Abstract
Adolescent females of 11 primate species display exaggerated versions of the cues to sexual cycle state or fertility which are displayed by adult females: anubis baboons; geladas; Assamese, Barbary, crab-eating, Japanese, and stump-tailed macaques; patas monkeys; gorillas; and humans. These cases are briefly described and a variety of hypotheses is presented and evaluated to account for the adolescent exaggeration. Such exaggeration may be a super-normal sexual stimulus, a barrier to cross-species hybridization, a helpful prop in female:female competition, a passport for transfers, an insurance policy where unpredictable changes of circumstance are likely, or a non-adaptive side-effect of some other phenomenon. The transfer and unpredictability hypotheses seem to apply to the largest number of species, including humans.
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References
Anderson, C., 1986. Female age: male preference and reproductive success in primates.Int. J. Primatol., 7: 305–326.
—, 1989. The spread of exclusive mating in a chacma baboon population.Amer. J. Phys. Anthropol., 78: 355–360.
Bateman, G., 1984. All the World's Animals: Primates. Equinox, Oxford.
Baulu, T., 1976. Seasonal sex skin coloration and hormonal fluctuations in free-ranging and captive monkeys.Horm. Behav., 7: 481–494.
Bercovitch, F., 1991. Mate selection, consortship formation, and reproductive tactics in adult female savannah baboons.Primates, 32: 437–452.
Bernstein, I., 1968. The lutong of Kuala Selangor.Behaviour, 32: 1–16.
— &T. Gordon, 1980. Mixed taxa introductions, hybrids and macaque systematics. In:The Macaques,D. Lindburg (ed.), Van Nostrand Reinhold, New York, pp. 125–147.
Bielert, C. &C. Anderson, 1985. Baboon sexual swellings and male response: a possible operational mammalian supernormal stimulus and response interaction.Int. J. Primatol., 6: 377–393.
— &L. Girolami, 1986. Experimental asessments of behavioral and anatomical components of female chacma baboon sexual attractiveness.Psychoneuroendocrinology, 11: 75–90.
—, —, &C. Anderson, 1986. Male chacma baboon (Papio ursinus) sexual arousal: Studies with adolescent and adult females as visual stimuli.Dev. Psychobiol., 19: 369–383.
Borgerhoff Mulder, M., 1988. Kipsigis bridewealth payments. In:Human Reproductive Behaviour,L. Betzig,M. Borgerhoff Mulder, &P. Turke (eds.), Cambridge Univ. Press, Cambridge, pp. 65–82.
Burrell, R., M. Healy, &J. Tanner, 1961. Age at menarche in South African Bantu schoolgirls living in the Transkei Reserve.Human Biol., 33: 250–261.
Burt, A., 1989. Comparative methods using phylogenetically independent contrasts. Oxford Surv.Evol. Biol., 6: 33–53.
Cant, J., 1981. Hypothesis for the evolution of human breasts and buttocks.Amer. Naturalist, 117: 199–204.
Chism, J., T. Rowell, &D. Olson, 1984. Life history patterns of female patas monkeys. In:Female Primates,M. Small (ed.), Liss, New York, pp. 175–192.
Chivers, D. J., 1974. The siamang in Malaya.Contributions to Primatology Vol. 4.
Cohen, R., 1967.The Kanuri of Bornu. Holt, Rinehart & Winston, New York.
Cords, M., 1987. Forest guenons and patas monkeys. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 98–111.
Curtin, S. H., 1980. Dusky and banded leaf monkeys. In:Malayan Forest Primates,D. Chivers (ed.), Plenum, New York, pp. 18–27.
Deag, J., 1974. A study of the social behaviour and ecology of the wild barbary macaque,Macaca sylvanus L., Unpubl. Ph.D. thesis, Bristol Univ., Avon.
Deputte, B. &M. Goustard, 1980. Copulatory vocalizations of female macaques (Macaca fascicularis).Primates, 21: 83–99.
DeWaal, F. &L. Luttrell, 1989. Toward a comparative social ecology of the genusMacaca: different dominance styles in rhesus and stumptail monkeys.Amer. J. Primatol., 19: 83–109.
Dittus, W., 1975. Population dynamics of the toque monkey,Macaca sinica. In:Socioecology and Psychology of Primates,R. H. Tuttle (ed.), Mouton, The Hague, pp. 125–151.
—, 1977. The social regulation of population density and age-sex distribution in the toque monkey.Behaviour, 63: 281–322.
Dixson, A., 1983. Observations on the evolution and behavioral significance of “sexual skin” in female primates. In:Advances in the Study of Behavior, Vol. 13,J. Rosenblatt,R. Hinde,C. Beer, &M.-C. Busnel (eds.), Academic Press, New York, pp. 63–106.
Dunbar, R., 1977. Age-dependent changes in sexual skin colour and associated phenomena of female gelada baboons.J. Human Evol., 6: 667–672.
—, 1979. Structure of gelada baboon reproductive units.Behaviour, 69: 72–87.
— &P. Dunbar, 1973. On hybridization betweenTheropithecus gelada andPapio anubis in the wild.Amer. J. Phys. Anthropol., 43: 187–192.
Eaton, G., 1976. The social order of Japanese macaques.Sci. Amer., 235: 96–106.
Eisenberg, J., N. Muckenhirn, &R. Rudran, 1972. The relationship between ecology and social structure in primates.Science, 176: 863–874.
Enomoto, T., 1978. On social preferences in sexual behavior of Japanese monkeys (Macaca fuscata).J. Human Evol., 7: 283–293.
Estrada, A., 1984. Adult male-immature interactions in captive stumptail macaques (Macaca arctoides). In:Primate Paternalism,D. Taub (ed.), Van Nostrand Reinhold, New York, pp. 56–87.
Fa, J., 1984. The Barbary macaque. In:The Barbary Macaque,J. Fa (ed.), Plenum, New York, pp. 3–15.
Felsenstein, J., 1985. Phylogenies and the comparative method.Amer. Naturalist, 125: 1–16.
Fisher, R., 1930.The Genetical Theory of Natural Selection. Clarendon, Oxford.
Fleagle, J. G., 1988.Primate Adaptations and Evolution. Academic Press, San Diego.
Fossey, D., 1983.Gorillas in the Mist. Houghton Mifflin, Boston.
Furuichi, T., 1987. Sexual swelling, receptivity, and grouping of wild pygmy chimpanzee females at Wamba, Zaire.Primates, 28: 309–318.
Galdikas, B., 1985. Subadult male orangutan socially and reproductive behavior at Tanjung Puting.Amer. J. Primatol., 8: 87–99.
Gallup, G., 1982. Permanent breast enlargement in human females.J. Human Evol., 11: 597–601.
Gillman, J. &C. Gilbert, 1946. The reproductive role of the chacma baboonPapio ursinus with specific reference to the problems of menstrual irregularities as assessed by the behaviour of the sexual skin.S. Af. J. Med. Sci., 11: 1–54.
Girolami, L. &C. Bielert, 1987. Female perineal swelling and its effects on male sexual arousal.Int. J. Primatol., 8: 651–661.
Glick, B., 1980. Ontogenetic and psychobiological aspects of the mating activities of maleMacaca radiata. In:The Macaques,D. Lindburg (ed.), Van Nostrand Reinhold, New York, pp. 345–370.
Goodall, J., 1983. Population dynamics during a 15-year period in one community of free-living chimpanzees in the Gombe National Park, Tanzania.Zeit. Tierpsychol., 61: 1–60.
—, 1986.The Chimpanzees of Gombe. Harvard Univ. Press, Cambridge, Massachusetts.
—, 1989. Gombe: highlights and current research. In:Understanding Chimpanzees,P. Heltne &L. Marquardt (eds.), Harvard Univ. Press, Cambridge, Massachusetts, pp. 2–21.
Greska, L., 1990. Age of menarche in Bolivian girls of European and Aymara ancestry.Ann. Human Biol., 17: 49–53.
Gust, D. &T. Gordon, 1991. Male age and reproductive behavior in sooty mangabeys,Cercocebus torquatus atys.Anim. Behav., 41: 277–283.
Hadidan, J. &I. Bernstein, 1979. Female reproductive cycles and birth data from an Old World monkey colony.Primates, 20: 429–442.
Hamilton, M., 1984. Revising evolutionary narratives: a consideration of evolutionary assumptions about sexual selection and competition for mates.Amer. Anthropol., 86: 651–662.
Harcourt, A., D. Fossey, K. Stewart, &D. Watts, 1980. Reproduction in wild gorillas and some comparisons with chimpanzees.J. Reprod. Fertil. Suppl., 28: 59–70.
Harrison, M. J. S., 1988. The mandrill in Gabon's rain forest.Oryx, 22: 218–228.
Harvey, P. &M. Pagel, 1991.The Comparative Method in Evolutionary Biology. Oxford Univ. Press, Oxford.
—,R. Martin, &T. Clutton-Brock, 1987. Life histories in comparative perspective. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 181–196.
Hill, D., 1987. Social relationships between adult male and female rhesus macaques: I. Sexual consortships.Primates, 28: 439–456.
Hrdy, S., 1977.The Langurs of Abu. Harvard Univ. Press, Cambridge, Massachusetts.
—, 1981.The Woman that Never Evolved. Harvard Univ. Press, Cambridge, Massachusetts.
— &P. Whitten, 1987. Patterning of sexual activity. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 370–384.
Israel, S., 1959. The onset of menstruation in Indian women.J. Obstet. Gynecol. Brit. Emp., 66: 311–316.
Jolly, A., 1972.The Evolution of Primate Behavior. MacMillan, New York.
Kalkstein, T., 1991. Occurrence and function of sexual swelling in stumptail macaques.Amer. J. Phys. Anthropol., Suppl., 12: 101–102.
Katch, V., B. Campaigne, P. Freedson, S. Sady, F. Katch, &A. Behnke, 1980. Contribution of breast volume and weight to body fat distribution in females.Amer. J. Phys. Anthropol., 53: 93–100.
Koyama, N., Y. Takahata, M. Huffman, K. Norikoshi, &A. Suzuki, 1992. Reproductive parameters of female Japanese Macaques.Primates, 33: 33–47.
Kummer, H., 1968.Social Organization of Hamadryas Baboons. Univ. of Chicago Press, Chicago.
—, 1985. A male-dominated society. In:All the World's Animals: Primates,G. Bateman (ed.), Torstar, New York, pp. 98–99.
Lancaster, J., 1984. Evolutionary perspectives on sex differences in the higher primates. In:Gender and the Life Course,A. Rossi (ed.), Aldine, New York, pp. 3–27.
—, 1986. Human adolescence and reproduction. In:Schoolage Pregnancy and Parenthood,J. Lancaster &B. Hamburg (eds.), Aldine de Gruyter, New York, pp. 17–37.
Lewontin, R., 1979. Sociobiology as an adaptationist program.Behav. Sci., 24: 5–14.
— &S. Gould, 1979. The spandrels of San Macro and the Panglossian paradigm: a critique of the adaptationist programme.Proc. Roy. Soc. Lond. Ser. B, 205: 581–598.
Lindburg, D., 1983. Mating behavior and estrus in the Indian rhesus monkey. In:Perspectives in Primate Biology,P. Seth (ed.), Today & Tomorrow, New Delhi, pp. 45–61.
Linnankoski, I. &L. Leinonen, 1985. Compatibility of male and female sexual behavior inMacaca arctoides.Z. Tierpsychol., 70: 115–122.
Loy, J., 1975. The copulatory behavior of the adult male patas monkeys,Erythrocebus patas.J. Reprod. Fertil., 45: 193–195.
Marsh, C., 1979. Comparative aspects of social organization in the Tana River red colobus,Colobus badius rufomitratus.Z. Tierpsychol., 51: 337–362.
Martin, R., 1983.Human Brain Evolution in an Ecological Context. American Museum of Natural History, New York.
Mascia-Lees, F., J. Relethford, &T. Sorger, 1986. Evolutionary perspectives on permanent breast enlargement in human females.Amer. Anthropol., 88: 423–428.
Melnick, D. &M. Pearl, 1987. Cercopithecines in multimale groups. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 121–134.
Molnar, S., 1992.Human Variation. Prentice-Hall, Englewood Cliffs.
Moore, J., 1984. Female transfer in primates.Int. J. Primatol., 5: 537–590.
Mori, A., 1979. Unit formation and the emergence of a new leader. In:Ecological and Sociological Studies of Gelada Baboons,M. Kawai (ed.), Karger, Basel, pp. 155–181.
Morris, D., 1967.The Naked Ape. McGraw-Hill, New York.
Nakagawa, N., 1989. Activity budget and diet of patas monkeys in Kala Maloue National Park, Cameroon.Primates, 30: 27–34.
Nash, M., 1965.The Golden Road to Modernity. Wiley & Sons, New York.
Nieuwenhuijsen, K., M. Bonkejansen, E. Broekhuijzan, K. de Neef, J. van Hooff, J. van der Ten Bosch, &A. Slob, 1988. Behavioral aspects of puberty in group-living stumptail monkeys (Macaca arctoides).Physiol. Behav., 42: 255–264.
Oates, J., 1977. The social life of a black-and-white colobus monkey (Colobus guereza).Z. Tierpsychol., 45: 1–60.
Paul, A. &D. Thommen, 1984. Timing of birth, female reproductive success and infant sex ratio in semifree-ranging Barbary macaques (Macaca sylvanus).Folia Primatol., 42: 2–16.
Pereira, M. &J. Altmann, 1985. Development of social behavior in free-living non-human primates. In:Nonhuman Primate Models for Human Growth and Development,E. Watts (ed.), Liss, New York, pp. 217–309.
Poirier, F. E., 1970. The Nilgiri langur (Presbytis johnii) of South India. In:Primate Behavior, Vol. 1, Academic Press, New York, pp. 251–283.
— &E. Smith, 1974. Socializing function of primate play.Amer. Zool., 14: 275–287.
Prud'Homme, J., 1991. Group fission in a semifree-ranging population of Barbary macaques (Macaca sylvanus).Primates, 32: 9–22.
Pusey, A., 1990. Behavioural changes at adolescence in chimpanzees.Behaviour, 115: 203–246.
Rasmussen, K., 1983. Age-related variation in the interactions of adult females with adult males in yellow baboons. In:Primate Social Relationships,R. Hinde (ed.), Blackwell, Oxford, pp. 47–53.
Rodman, P., 1991. Structural differentiation of microhabitats of sympatricMacaca fascicularis andMacaca nemestrina in East Kalimantan, Indonesia.Int. J. Primatol., 12: 357–375.
Rowell, T., 1972.The Social Behavior of Monkeys. Penguin, Baltimore.
—, 1979. How would we know if social organization were not adaptive? In:Primate Ecology and Human Origins,I. Bernstein &E. Smith (eds.), Garland, New York, pp. 1–22.
— &S. Richard, 1979. Reproductive strategies of some African monkeys.J. Mammal., 60: 58–69.
Rudran, R., 1973. The reproductive cycles of two subspecies of purple-faced langurs (Presbytis senex) with relation to environmental factors.Folia Primatol., 19: 166–192.
Santillan-Doherty, A.-M. &R. Mondragon-Ceballos, 1991. Male-female coalitions in dominance takeovers in a captive group of stumptail macaques. In:Primatology Today,A. Ehara,T. Kimura,O. Takenaka, &M. Iwamoto (eds.), Elsevier, Amsterdam, pp. 145–146.
Schulman, S. &B. Chapais, 1980. Reproductive value and rank relations among macaque sisters.Amer. Naturalist, 115: 580–593.
Schultz, A., 1969.The Life of the Primates. Universe Books, New York.
Scott, L., 1984. Reproductive behavior of adolescent female baboons (Papio anubis) in Kenya. In:Female Primates,M. Small (ed.), Liss, New York, pp. 77–102.
Service, E., 1962.Primitive Social Organization: An Evolutionary Perspective. Random House, New York.
Shiveley, C., S. Clarke, N. King, S. Schapiro, &G. Mitchell, 1982. Patterns of sexual behavior in male macaques.Amer. J. Primatol., 2: 373–384.
Short, R., 1976. The evolution of human reproduction.Proc. Roy. Soc. Lond., 195: 3–24.
Small, M., 1983. Females without infants: mating strategies in two species of captive macaques.Folia Primatol., 40: 125–133.
—, 1990. Promiscuity in Barbary macaques (Macaca sylvanus).Amer. J. Primatol., 20: 267–282.
Smuts, B., 1985.Sex and Friendship in Baboons. Aldine, Hawthorne, New York.
Stephenson, G., 1974. Social structure of mating activity in Japanese macaques. In:Proceedings from the Symposia of the Fifth Congress of the International Primatological Society,S. Kondo,M. Kawai,A. Ehara, &S. Kawamura (eds.), Japan Science Press, Tokyo, pp. 63–115.
Stewart, K. &A. Harcourt, 1987. Gorillas: variation in female relationships. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 155–164.
Struhsaker, T. &L. Leland, 1987. Colobines: infanticide by adult males. In:Primate Societies,B. Smuts,D. Cheney,R. Seyfarth,R. Wrangham, &T. Struhsaker (eds.), Univ. of Chicago Press, Chicago, pp. 83–97.
Strum, S., 1984. Why males use infants. In:Primate Paternalism,D. Taub (ed.), Van Nostrand Reinhold, New York, pp. 146–185.
— &J. Western, 1982. Variations in fecundity with age and environment in olive baboons (Papio anubis).Amer. J. Primatol., 3: 61–76.
Stukovsky, R., J. Valsic, &M. Bulai-Stirbu, 1967. Family size and menarcheal age in Constanza, Roumania.Human Biol., 39: 277–283.
Szalay, F. &E. Delson, 1979.Evolutionary History of the Primates. Academic Press, New York.
Taub, D., 1980. Female choice and mating strategies among wild Barbary macaques (Macaca sylvanus L.). In:The Macaques,D. Lindburg (ed.), Van Nostrand Reinhold, New York, pp. 287–344.
Turke, P., 1984. Effects of ovulatory concealment and synchrony on protohominid mating systems and parental roles.Ethol. Sociobiol., 5: 33–44.
van Noordwijk, M., 1985. Sexual behaviour of Sumatran long-tailed macaques (Macaca fascicularis).Zeit. Tierpsychol., 70: 277–296.
van Schaik, C., 1989. The ecology of social relationships amongst female primates. In:Comparative Socioecology of Humans and Other Mammals,V. Standen &R. Foley (eds.), Blackwell, Oxford, pp. 195–218.
Watanabe, K., H. Lapasere, &R. Tantu, 1991. External characteristics and associated developmental changes in two species of Sulawesi macaques,Macaca tonkeana andM. hecki, with special reference to hybrids and the borderland between the species.Primates, 32: 61–76.
Wheatley, B., 1978. The behavior and ecology of the crab-eating macaque (Macaca fascicularis) in the Kutai Nature Reserve, East Kalimantan, Indonesia. Unpubl. Ph.D. thesis, Univ. of California, Davis.
Wickler, W., 1967. Socio-sexual signals. In:Primate Ethology,D. Morris (ed.), Weidenfeld & Nicolson, London, pp. 89–189.
Wilson, E., 1975.Sociobiology: The New Synthesis. Harvard Univ. Press, Cambridge, Massachusetts.
Wilson, M., M. Walker, N. Pope, &T. Gordon, 1988. Prolonged lactational infertility in adolescent rhesus monkeys.Biol. Reprod., 38: 163–174.
Wolfe, K. &S. Schulman, 1984. Male response to “stranger” females as a function of female reproductive value among chimpanzees.Amer. Naturalist, 123: 163–174.
Wolfe, L., 1984. Japanese macaque female sexual behavior. In:Female Primates,M. Small (ed.), Liss, New York, pp. 141–158.
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Anderson, C.M., Bielert, C.F. Adolescent exaggeration in female catarrhine primates. Primates 35, 283–300 (1994). https://doi.org/10.1007/BF02382726
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DOI: https://doi.org/10.1007/BF02382726
Key Words
- Adolescentes
- Sexual displays