, 183, 1–39CrossRefGoogle Scholar
Clutton-Brock, T. H. & Parker, G. A. 1992. Potential reproductive rates and the operation of sexual selection. The Quarterly Review of Biology, 67, 437–56CrossRefGoogle Scholar
Clutton-Brock, T. H. & Parker, G. A. 1995. Sexual coercion in animal societies. Animal Behaviour, 49, 1345–65CrossRefGoogle Scholar
Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. 1977. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature, 269, 797–800CrossRefGoogle ScholarPubMed
Colmenares, F. & Gomendio, M. 1988. Changes in female reproductive condition following male take-overs in a colony of hamadryas and hybrid baboons. Folia Primatologica, 50, 157–74CrossRefGoogle Scholar
Converse, L. J., Carlson, A. A., Ziegler, T. E. & Snowdon, C. T. 1995. Communication of ovulatory state to mates by female pygmy marmosets, Cebuella pygmaea. Animal Behaviour, 49, 615–21CrossRefGoogle Scholar
Cords, M. 2000. The number of males in guenon groups. In Primate Males: Causes and Consequences of Variation in Group Composition, ed. P. M. Kappeler. Cambridge: Cambridge University Press, pp. 84–96
Cox, C. R. & LeBoeuf, B. J. 1977. Female incitation of male competition: a mechanism in sexual selection. The American Naturalist, 111, 317–35CrossRefGoogle Scholar
Dahl, J. F. 1986. Cyclic perineal swelling during the intermenstrual intervals of captive female pygmy chimpanzees (Pan paniscus). Journal of Human Evolution, 15, 369–85CrossRefGoogle Scholar
Darwin, C. 1871. The Descent of Man, and Selection in Relation to Sex. London: John Murray
Darwin, C. 1876. Sexual selection in relation to monkeys. Nature, 15, 18–19CrossRefGoogle Scholar
Davies, N. B., Hartly, I. R., Hatchwell, B. J. & Langmore, N. E. 1996. Female control of copulations to maximise male help: a comparison of polygynandrous alpine accentors, Prunella collaris, and dunnocks, P. modularis. Animal Behaviour, 51, 27–47CrossRefGoogle Scholar
Deschner, T., Heistermann, M., Hodges, J. K. & Boesch, C. 2003. Timing and probability of ovulation in relation to sex skin swelling in wild West African chimpanzees, Pan troglodytes verus. Animal Behaviour, in press
de Waal, F. B. M. 1982. Chimpanzee Politics. New York, NY: Harper & Row
Dixson, A. F. 1977. Observations on the displays, menstrual cycles and sexual behaviour in the ‘black ape’ of Celebes (Macaca nigra). Journal of Zoology, London, 182, 63–84CrossRefGoogle Scholar
Dixson, A. F. 1983. Observations on the evolution and behavioral significance of ‘sexual skin’ in female primates. Advances in the Study of Behavior, 13, 63–106CrossRefGoogle Scholar
Dixson, A. F. 1998. Primate Sexuality: Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings. Oxford: Oxford University Press
Dixson, A. F. & Herbert, J. 1977. Gonadal hormones and sexual behavior in groups of adult talapoin monkeys (Miopithecus talapoin). Hormones and Behavior, 8, 141–54CrossRefGoogle Scholar
Dixson, A. F. & Mundy, N. I. 1994. Sexual behavior, sexual swelling and penile evolution in chimpanzees (Pan troglodytes). Archives of Sexual Behavior, 23, 267–80CrossRefGoogle Scholar
Dixson, A. F., Everitt, B. J., Herbert, J., Rugma, S. M. & Scruton, D. M. 1973. Hormonal and other determinants of sexual attractiveness and receptivity in rhesus and talapoin monkeys. In Primate Reproductive Behavior, ed. C. H. Phoenix. Basel: Karger, pp. 36–63
Domb, L. G. 2000. Sexual swellings in wild baboons (Papio cynocephalus anubis) at Gombe National Park, Tanzania. Ph.D. thesis, Harvard University, Cambridge, MA
Domb, L. G. & Pagel, M. 2001. Sexual swellings advertise female quality in wild baboons. Nature, 410, 204–6CrossRefGoogle ScholarPubMed
Domb, L. G. & Pagel, M. 2002. Significance of primate sexual swellings. Reply to Zinner et al.Nature, 420, 143CrossRefGoogle Scholar
Eberhard, W. G. 1996. Female Control: Sexual Selection by Cryptic Female Choice. Princeton, NJ: Princeton University Press
Fa, J. E. & Southwick, C. H. (eds.) 1988. Ecology and Behavior of Food-Enhanced Primate Groups. New York, NY: Alan R. Liss
Fisher, R. A. 1915. The evolution of sexual preference. Eugenics Review, 7, 184–92Google ScholarPubMed
Fisher, R. A. 1930. The Genetical Theory of Natural Selection. Oxford: Clarendon Press
Gillman, J. & Gilbert, C. 1946. The reproductive cycle of the chacma baboon with special reference to the problems of menstrual irregularities as assessed by the behavior of the sex skin. The South African Journal of Medical Sciences, Biological Supplement, 11, 1–54Google ScholarPubMed
Girolami, L. & Bielert, C. 1987. Female perineal swelling and its effects on male sexual arousal: an apparent sexual releaser in the chacma baboon (Papio ursinus). International Journal of Primatology, 8, 651–61CrossRefGoogle Scholar
Glander, K. E. 1980. Reproduction and population growth in free-ranging mantled howling monkeys. American Journal of Physical Anthropology, 53, 25–36CrossRefGoogle ScholarPubMed
Goldfoot, D. A. 1981. Olfaction, sexual behavior, and the pheromone hypothesis in rhesus monkeys: a critique. American Zoologist, 21, 153–64CrossRefGoogle Scholar
Goldfoot, D. A., Kravetz, M. A., Goy, R. W. & Freeman, S. K. 1976. Lack of effect of vaginal lavages and aliphatic acids on ejaculatory responses in rhesus monkeys: behavioral and chemical responses. Hormones and Behavior, 7, 1–27CrossRefGoogle Scholar
Goodall, J. 1986. The Chimpanzees of Gombe. Cambridge, MA: Harvard University Press
Gordon, T. P., Gust, D. A., Busse, C. D. & Wilson, M. E. 1991. Hormones and sexual behavior associated with postconception swelling in the sooty mangabey (Cercocebus torquatus atys). International Journal of Primatology, 12, 585–97CrossRefGoogle Scholar
Gowaty, P. A. 1996. Battles of the sexes and origins of monogamy. In Partnership in Birds, ed. J. M. Black, pp. 21–52. Oxford: Oxford University Press
Gowaty, P. A. 1997. Sexual dialectics, sexual selection, and variation in mating behavior. In Feminism and Evolutionary Biology: Boundaries, Intersections, and Frontiers, ed. P. A. Gowaty, pp. 351–84. New York: Chapman & Hall
Gust, D. A. 1994. Alpha-male sooty mangabeys differentiate between females' fertile and their postconception maximal swellings. International Journal of Primatology, 15, 289–301CrossRefGoogle Scholar
Hamilton, W. D. & Zuk, M. 1982. Heritable true fitness and bright birds: a role for parasites?Science, 218, 384–7CrossRefGoogle Scholar
Hamilton, W. J. 1984. Significance of paternal investment by primates to the evolution of male–female associations. In Primate Paternalism, ed. D. M. Taub. New York, NY: Van Nostrand, pp. 309–35
Harth, I. 1978. Zyklusabhängige Veränderungen der Geschlechtsorgane weiblicher Procolobus badius. Ph.D. thesis, University of Frankfurt
Harvey, P. H. & May, R. M. 1989. Out for the sperm count. Nature, 337, 508–9CrossRefGoogle ScholarPubMed
Hauser, M. 1990. Do chimpanzee copulatory calls incite male–male competition?Animal Behaviour, 39, 596–7CrossRefGoogle Scholar
Hausfater, G. 1975. Dominance and reproduction in baboons: a quantitative analysis. Contributions to Primatology, 7, 1–150. Basel: Karger
Heistermann, M., Möhle, U., Vervaecke, H., Elsacker, L. & Hodges, J. K. 1996. Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns in relation to endocrine events. Biology of Reproduction, 55, 844–53CrossRefGoogle ScholarPubMed
Hendrickx, A. G. & Kraemer, D. C. 1969. Observation of the menstrual cycle, optimal mating time, and pre-implantation embryos of the baboons, Papio anubis and Papio cynocephalus. Journal of Reproduction and Fertility, Supplement, 6, 119–28Google Scholar
Hill, W. C. O. 1952. The external and visceral anatomy of the olive colobus monkey (Procolobus verus). Proceedings of the Zoological Society, London, 122, 127–86CrossRefGoogle Scholar
Holland, B. & Rice, W. R. 1998. Perspective: chase-away sexual selection – antagonistic seduction versus resistance. Evolution, 52, 1–7CrossRefGoogle ScholarPubMed
Hrdy, S. B. 1974. Male–male competition and infanticide among the langurs (Presbytis entellus) of Abu, Radjasthan. Folia Primatologica, 22, 19–58CrossRefGoogle Scholar
Hrdy, S. B. 1981. The Woman that Never Evolved. Cambridge, MA: Harvard University Press
Hrdy, S. B. 1988. The primate origins of human sexuality. In The Evolution of Sex, ed. R. Bellig & G. Stevens. San Francisco, CA: Harper & Row, pp. 101–36
Hrdy, S. B. & Whitten, P. L. 1987. Patterning of sexual activity. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. W. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 370–84
Johnstone, R. A., Reynolds, J. D. & Deutsch, J. C. 1996. Mutual mate choice and sex differences in choosiness. Evolution, 50, 1382–91CrossRefGoogle ScholarPubMed
Jolly, A. 1967. Breeding synchrony in wild Lemur catta. In Social Communication among Primates, ed. S. A. Altman. Chicago, IL: University of Chicago Press, pp. 3–14
Jones, A. G., Rosenqvist, G., Berglund, A., Arnold, S. J. & Avise, J. C. 2000. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proceedings of the Royal Society London, Series B, 267, 677–80CrossRefGoogle Scholar
Kappeler, P. M. 1988. A preliminary study of olfactory behavior of captive Lemur coronatus during the breeding season. International Journal of Primatology, 9, 135–46CrossRefGoogle Scholar
Kappeler, P. M. 1998. To whom it may concern: transmission and function of chemical signals in Lemur catta. Behavioral Ecology and Sociobiology, 42, 411–21CrossRefGoogle Scholar
Kappeler, P. M. 1999. Primate socioecology: new insights from males. Naturwissenschaften, 86, 18–29CrossRefGoogle ScholarPubMed
Keddy-Hector, A. C. 1992. Mate choice in non-human primates. American Zoologist, 32, 62–70CrossRefGoogle Scholar
Keverne, E. B. 1982. Olfaction and the reproductive behaviour of nonhuman primates. In Primate Communication, ed. C. T. Snowdon, C. H. Brown & M. R. Petersen. Cambridge: Cambridge University Press, pp. 396–412
Krohn, P. L. & Zuckermann, S. 1937. Water metabolism in relation to the menstrual cycle. The Journal of Physiology, London, 88, 369–87CrossRefGoogle ScholarPubMed
Kuester, J. & Paul, A. 1984. Female reproductive characteristics in semifree-ranging Barbary macaques (Macaca sylvanus L. 1758). Folia Primatologica, 43, 69–83Google Scholar
Kuhn, H. J. 1972. On the perineal organ of male Procolobus badius. Journal of Human Evolution, 1, 371–8CrossRefGoogle Scholar
Kummer, H. 1968. Social Organization of Hamadryas Baboons. A Field Study. Chicago, IL: University of Chicago Press
Manson, J. H. 1992. Measuring female mate choice in Cayo Santiago rhesus macaques. Animal Behaviour, 44, 405–16CrossRefGoogle Scholar
Manson, J. H. 1995. Female mate choice in primates. Evolutionary Anthropology, 3, 192–5CrossRefGoogle Scholar
Michael, R. P. & Keverne, E. B. 1968. Pheromones and the communication of sexual status in primates. Nature, 218, 746–9CrossRefGoogle ScholarPubMed
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 Koshima troop. International Journal of Primatology, 18, 553–80CrossRefGoogle Scholar
Nadler, R. D., Graham, C. E., Collins, D. C. & Gould, K. G. 1979. Plasma gonadotropins, prolactin, gonadal steroids, and genital swelling during the menstrual cycle of lowland gorillas. Endocrinology, 105, 290–6CrossRefGoogle ScholarPubMed
Nakamura, M. 1998. Multiple mating and cooperative breeding in polygynous alpine accentors. I. Competition among females. Animal Behaviour, 55, 259–75CrossRefGoogle Scholar
Nunn, C. L. 1999a. The evolution of exaggerated sexual swellings in primates and the graded signal hypothesis. Animal Behaviour, 58, 229–46CrossRefGoogle Scholar
Nunn, C. L. 1999b. The number of males in primate social groups: a comparative test of the socioecological model. Behavioral Ecology and Sociobiology, 46, 1–13CrossRefGoogle Scholar
Nunn, C. L. & van Schaik, C. P. 2000. Social evolution in primates: the relative role of ecology and intersexual conflict. In Infanticide by Males and Its Implications, ed. C. P. van Schaik & C. H. Janson. Cambridge: Cambridge University Press, pp. 388–412
Nunn, C. L., Schaik, C. P. & Zinner, D. 2001. Do exaggerated sexual swellings function in female mating competition in primates? A comparative test of the reliable indicator hypothesis. Behavioral Ecology, 5, 646–54CrossRefGoogle Scholar
Connell, S. M. & Cowlishaw, G. 1994. Infanticide avoidance, sperm competition and mate choice: the function of copulation calls in female baboons. Animal Behaviour, 48, 687–94CrossRefGoogle Scholar
Oda, R. & Masataka, N. 1992. Functional significance of female Japanese macaque copulatory calls. Folia Primatologica, 58, 146–9CrossRefGoogle ScholarPubMed
Pagel, M. 1994. The evolution of conspicuous oestrus advertisement in Old World monkeys. Animal Behaviour, 47, 1333–41CrossRefGoogle Scholar
Pagel, M. 1995. Sexual selection and oestrus advertisement: a reply to Radwan. Animal Behaviour, 49, 1401–2CrossRefGoogle Scholar
Palombit, R. A., Seyfarth, R. M. & Cheney, D. L. 1997. The adaptive value of ‘friendships’ to female baboons: experimental and observational evidence. Animal Behaviour, 54, 599–614CrossRefGoogle ScholarPubMed
Parker, G. A. 1979. Sexual selection and sexual conflict. In Sexual Selection and Reproductive Competition in Insects, ed. M. S. Blum & N. A. Blum. New York, NY: Academic Press, pp. 123–66
Paul, A. 2002. Sexual selection and mate choice. International Journal of Primatology, 23, 877–904CrossRefGoogle Scholar
Petrie, M. 1994. Improved growth and survival of offspring of peacocks with more elaborate trains. Nature, 371, 598–9CrossRefGoogle Scholar
Petrie, M., Halliday, T. & Sanders, C. 1991. Peahens prefer peacocks with elaborate trains. Animal Behaviour, 41, 323–31CrossRefGoogle Scholar
Pfeiffer, G., Kaumanns, W. & Schwibbe, M. H. 1985. A female ‘defeated leader’ in hamadryas baboons. A case study. Primate Report, 12, 18–26Google Scholar
Plavcan, J. M. 2001. Sexual dimorphism in primate evolution. Yearbook of Physical Anthropology, 44, 25–53CrossRefGoogle Scholar
Plavcan, J. M. & Schaik, C. P. 1994. Canine dimorphism. Evolutionary Anthropology, 2, 208–14CrossRefGoogle Scholar
Radwan, J. 1995. On oestrus advertisement, spite and sexual harassment. Animal Behaviour, 49, 1399–400CrossRefGoogle Scholar
Reichert, K. E., Heistermann, M., Hodges, J. K., Boesch, C. & Hohmann, G. 2002. What females tell males about their reproductive status: are morphological and behavioural cues reliable signals of ovulation in bonobos (Pan paniscus)?Ethology, 108, 1–18CrossRefGoogle Scholar
Reynolds, J. & Szekely, T. 1997. The evolution of parental care in shorebirds: life histories, ecology and sexual selection. Behavioral Ecology, 8, 126–34CrossRefGoogle Scholar
Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature, 381, 232–4CrossRefGoogle ScholarPubMed
Ridley, M. 1986. The number of males in a primate troop. Animal Behaviour, 34, 1848–58CrossRefGoogle Scholar
Roulin, A., Jungi, T. W., Pfister, H. & Dijkstra, C. 2000. Female barn owls (Tyto alba) advertise good genes. Proceedings of the Royal Society London, Series B, 267, 937–41CrossRefGoogle ScholarPubMed
Rowell, T. E. 1972. Female reproductive cycles of the talapoin monkey (Miopithecus talapoin). Folia Primatologica, 28, 188–202CrossRefGoogle Scholar
Rowell, T. E. & Dixson, A. F. 1975. Changes in social organisation during the breeding season of wild talapoin monkeys. Journal of Reproduction and Fertility, 43, 419–34CrossRefGoogle ScholarPubMed
Ryan, M. J. 1990. Sexual selection, sensory systems and sensory exploitation. Oxford Surveys in Evolutionary Biology, 7, 157–95Google Scholar
Saayman, G. S. 1970. The menstrual cycle and sexual behaviour in a troop of free-ranging chacma baboons (Papio ursinus). Folia Primatologica, 12, 81–110CrossRefGoogle Scholar
Schilling, A. 1979. Olfactory communication in prosimians. In The Study of Prosimian Behavior, ed. G. A. Doyle & R. D. Martin. New York, NY: Academic Press, pp. 461–542
Semple, S., McComb, K., Alberts, S. C. & Altmann, J. 2002. Information content of female copulation calls in yellow baboons. American Journal of Primatology, 56, 43–56CrossRefGoogle ScholarPubMed
Shaikh, A. A., Celaya, C. L., Gomez, I. & Shaikh, S. A. 1982. Temporal relationship of hormonal peaks to ovulation and sex skin deturgescence in the baboon. Primates, 23, 444–52CrossRefGoogle Scholar
Sicchar, L. A. & Heymann, E. W. 1992. Preliminary observations on external signs of oestrus in moustached tamarins, Saguinus mystax, Callitrichidae. Laboratory Primate Newsletter, 31, 4–6Google Scholar
Sillén-Tullberg, B. & M⊘ller, A. P. 1993. The relationship between concealed ovulation and mating systems in anthropoid primates: a phylogenetic analysis. American Naturalist, 141, 1–25CrossRefGoogle ScholarPubMed
Small, M. 1989. Female choices in nonhuman primates. Yearbook of Physical Anthropology, 32, 103–27CrossRefGoogle Scholar
Smuts, B. B. & Smuts, R. W. 1993. Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior, 22, 1–63CrossRefGoogle Scholar
Sommer, V., Srivastava, A. & Borries, C. 1992. Cycles, sexuality, and conception in free-ranging langurs (Presbytis entellus). American Journal of Primatology, 28, 1–27CrossRefGoogle Scholar
Stallmann, R. R. & Babo, N. 1996. The telltale tail: a possible mechanism of specific mate recognition in Sulawesi macaques. Abstracts, 16th IPS Conference, Madison, #175
Stallmann, R. R. & Froehlich, J. W. 2000. Primate sexual swellings as coevolved signal systems. Primates, 41, 1–16CrossRefGoogle Scholar
Struhsaker, T. T. 1975. The Red Colobus Monkey. Chicago, IL: University of Chicago Press
Swedell, L. 2000. Two takeovers in wild hamadryas baboons. Folia Primatologica, 71, 169–72CrossRefGoogle ScholarPubMed
Thierry, B., Heistermann, M., Aujard, F. & Hodges, J. K. 1996. 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). American Journal of Primatology, 39, 47–623.0.CO;2-S>CrossRefGoogle Scholar
Trivers, R. L. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, 1871–1971, ed. B. Campbell. Chicago, IL: Aldine, pp. 136–79
van Schaik, C. P., van Noordwijk, M. A. & Nunn, C. L. 1999. Sex and social evolution in primates. In Comparative Primate Socioecology, ed. P. C. Lee. Cambridge: Cambridge University Press, pp. 204–31
van Schaik, C. P., Hodges, J. K. & Nunn, C. L. 2000. Paternity confusion and the ovarian cycles of female primates. In Infanticide by Males and Its Implications, ed. C. P. van Schaik & C. H. Janson. Cambridge: Cambridge University Press, pp. 361–87
Wallis, J. & Goodall, J. 1993. Anogenital swelling in pregnant chimpanzees of Gombe National Park. American Journal of Primatology, 31, 89–98CrossRefGoogle Scholar
Wasser, S. K. 1983. Reproductive competition and cooperation among female yellow baboons. In Social Behavior of Female Vertebrates, ed. S. K. Wasser. New York, NY: Academic Press, pp. 349–90
Wasser, S. K. 1996. Reproductive control in wild baboons measured by fecal steroids. Biology of Reproduction, 55, 393–9CrossRefGoogle ScholarPubMed
Weingrill, T. 2000. Infanticide and the value of male–female relationships in mountain chacma baboons. Behaviour, 137, 337–59CrossRefGoogle Scholar
West-Eberh ard, M. J. 1984. Sexual selection, competitive communication and species-specific signals in insects. In Insect Communication, ed. T. Lewis. New York, NY: Academic Press, pp. 283–324
Whitten, P. L. & Russel, E. 1996. Information content of sexual swellings and fecal steroids in sooty mangabeys (Cercocebus torquatus atys). American Journal of Primatology, 40, 67–823.0.CO;2-Z>CrossRefGoogle Scholar
Wickler, W. 1967. Socio-sexual signals and their intraspecific imitation among primates. In Primate Ethology, ed. D. Morris. London: Weidenfeld and Nicolson, pp. 69–147
Wildt, D. E., Doyle, U., 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, 261–70CrossRefGoogle Scholar
Wiley, R. H. & Poston, J. 1996. Perspective: indirect mate choice, competition for mates, and coevolution of the sexes. Evolution, 50, 1371–81CrossRefGoogle ScholarPubMed
Williams, G. C. 1966. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thoughts. Princeton, NJ: Princeton University Press
Wrangham, R. W. 2002. The cost of sexual attraction: is there a trade-off in female Pan between sex appeal and received coercion? In Behavioural Diversity in Chimpanzees and Bonobos, ed. C. Boesch, G. Hohmann & L. F. Marchant. Cambridge: Cambridge University Press, pp. 204–15
Zahavi, A. 1975. Mate selection – a selection for handicap. Journal of Theoretical Biology, 53, 205–14CrossRefGoogle ScholarPubMed
Zinner, D. & Deschner, T. 2000. Sexual swellings in female hamadryas baboons after male take-overs: ‘deceptive’ swellings as a possible female counter-strategy against infanticide. American Journal of Primatology, 52, 157–683.0.CO;2-L>CrossRefGoogle Scholar
Zinner, D., Schwibbe, M. H. & Kaumanns, W. 1994. Cycle synchrony and probability of conception in female hamadryas baboons, Papio hamadryas. Behavioral Ecology and Sociobiology, 35, 175–83CrossRefGoogle Scholar
Zinner, D., Alberts, S. C., Nunn, C. L. & Altmann, J. 2002. Significance of primate sexual swellings. Nature, 420, 142–3CrossRefGoogle ScholarPubMed
Zuckerman, S. & Parkes, A. S. 1939. Observations on the secondary characters in monkeys. Journal of Endocrinology, 1, 430–9CrossRefGoogle Scholar

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×