Development and sexual selection in primates

doi:10.1017/CBO9780511542459.012

10 - Development and sexual selection in primates

Published online by Cambridge University Press: 10 August 2009

Joanna M. Setchell and

Phyllis C. Lee

Edited by

Peter M. Kappeler and

Carel P. van Schaik

Show author details

Joanna M. Setchell: Affiliation:
Department of Biological Anthropology, University of Cambridge, Downing Street, Cambridge, UK
Phyllis C. Lee: Affiliation:
Department of Anthropology, University of Cambridge, Cambridge, UK
Peter M. Kappeler: Affiliation:
Deutsches Primatenzentrum, Göttingen, Germany
Carel P. van Schaik: Affiliation:
Duke University, North Carolina

Book contents

Get access

Summary

INTRODUCTION

Studies of sexual selection in primates or other animals tend to focus on outcomes – sexual dimorphism, differential mating and reproductive success for adult males and females. However, adult sex differences represent the end-points of complex and interrelated developmental processes, and arise from differences in behaviour and physiology between males and females. In most vertebrates, including primates, the sexes are nearly identical in size and shape during early development, and adult differences are thus the product of divergent growth strategies (Badyaev, 2002). Sex differences in growth and development arise as a result of the different roles played by the two sexes in reproduction and the corresponding determinants of reproductive success for males and females, which are intricately linked to social organisation and mating system (Kappeler & van Schaik, 2002). Evolution shapes processes throughout the lifecycle, and the mechanisms for partitioning resources among growth, reproduction and survival are, to a large part, established during development, while consequences may not be observed until the end of the lifespan. A developmental perspective is therefore fundamental to studies of the action of sexual selection (see also Pereira & Leigh, 2003).

For mammals in general, and primates in particular, past work on sexual selection and development has concentrated on the influence of growth on sexual dimorphism (e.g. ungulates: Jarman, 1983; Georgiadis, 1985; Clutton-Brock et al., 1992; seals: Trillmich, 1996; primates: Leigh, 1995; Pereira & Leigh, 2003) or growth and life-history traits such as rates of reproduction (e.g. Gordon, 1989; Pontier et al. , 1989; Lee & 2003).

Type: Chapter
Information: Sexual Selection in Primates
New and Comparative Perspectives
, pp. 175 - 195

DOI: https://doi.org/10.1017/CBO9780511542459.012 [Opens in a new window]

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.)

Book purchase

Temporarily unavailable

References

Abbott, D. H., George, L. M., Barrett, J. et al. 1990. Social control of ovulation in marmoset monkeys: a neuroendocrine basis for the study of infertility. In Socioendocrinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley Liss, pp. 135–58

Alberts, S. C. & Altmann, J. 1995a. Preparation and activation – determinants of age at reproductive maturity in male baboons. Behavioral Ecology and Sociobiology, 36, 397–406CrossRef Google Scholar

Alberts, S. C. & Altmann, J. 1995b. Balancing costs and opportunities – dispersal in male baboons. American Naturalist, 145, 279–306CrossRef Google Scholar

Alberts, S. C., Altmann, J. & Wilson, M. 1996. Mate guarding constrains foraging activity of male baboons. Animal Behaviour, 51, 1269–77CrossRef Google Scholar

Altmann, J. 1980. Baboon Mothers and Infants. Chicago, IL: University of Chicago Press

Altmann, J. & Alberts, S. C. 1987. Body mass and growth rates in a wild primate population. Oecologia, 72, 15–20CrossRef Google Scholar

Altmann, J., Alberts, S. C., Haines, S. A.et al. 1996. Social structure predicts genetic structure in a wild primate group. Proceedings of the National Academy of Science, USA, 93, 5797–801CrossRef Google Scholar

Altmann, J., Altmann, S. A. & Hausfater, G. 1981. Physical maturation and age estimates of yellow baboons. American Journal of Primatology, 1, 389–99CrossRef Google Scholar

Altmann, S. A. 1991. Diets of yearling female primates, Papio cynocephalus, predict lifetime fitness. Proceedings of the National Academy of Science, USA, 88, 420–3CrossRef Google Scholar PubMed

Altmann, S. A. 1998. Foraging for Survival. Chicago, IL: University of Chicago Press

Badyaev, A. V. 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends of Ecology and Evolution, 17, 369–78CrossRef Google Scholar

Bateson, P. P. G. 1981. Ontogeny of behaviour. British Medical Journal, 37, 159–64Google Scholar PubMed

Bearder, S. K. 1987. Lorises, bushbabies and tarsiers: diverse societies in solitary foragers. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 11–24

Bercovitch, F. B. 1983. Time budgets and consortships in olive baboons, Papio anubis. Folia Primatologica, 41, 180–90CrossRef Google Scholar

Bercovitch, F. B. 1993. Dominance rank and reproductive maturation in male rhesus macaques, Macaca mulatta. Journal of Reproduction and Fertility, 99, 113–20CrossRef Google Scholar

Bercovitch, F. B. 2000. Behavioral ecology and socioendocrinology of reproductive maturation in cercopithecine monkeys. In Old World Monkeys, ed. P. F. Whitehead & C. J. Jolly. Cambridge: Cambridge University Press, pp. 298–320

Bercovitch, F. B. 2001. Reproductive ecology of Old World Monkeys. In Reproductive Ecology and Human Evolution, ed. P. T. Ellison. New York, NY: Aldine, pp. 369–96

Bercovitch, F. B. 2002. Sex-biased parental investment in primates. International Journal of Primatology, 23, 905–21CrossRef Google Scholar

Bercovitch, F. B. & Goy, R. 1990. The socioendocrinology of reproductive development and reproductive success in macaques. In Socioendocrinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley-Liss, pp. 59–93

Bercovitch, F. B. & Strum, S. 1993. Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behavioral Ecology and Sociobiology, 33, 313–18CrossRef Google Scholar

Bercovitch, F. B., Lebron, M. R., Martinez, H. S. & Kessler, M. J. 1998. Primigravidity, body weight and the costs of rearing first offspring in rhesus macaques. American Journal of Primatology, 46, 135–443.0.CO;2-X>CrossRef Google Scholar PubMed

Berman, C. M. 1980. Mother–infant relationships among free-ranging rhesus monkeys on Cayo Santiago: a comparison with captive pairs. Animal Behaviour, 28, 860–73CrossRef Google Scholar

Bernstein, I. S., Ruehlmann, T. E., Judge, P. G., Lindquist, T. & Weed, J. L. 1991. Testosterone changes during the period of adolescence in male rhesus monkeys, Macaca mulatta. American Journal of Primatology, 24, 29–38CrossRef Google Scholar

Boesch, C. 1997. Evidence for dominant wild chimpanzees investing more in sons. Animal Behaviour, 54, 811–15CrossRef Google Scholar PubMed

Bogin, B. 1999. Patterns of Human Growth. Cambridge: Cambridge University Press

Bowman, J. E. & Lee, P. C. 1995. Growth and threshold weaning weights among captive rhesus macaques. American Journal of Physical Anthropology, 96, 159–75CrossRef Google Scholar PubMed

Brockmann, H. J. 2001. The evolution of alternative strategies and tactics. Advances in the Study of Behavior, 30, 1–51CrossRef Google Scholar

Brody, S. 1945. Bioenergetics and Growth. New York, NY: Rheinhold

Brown, G. R. 2001. Sex-biased investment in non-human primates: can Trivers & Willard's theory be tested? Animal Behaviour, 61, 683–94CrossRef Google Scholar

Brown, G. R. & Dixson, A. F. 2000. The development of behavioural sex differences in infant rhesus macaques, Macaca mulatta. Primates, 41, 63–77CrossRef Google Scholar

Brown, G. R. & Silk, J. B. 2002. Reconsidering the null hypothesis: is maternal rank associated with birth sex ratios in primate groups?Proceedings of the National Academy of Science, USA, 99, 11252–5CrossRef Google Scholar PubMed

Caine, N. G. 1987. Behavior during puberty and adolescence. In Comparative Primate Biology, Vol. 2A, ed. G. Mitchell & J. Erwin. New York, NY: Alan R. Liss, pp. 327–61

Caro, T. M. & Bateson, P. P. G. 1986. Organisation and ontogeny of alternative tactics. Animal Behaviour, 34, 1483–99CrossRef Google Scholar

Charles-Dominique, P. 1977. Ecology and Behaviour of Nocturnal Primates. London: Duckworth

Cheverud, J. M., Wilson, P. & Dittus, W. P. J. 1992. Primate population studies at Polonnaruwa. 3. Somatometric growth in a natural population of toque macaques, Macaca sinica. Journal of Human Evolution, 23, 51–77CrossRef Google Scholar

Clubb, R. & Mason, G. 2002. A Review of the Welfare of Zoo Elephants in Europe. Oxford: Department of Zoology, University of Oxford

Clutton-Brock, T. H. 1991. The evolution of sex differences and the consequences of polygyny in mammals. In The Development and Integration of Behaviour, ed. P. P. G. Bateson. Cambridge: University of Cambridge Press, pp. 229–53

Clutton-Brock, T. H., Harvey, P. H. & Rudder, B. 1977. Sexual dimorphism, socionomic sex ratio and body weight in primates. Nature, 269, 797–800CrossRef Google Scholar PubMed

Clutton-Brock, T. H., Guinness, F. E. & Albon, S. D. 1992. Red Deer: Behavior and Ecology of Two Sexes. Edinburgh: Edinburgh University Press

Colvin, J. 1983. Familiarity, rank and the structure of rhesus male peer networks. In Primate Social Relationships, ed. R. A. Hinde. Oxford: Blackwell, pp. 190–200

Dang, D. C. & Meussy-Dessolle, N. 1984. Quantitative study of testis histology and plasma androgens at onset of spermatogenesis in the prepubertal laboratory-born macaque, Macaca fascicularis. Archives of Andrology, 12, S43–51Google Scholar

Debyser, I. 1995. Prosimian juvenile mortality in zoos and primate centers. International Journal of Primatology, 16, 889–907CrossRef Google Scholar

Demment, M. W. 1983. Feeding ecology and the evolution of body size of baboons. African Journal of Ecology, 21, 219–33CrossRef Google Scholar

Dixson, A. F. 1998. Primate Sexuality. Comparative Studies of the Prosimians, Monkeys, Apes and Human Beings. Oxford: Oxford University Press

Dixson, A. F. & Nevison, C. 1997. The socioendocrinology of adolescent development in male rhesus monkeys, Macaca mulatta. Hormones and Behavior, 31, 126–35CrossRef Google Scholar

Draper, P. & Harpending, H. 1982. Father absence and reproductive strategy: an evolutionary perspective. Journal of Anthropological Research, 38, 255–73CrossRef Google Scholar

Dunbar, R. I. M. 1984. Reproductive Decisions: An Economic Analysis of Gelada Baboon Social Strategies. Princeton, NJ: Princeton University Press

Eisler, J. A., Tannenbaum, P. L., Mann, D. R. & Wallen, K. 1993. Neonatal testicular suppression with a GnRH agonist in rhesus monkeys: effect on adult endocrine function and behavior. Hormones and Behavior, 27, 551–67CrossRef Google Scholar PubMed

Fairbanks, L. M. 1996. Individual differences in maternal style: causes and consequences for offspring. In Parental Care: Evolutionary Mechanisms and Adaptive Significance, ed. J. S. Rosenblatt & C. T. Snowdon. London: Academic Press, pp. 579–611

Fedigan, L. M. & Zohar, S. 1997. Sex differences in mortality of Japanese macaques: twenty-one years of data from the Arashiyama West population. American Journal of Physical Anthropology, 102, 161–723.0.CO;2-1>CrossRef Google Scholar PubMed

Folstad, I. & Karter, A. J. 1992. Parasites, bright males and the immunocompetence handicap. American Naturalist, 139, 603–22CrossRef Google Scholar

Ford, S. M. 1994. Evolution of sexual dimorphism in body weight in platyrrhines. American Journal of Primatology, 34, 221–44CrossRef Google Scholar

Galliari, C. A. & Colillas, O. J. 1985. Sequences and timing of dental eruption in Bolivian captive-born squirrel-monkeys, Saimiri sciureus. American Journal of Primatology, 8, 195–204CrossRef Google Scholar

Gavan, J. A. & Swindler, D. R. 1966. Growth rates and phylogeny in primates. American Journal of Physical Anthropology, 38, 69–82CrossRef Google Scholar

Georgiadis, N. 1985. Growth patterns, sexual dimorphism and reproduction in African ruminants. African Journal of Ecology, 23, 75–87CrossRef Google Scholar

Glick, B. B. 1979. Testicular size, testosterone level and body weight in male Macaca radiata. Folia Primatologica, 32, 268–89Google Scholar

Godfrey, L., Samonds, K., Jungers, W. & Sutherland, M. 2001. Teeth, brains, and primate life histories. American Journal of Physical Anthropology, 114, 192–2143.0.CO;2-Q>CrossRef Google Scholar PubMed

Gomendio, M. 1990. The influence of maternal rank and infant sex on maternal investment trends in macaques: birth sex ratios, inter-birth intervals and suckling patterns. Behavioral Ecology and Sociobiology, 27, 365–75CrossRef Google Scholar

Gordon, I. J. 1989. The interspecific allometry of reproduction – do larger species invest relatively less in their offspring? Functional Ecology, 3, 285–8CrossRef Google Scholar

Graham, C. & Nadler, R. 1990. Socioendocrine interactions in great ape reproduction. In Socioendocrinology of Primate Reproduction, ed. T. Ziegler & F. B. Bercovitch. New York, NY: Wiley Liss, pp. 33–58

Gust, D. A. & Gordon, T. P. 1991. Male age and reproductive behavior in sooty mangabeys, Cercocebus torquatus atys. Animal Behaviour, 41, 277–83CrossRef Google Scholar

Hamada, Y. & Udono, T. 2002. Longitudinal analysis of length-growth in the chimpanzee Pan troglodytes. American Journal of Physical Anthropology, 118, 268–84CrossRef Google Scholar PubMed

Hamilton, W. J. III & Bulger, J. B. 1990. Natal male baboon rank rises and successful challenges to resident alpha males. Behavioral Ecology and Sociobiology, 26, 357–62CrossRef Google Scholar

Harcourt, A. H. & Stewart, K. J. 1981. Gorilla male relationships – can differences during immaturity lead to contrasting reproductive tactics in adulthood? Animal Behaviour, 29, 206–10CrossRef Google Scholar

Hauser, M. & Harcourt, A. H. 1992. Is there sex-biased mortality in primates?Folia Primatologica, 58, 47–52CrossRef Google Scholar PubMed

Hobson, W. C., Winter, J. S. D., Reyes, F. I., Fuller, G. B. & Faiman, C. 1980. Nonhuman primates as models for studies on puberty. In Animal Models in Human Reproduction, ed. M. Serio & L. Martin. New York, NY: Raven Press, pp. 409–21

Isbell, L. A., Cheney, D. L. & Seyfarth, R. M. 1990. Costs and benefits of home range shifts among vervet monkeys, Cercopithecus aethiops, in Amboseli National Park, Kenya. Behavioral Ecology and Sociobiology, 27, 351–8CrossRef Google Scholar

Itoigawa, N., Tanaka, T., Ukai, N.et al. 1992. Demography and reproductive parameters of a free-ranging group of Japanese macaques, Macaca fuscata, at Katsuyama. Primates, 33, 49–68CrossRef Google Scholar

Izard, M. 1990. Social influences on the reproductive success and reproductive endocrinology of prosimian primates. In Socioendocrinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley-Liss, pp. 159–86

Janson, C. H. & van Schaik, C. P. 1993. Ecological risk aversion in juvenile primates: slow and steady wins the race. In Juvenile Primates: Life History, Development, and Behavior, ed. M. E. Pereira & L. A. Fairbanks. New York, NY: Oxford University Press, pp. 57–74

Jarman, P. J. 1983. Mating system and sexual dimorphism in large terrestrial mammalian herbivores. Biological Reviews, 58, 485–520CrossRef Google Scholar

Johnson, R. L. & Kapsalis, E. 1995. Determinants of postnatal weight in infant rhesus monkeys: implications for the study of interindividual differences in neonatal growth. American Journal of Physical Anthropology, 98, 343–53CrossRef Google Scholar

Johnson, R. L. & Kapsalis, E. 1998. Menopause in free-ranging rhesus macaques: estimated incidence, relation to body condition, and adaptive significance. International Journal of Primatology, 19, 751–65CrossRef Google Scholar

Kappeler, P. M. 1999. Primate socioecology: new insights from males. Naturwissenschaften, 86, 8–29CrossRef Google Scholar PubMed

Kappeler, P. M. & Schaik, C. P. 2002. The evolution of primate social systems. International Journal of Primatology, 23, 707–40CrossRef Google Scholar

Kraemer, H. C., Horvat, J. R., Doering, C. & McGinnis, P. R. 1982. Male chimpanzee development focusing on adolescence: integration of behavior with physiological changes. Primates, 23, 393–405CrossRef Google Scholar

Kruuk, L. E. B., Clutton-Brock, T. H., Rose, K. E. & Guinness, F. E. 1999. Early determinants of lifetime reproductive success differ between the sexes in red deer. Proceedings of the Royal Society of London, Series B, 266, 1655–61CrossRef Google Scholar PubMed

Kuester, J. & Paul, A. 1999. Male migration in Barbary macaques, Macaca sylvanus, at Affenberg Salem. International Journal of Primatology, 20, 85–106CrossRef Google Scholar

Lee, P. C. 1997. The meanings of weaning: growth, lactation and life history. Evolutionary Anthropology, 5, 87–963.0.CO;2-T>CrossRef Google Scholar

Lee, P. C. 1999. Comparative ecology of post-natal growth and weaning among haplorhine primates. In Comparative Primate Socioecology, ed. P. C. Lee. Cambridge: Cambridge University Press, pp. 111–39

Lee, P. C. & Johnson, J. 1992. Sex differences in the acquisition of dominance status among primates. In Cooperation and Competition in Animals and Humans, ed. A. H. Harcourt & F. B. de Waal. Oxford: Oxford University Press, pp. 391–414

Lee, P. C. & Kappeler, P. M. 2003. Socio-ecological correlates of phenotypic plasticity in primate life history. In Primate Life History and Socioecology, ed. P. M. Kappeler & M. E. Pereira, in press. Chicago, IL: University of Chicago Press

Lee, P. C. & Moss, C. J. 1986. Early maternal investment in male and female African elephant calves. Behavioral Ecology and Sociobiology, 18, 353–61CrossRef Google Scholar

Lee, P. C. 1995. Statural growth in known-age African elephants, Loxodonta africana. Journal of Zoology, London, 236, 29–41CrossRef Google Scholar

Lee, P. C., Majluf, P. & Gordon, I. 1991. Growth, weaning and maternal investment from a comparative perspective. Journal of Zoology, London, 225, 99–114CrossRef Google Scholar

Leigh, S. R. 1992. Patterns of variation in the ontogeny of primate body size dimorphism. Journal of Human Evolution, 23, 27–50CrossRef Google Scholar

Leigh, S. R. 1995. Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates. American Journal of Physical Anthropology, 97, 339–56CrossRef Google Scholar PubMed

Leigh, S. R. 2001. Evolution of human growth. Evolutionary Anthropology, 10, 223–36CrossRef Google Scholar

Leigh, S. R. & Shea, B. T. 1995. Ontogeny and the evolution of adult body size dimorphism in apes. American Journal of Primatology, 36, 37–60CrossRef Google Scholar

Leigh, S. R. & Pereira, M. E. 2003. Modes of primate development. In Primate Life Histories and Socioecology, ed. P. M. Kappeler & M. E. Pereira. Chicago, IL: University of Chicago Press, pp. 149–76

Leigh, S. R. & Terranova, C. J. 1998. Comparative perspectives on bimaturism, ontogeny, and dimorphism in lemurid primates. International Journal of Primatology, 19, 723–49CrossRef Google Scholar

Liang, B., Zhang, S. Y. & Wang, L. X. 2000. Development of sexual morphology, physiology and behaviour in Sichuan golden monkeys, Rhinopithecus roxellana. Folia Primatologica, 71, 413–16CrossRef Google Scholar PubMed

Lunn, S. F., Recio, R., Morris, K. & Fraser, H. M. 1994. Blockade of the neonatal rise in testosterone by a gonadotrophin-releasing hormone antagonist: effects on timing of puberty and sexual behaviour in the male marmoset monkey. Journal of Endocrinology, 141, 439–47CrossRef Google Scholar PubMed

Lycett, J. E., Dunbar, R. I. M. & Volland, E. 2000. Longevity and the cost of reproduction in a historical human population. Proceedings of the Royal Society of London, Series B, 267, 2355–8CrossRef Google Scholar

Maggioncalda, A. N., Sapolsky, R. M. & Czekala, N. M. 1999. Reproductive hormone profiles in captive male orangutans: implications for understanding developmental arrest. American Journal of Physical Anthropology, 109, 19–323.0.CO;2-3>CrossRef Google Scholar PubMed

Malina, R. M. 1978. Adolescent growth and maturation: selected aspects of current research. Yearbook of Physical Anthropology, 21, 63–94Google Scholar

Mann, D. R., Gould, K. G., Collins, D. C. & Wallen, K. 1989. Blockade of neonatal activation of the pituitary testicular axis: effect on peripubertal luteinizing hormone and testicular secretion and on testicular development in male monkeys. Journal of Clinical Endocrinology and Metabolism, 68, 600–7CrossRef Google Scholar PubMed

Mann, D. R., Akinbami, M. A., Gould, K. G., Paul, K. & Wallen, K. 1998. Sexual maturation in male rhesus monkeys: importance of neonatal testosterone exposure and social rank. Journal of Endocrinology, 159, 493–501CrossRef Google Scholar

Martin, P. S. 1984. The meaning of weaning. Animal Behaviour, 32, 1257–9CrossRef Google Scholar

Martin, R. D, Wilner, L. A. & Dettling, A. 1994. The evolution of sexual size dimorphism in primates. In The Differences Between the Sexes, ed. R. V. Short & E. Balaban. Cambridge: Cambridge University Press, pp. 159–200

Nadler, R. D., Wallis, J., Rothmeyer, C., Cooper, R. W. & Baulieu, E. E. 1987. Hormones and behavior of prepubertal and peripubertal chimpanzees. Hormones and Behaviour, 21, 118–31CrossRef Google Scholar PubMed

Nash, L. T. 1993. Juveniles in nongregarious primates. In Juvenile Primates: Life History, Development, and Behavior, ed. M. E. Pereira & L. A. Fairbanks. New York, NY: Oxford University Press, pp. 119–37

Nielson, C. T., Skakkebaek, N. E., Richardson, D. W.et al. 1986. Onset of the release of spermatozoa spermarche in boys in relation to age, testicular growth, pubic hair and height. Journal of Clinical Endocrinology and Metabolism, 62, 532–5CrossRef Google Scholar

Nieuwenhuijsen, K., Bonke-Jansen, M., Neef, K. J., Werff ten Bosch, J. J. & Slob, A. K. 1987a. Physiological aspects of puberty in group-living stump-tail monkeys, Macaca arctoides. Physiology and Behavior, 41, 37–45CrossRef Google Scholar

Nieuwenhuijsen, K., Neef, K. J., Werff den Bosch, J. J. & Slob, A. K. 1987b. Testosterone, testes size, seasonality and behaviour in group living stump-tail macaques, Macaca arctoides. Hormones and Behavior, 21, 153–67CrossRef Google Scholar

Nikolei, J. & Borries, C. 1997. Sex differential behaviour of immature hanuman langurs, Presbytis entellus, in Ramnagar, South Nepal. International Journal of Primatology, 18, 415–37CrossRef Google Scholar

Nigi, H., Tiba, T., Yamamoto, S., Floescheim, Y. & Ohsawa, N. 1980. Sexual maturation and seasonal changes in the reproductive phenomena of female Japanese monkeys. Primates, 21, 230–40CrossRef Google Scholar

Partridge, L. 1988. Lifetime reproductive success in Drosophila. In Reproductive Success, ed. T. H. Clutton-Brock. Chicago, IL: University of Chicago Press, pp. 11–23

Paul, A. & Thommen, D. 1984. Timing of birth, female reproductive success and infant sex ratio in semifree-ranging Barbary macaques, Macaca sylvanus. Folia Primatologica, 42, 2–16CrossRef Google Scholar

Pereira, M. E. 1988. Effects of age and sex on intra-group spacing behaviour in juvenile savannah baboons, Papio cynocephalus cynocephalus. Animal Behavior, 36, 184–204CrossRef Google Scholar

Pereira, M. E. 1995. Development and social dominance among group-living primates. American Journal of Primatology, 37, 143–75CrossRef Google Scholar

Pereira, M. E. & Altmann, J. 1985. Development of social behaviour in free-living non-human primates. In Nonhuman Primate Models for Human Growth and Development, ed. E. Watts. New York, NY: Alan R. Liss, pp. 217–309

Pereira, M. E. & Fairbanks, L. A. (eds.) 1993. Juvenile Primates: Life History, Development, and Behavior. New York, NY: Oxford University Press

Pereira, M. E. & Leigh, S. R. 2003. Modes of primate development. In Primate Life History and Socioecology, ed. P. M. Kappeler & M. E. Pereira, in press. Chicago, IL: University of Chicago Press

Phillips-Conr oy, J. E., Bergman, T. & Jolly, C. J. 2000. Quantitative assessment of occlusal wear and age estimation in Ethiopian and Tanzanian baboons. In Old World Monkeys, ed. P. F. Whitehead & C. J. Jolly. Cambridge: Cambridge University Press, pp. 321–40

Plant, T. M. 1994. Puberty in primates. In The Physiology of Reproduction, Vol. 2, ed. E. Knobil & J. D. Neill. New York, NY: Raven Press, pp. 1763–88

Plavcan, J. M. 1999. Mating systems, intrasexual competition and sexual dimorphism in primates. In Comparative Primate Socioecology, ed. P. C. Lee. Cambridge: Cambridge University Press, pp. 241–69

Pontier, D., Gaillard, J. M., Allaine, D.et al. 1989. Postnatal-growth rate and adult body-weight in mammals – a new approach. Oecologia, 80, 390–4CrossRef Google Scholar PubMed

Promislow, D. E. L. & Harvey, P. H. 1990. Living fast and dying young: a comparative analysis of life history variation among mammals. Journal of Zoology, London, 220, 417–38CrossRef Google Scholar

Pusey, A. E. 1990. Behavioural changes at adolescence in chimpanzees. Behaviour, 115, 203–46CrossRef Google Scholar

Pusey, A. E. & Packer, C. 1987. Dispersal and philopatry. In Primate Societies, ed. B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham & T. T. Struhsaker. Chicago, IL: University of Chicago Press, pp. 250–66

Raleigh, M. J. & MacGuire, M. T. 1990. Social influences on endocrine function in male vervet monkeys. In Socioendo-crinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley-Liss, pp. 95–111

Ross, C. & Jones, K. E. 1999. Socioecology and the evolution of primate reproductive rates. In Comparative Primate Socioecology, ed. P. C. Lee. Cambridge: Cambridge University Press, pp. 73–110

Rowell, T. E. 1977. Variation in age at puberty in monkeys. Folia Primatologica, 27, 284–90CrossRef Google Scholar PubMed

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, 419–34CrossRef Google Scholar PubMed

Sapolsky, R. I. M. 1985. Stress-induced suppression of testicular function in the wild baboon – role of glucocorticoids. Endocrinology, 116, 2273–8CrossRef Google Scholar PubMed

Sapolsky, R. I. M. 1993. The physiology of dominance in stable vs. unstable hierarchies. In Primate Social Conflict, ed. W. Mason & S. Mendoza. New York, NY: State University of New York Press, pp. 171–204

Scanlan, J. M., Coe, C. L., Latts, A. & Suomi, S. J. 1987. Effects of age, rearing, and separation stress on immunoglobulin levels in rhesus monkeys. American Journal of Primatology, 13, 11–22CrossRef Google Scholar

Schultz, A. H. 1956. Postembryonic changes. Primatologia, 1, 887–964Google Scholar

Schultz, A. H. 1969. The Life of Primates. New York, NY: Universe Books

Schwartz, S. M. & Kemnitz, H. W. 1992. Age-related and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques. American Journal of Physical Anthropology, 89, 109–21CrossRef Google Scholar PubMed

Schwartz, S. M., Wilson, M. E., Walker, M. L. & Collins, D. C. 1988. Dietary influences on growth and sexual maturation in premenarchial rhesus monkeys. Hormones and Behavior, 22, 231–51CrossRef Google Scholar PubMed

Scott, L. 1984. Reproductive behavior of adolescent female baboons, Papio anubis, in Kenya. In Female Primates: Studies by Women Primatologists, ed. M. F. Small. New York, NY: Alan R Liss, pp. 77–100

Setchell, J. M. 1999. Socio-sexual development in the male mandrill Mandrillus sphinx. Ph. D. thesis, University of Cambridge

Setchell, J. M. 2003. The evolution of alternative reproductive morphs in male primates. In Sexual Selection and Reproductive Competition in Primates: New Perspectives and Directions, ed. C. B. Jones, in press. American Society of Primatologists Special Topics in Primatology

Setchell, J. M. & Dixson, A. F. 2001a. Arrested development of secondary sexual adornments in subordinate adult male mandrills, Mandrillus sphinx. American Journal of Physical Anthropology, 115, 245–52CrossRef Google Scholar

Setchell, J. M. & Dixson, A. F. 2001b. Changes in the secondary sexual adornments of male mandrills Mandrillus sphinx are associated with gain and loss of alpha status. Hormones and Behavior, 39, 177–84CrossRef Google Scholar

Setchell, J. M. & Dixson, A. F. 2002. Developmental variables and dominance rank in male mandrills Mandrillus sphinx. American Journal of Primatology, 56, 9–25CrossRef Google Scholar PubMed

Setchell, J. M., Lee, P. C., Wickings, E. J. & Dixson, A. F. 2001. Growth and ontogeny of sexual size dimorphism in the mandrill Mandrillus sphinx. American Journal of Physical Anthropology, 115, 349–60CrossRef Google Scholar PubMed

Setchell, J. M., Lee, P. C., Wickings, E. J. & Dixson, A. F. 2002. Reproductive parameters and maternal investment in mandrills Mandrillus sphinx. International Journal of Primatology, 23, 51–68CrossRef Google Scholar

Shea, B. T. 1983. Allometry and heterochrony in the African apes. American Journal of Physical Anthropology, 62, 275–89CrossRef Google Scholar PubMed

Shea, B. T. 1986. Ontogenetic approaches to sexual dimorphism in anthropoids. Human Evolution, 1, 97–110CrossRef Google Scholar

Shea, B. T. 2000. Current issues in the investigation of evolution by heterochrony, with emphasis on the debate over human neotony. In Biology, Brains and Behaviour, ed. S. Taylor Parker, J. Langer & M. L. McKinney. Santa Fe: School of American Research Press, pp. 181–214

Small, M. F. & Smith, D. G. 1986. The influence of birth timing upon infant growth and survival in captive rhesus macaques, Macaca mulatta. International Journal of Primatology, 7, 289–304CrossRef Google Scholar

Smith, B. H. 1992. Life history and the evolution of human maturation. Evolutionary Anthropology, 14, 134–42Google Scholar

Smith, B. H., Crummett, T. L. & Brandt, K. L. 1994. Ages of eruption of primate teeth: a compendium for ageing individuals and comparing life histories. Yearbook of Physical Anthropology, 37, 177–231CrossRef Google Scholar

Smith, R. J. & Jungers, W. L. 1997. Body mass in comparative primatology. Journal of Human Evolution, 32, 523–59CrossRef Google Scholar PubMed

Smith, R. J. & Leigh, S. R. 1998. Sexual dimorphism in primate neonatal body mass. Journal of Human Evolution, 34, 173–201CrossRef Google Scholar PubMed

Sommer, V. & Rajpurohit, L. S. 1989. Male reproductive success in harem troops of Hanuman langurs, Presbytis entellus. International Journal of Primatology, 10, 293–317CrossRef Google Scholar

Stanford, C. B. 1998. Chimpanzee and Red Colobus: The Ecology of Predator and Prey. Cambridge, MA: Harvard University Press

Strum, S. C. 1991. Weight and age in wild olive baboons. American Journal of Primatology, 25, 219–37CrossRef Google Scholar

Strum, S. C. & Western, J. D. 1982. Variations in fecundity with age and environment in olive baboons, Papio anubis. American Journal of Primatology, 3, 61–76CrossRef Google Scholar

Surbey, M. K. 1990. Family composition, stress and the timing of human menarche. In Socioendocrinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley Liss, pp. 11–32

Tanner, J. M. 1962. Growth at Adolescence. Oxford: Blackwell

Treves, A. 1997. Primate natal coats: a preliminary analysis of distribution and function. American Journal of Physical Anthropology, 104, 47–703.0.CO;2-A>CrossRef Google Scholar PubMed

Trillmich, F. 1996. Parental investment in pinnipeds. In Parental Care: Evolutionary Mechanisms and Adaptive Significance, ed. J. S. Rosenblatt & C. T. Snowdon. London: Academic Press, pp. 533–77

Trivers, R. M. 1985. Social Evolution. Menlo Park, CA: Benjamin Cummings

Utami, S. S., Goossens, B., Bruford, M. W., Ruiter, J. & Hooff, J. A. R. A. M. 2002. Male bimaturism and reproductive success in Sumatran orangutans. Behavioral Ecology, 13, 643–52CrossRef Google Scholar

Vandenbergh, J. G. & Coppola, D. M. 1986. The physiology and ecology of puberty modulation by primer pheromones. Advances in the Study of Behavior, 16, 71–107CrossRef Google Scholar

Vandenbergh, J. G., Drickamer, L. C. & Colby, D. R. 1972. Social and dietary factors in the sexual maturation of female mice. Journal of Reproduction and Fertility, 28, 515–23CrossRef Google Scholar PubMed

Noordwijk, M. A. & Schaik, C. P. 2001. Career moves: transfer and rank challenge decisions by male long-tailed macaques. Behaviour, 138, 359–95CrossRef Google Scholar

Schaik, C. P. 1992. Sex-biased juvenile mortality in primates: a reply to Hauser & Harcourt. Folia Primatologica, 58, 53–5CrossRef Google Scholar PubMed

Schaik, C. P. & Visser, J. A. G. M. 1990. Fragile sons or harassed daughters? Sex differences in mortality among juvenile primates. Folia Primatologica, 55, 10–23CrossRef Google Scholar PubMed

Schaik, C. P. & Hrdy, S. B. 1991. Intensity of local resource competition shapes the relationship between maternal rank and sex ratios at birth in Cercopithecine primates. American Naturalist, 138, 1555–61CrossRef Google Scholar

van Schaik, C. P. & Janson, C. H. (eds.) 2000. Infanticide by Males and Its Implications. Cambridge: Cambridge University Press

Watts, E. S. 1985. Adolescent growth and development of monkeys, apes and humans. In Nonhuman Primate Models for Human Growth and Development, ed. E. S. Watts. New York, NY: Liss, pp. 41–65

Watts, E. S. 1986. Evolution of the human growth spurt. In Human Growth, ed. F. Falkner & J. M. Tanner. New York, NY: Plenum, pp. 153–66

Whitten, P. L., Brockman, D. K. & Stavisky, R. C. 1998. Recent advances in noninvasive techniques to monitor hormone–behavior interactions. Yearbook of Physical Anthropology, 41, 1–233.0.CO;2-H>CrossRef Google Scholar

Wickings, E. J. & Dixson, A. F. 1992. Development from birth to sexual maturity in a semi-free-ranging colony of mandrills, Mandrillus sphinx in Gabon. Journal of Reproduction and Fertility, 95, 129–38CrossRef Google Scholar

Wiley, R. H. 1974. Effects of delayed reproduction on survival, fecundity, and the rate of population increase. American Naturalist, 108, 705–9CrossRef Google Scholar

Wilner, L. A. & Martin, R. D. 1985. Some basic principles of mammalian sexual dimorphism. In Human Sexual Dimorphism, ed. J. Ghesquiere, R. D. Martin & F. Newcombe. London: Taylor & Francis, pp. 1–42

Worthman, C. M. 1993. Biocultural interactions in human development. In Juvenile Primates: Life History, Development, and Behavior, ed. M. E. Pereira & L. A. Fairbanks. New York, NY: Oxford University Press, pp. 339–58

Ziegler, T. E., Snowdon, C. T. & Uno, H. 1990. Social interactions and determinants of ovulation in tamarins, Saguinus. In Monographs in Primatology. Vol. 13: Socioendocrinology of Primate Reproduction, ed. T. E. Ziegler & F. B. Bercovitch. New York, NY: Wiley Liss, pp. 113–33