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7 - Growth and sexual maturation in human and non-human primates: a brief review

Published online by Cambridge University Press:  16 May 2011

Phyllis C. Lee
Affiliation:
University of Stirling, UK
C. G. Nicholas Mascie-Taylor
Affiliation:
University of Cambridge
Lyliane Rosetta
Affiliation:
Centre National de la Recherche Scientifique (CNRS), Paris
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Summary

Introduction

“…adult size can be reached through many pathways involving timing differences and rate differences.”

(Leigh, 2001, p. 236)

If there are indeed many pathways to the adult endpoint during growth, what becomes of interest is the nature of those different pathways and, more significantly, the consequences of differences in pathways for early survival, for the timing of the onset of reproductive activity, and for subsequent lifespan. This chapter explores some of the strategies for growth observed in primates, and outlines potential consequences of these strategies. I do this in the context of an abundance of detailed literature on growth rates, growth constraints and models of rates of growth for humans (see for example Bogin, 1999) and non-human primates (e.g. Leigh, 1996). Models of growth can provide explanations for primate life history variation (Leigh, 1995; Dirks & Bowman, 2007) and, in addition, potentially elucidate the variation that exists at the level of the individual and population between rapid and late maturation (e.g. Wilson et al., 1983; Bercovitch & Berard, 1993; Setchell et al., 2001; Altmann & Alberts, 2005).

Physical maturation is obviously a consequence of growth, but the timing of physiological or hormonal reproductive onset, rather than simply attained size, determines much of the subsequent reproductive success of the individual. Early reproduction, combined with high survival, provides significant advantages in terms of lifetime reproductive success.

Type
Chapter
Information
Reproduction and Adaptation
Topics in Human Reproductive Ecology
, pp. 128 - 148
Publisher: Cambridge University Press
Print publication year: 2011

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References

Altmann, S. A. (1991). Diets of yearling female primates (Papio cynocephalus) predict lifetime fitness. Proceedings of the National Academy of Sciences of the United States of America, 88, 420–3.CrossRefGoogle ScholarPubMed
Altmann, J. & Alberts, S. C. (2005). Growth rates in a wild primate population: ecological influences and maternal effects. Behavioral Ecology and Sociobiology, 57, 490–501.CrossRefGoogle Scholar
Altmann, J. & Samuels, A. (1992). Costs of maternal care: infant carrying in baboons. Behavioral Ecology and Sociobiology, 29, 391–8.CrossRefGoogle Scholar
Altmann, J., Schoeller, D., Altmann, S. A., Murithi, P. & Sapolsky, R. M. (1993). Body size and fatness of free-living baboons reflect food availability and activity levels. American Journal of Primatology, 30, 149–61.CrossRefGoogle Scholar
Barker, D. J. (2001). The malnourished baby and infant. British Medical Bulletin, 60, 69–88.CrossRefGoogle ScholarPubMed
Belsky, J., Steinberg, L. D., Houts, R. M.et al. (2007). Family-rearing antecedents of pubertal timing. Child Development, 78, 1302–21.CrossRefGoogle ScholarPubMed
Bercovitch, F. B. & Berard, J. D. (1993). Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behavioral Ecology and Sociobiology, 32, 103–9.CrossRefGoogle Scholar
Bercovitch, F. B. & Strum, S. C. (1993). Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behavioral Ecology and Sociobiology, 33, 313–18.CrossRefGoogle Scholar
Bernstein, R. M., Leigh, S. R., Donovan, S. M. & Monaco, M H. (2008). Hormonal correlates of ontogeny in baboons (Papio hamadryas anubis) and mangabeys (Cercocebus atys). American Journal of Physical Anthropology, 136, 156–68.CrossRefGoogle Scholar
Bogin, B. (1999). Patterns of Human Growth (2nd ed.). Cambridge: Cambridge University Press.Google ScholarPubMed
Bowman, J. E. & Lee, P. C. (1995). Growth and threshold-weaning weights among captive rhesus macaques. American Journal of Physical Anthropology, 96, 159–75.CrossRefGoogle ScholarPubMed
Charnov, E. L. (1993). Life History Invariants. Oxford: Oxford University Press.Google Scholar
Charpentier, M. J. E., Tung, J., Altmann, J. & Alberts, S. C. (2008). Age at maturity in wild baboons: genetic, environmental and demographic influences. Molecular Ecology, 17, 2026–40.CrossRefGoogle ScholarPubMed
Chowdhury, S., Shahabuddin, A. K., Seal, A. J.et al. (2000). Nutritional status and age at menarche in a rural area of Bangladesh. Annals of Human Biology, 27, 249–56.Google Scholar
Clutton-Brock, T. H., Albon, S. & Guinness, R. (1982). The Red Deer: The Ecology of Two Sexes. Princeton: Princeton University Press.Google Scholar
Cooper, G., Kuh, D., Egger, P., Wadsworth, M. & Barker, D. J. P. (1996). Childhood growth and age at menarche. British Journal of Obstetrics and Gynecology, 103, 814–17.CrossRefGoogle ScholarPubMed
Dirks, W. & Bowman, J. E. (2007). Life history theory and dental development in four species of catarrhine primates. Journal of Human Evolution, 55, 309–20.CrossRefGoogle Scholar
dos Santos Silva, I., Stavola, B. L., Mann, V.et al. (2002). Prenatal factors, childhood growth trajectories and age at menarche. International Journal of Epidemiology, 31, 405–12.CrossRefGoogle ScholarPubMed
Euling, S. Y., Herman-Giddens, M. E., Lee, P. A.et al. (2008). Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics, 121 (Suppl. 3), S172–91.CrossRefGoogle ScholarPubMed
Fairbanks, L. A. & McGuire, M. T. (1996). Maternal condition and the quality of maternal care in vervet monkeys. Behaviour, 132, 733–54.CrossRefGoogle Scholar
Fowden, A. L., Giussani, D. A. & Forhead, A. J. (2006). Intrauterine programming of physiological systems: causes and consequences. Physiology, 21, 29–37.CrossRefGoogle ScholarPubMed
Frisch, R. E. (1987). Body fat, menarche, fitness and fertility. Human Reproduction, 2, 521–33.CrossRefGoogle ScholarPubMed
Garcia, C., Lee, P. C. & Rosetta, L. (2006). Dominance and reproductive rates in captive female olive baboons, Papio anubis. American Journal of Physical Anthropology, 131, 64–72.CrossRefGoogle ScholarPubMed
Garcia, C., Lee, P. C. & Rosetta, L. (2009). Growth in colony-living anubis baboon infants and its relationship with maternal activity budgets and reproductive status. American Journal of Physical Anthropology, 138, 123–35.CrossRefGoogle ScholarPubMed
Gesquiere, L. R., Altmann, J., Khan, M. Z.et al. (2005). Coming of age: steroid hormones of wild immature baboons (Papio cynocephalus). American Journal of Primatology, 67, 83–100.CrossRefGoogle Scholar
Gomendio, M. (1989). Differences in fertility and suckling patterns between primiparous and multiparous rhesus mothers (Macaca mulatta). Journal of Reproduction and Fertility, 87, 529–42.CrossRefGoogle Scholar
Gurven, M. & Walker, R. (2006). Energetic demand of multiple dependents and the evolution of slow human growth. Proceedings of the Royal Society B, 273, 835–41.CrossRefGoogle ScholarPubMed
Gurven, M., Kaplan, H. & Gutierrez, M. (2006). How long does it take to become a proficient hunter? Implications for the evolution of extended development and long life span. Journal of Human Evolution, 51, 454–70.CrossRefGoogle ScholarPubMed
Hauser, M. D. & Fairbanks, L. A. (1988). Mother–offspring conflict in vervet monkeys: variation in response to ecological conditions. Animal Behaviour, 36, 802–13.CrossRefGoogle Scholar
Hamel, S., Côté, S. D., Gaillard, J. M. & Festa-Bianchet, M. (2009). Individual variation in reproductive costs of reproduction: high-quality females always do better. Journal of Animal Ecology, 78, 143–51.CrossRefGoogle ScholarPubMed
Heger, S., Körner, A., Meigen, C.et al. (2008). Impact of weight status on the onset and parameters of puberty: analysis of three representative cohorts from central Europe. Journal of Pediatric Endocrinology & Metabolism, 21, 865–77.CrossRefGoogle ScholarPubMed
Helle, S., Lummaa, V. & Jokela, J. (2005). Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women. Proceedings of the Royal Society B, 272, 29–37.CrossRefGoogle Scholar
Janson, C. H. & 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. Pereira, M. E. and Fairbanks, L.A., pp. 57–74. Oxford: Oxford University Press.Google Scholar
Johnson, S. E. (2006). Maternal characteristics and offspring growth in chacma baboons: A life-history perspective. In Reproduction and Fitness in Baboons: Behavioral, Ecological, and Life History Perspectives, ed. Swedell, L. and Leigh, S. R., pp. 177–97. New York, NY: Springer.CrossRefGoogle Scholar
Juul, A., Teilmann, G., Scheike, T., et al. (2006). Pubertal development in Danish children: comparison of recent European and US data. International Journal of Andrology, 29, 247–55.CrossRefGoogle ScholarPubMed
Kappeler, P. M. & Heymann, E. (1996). Nonconvergence in the evolution of primate life history and socio-ecology. Biological Journal of the Linnean Society, 59, 297–326.CrossRefGoogle Scholar
Kelley, J. (2002). Life-history evolution in Miocene and extant apes. In Human Evolution Through Developmental Change, ed. Minugh-Purvis, N. and McNamara, K. J., pp. 223–48. Baltimore, MD: Johns Hopkins University Press.Google Scholar
Kennedy, G. E. (2005). From the ape's dilemma to the weanling's dilemma: early weaning and its evolutionary context. Journal of Human Evolution, 48, 123–45.CrossRefGoogle ScholarPubMed
Kozlowski, J. & Weiner, J. (1997). Interspecific allometries are by-products of body-size optimization. American Naturalist, 149, 352–80.CrossRefGoogle Scholar
Kramer, K.L. (2008). Early sexual maturity among Pumé foragers of Venezuela: fitness implications of teen motherhood. American Journal of Physical Anthropology, 136, 338–50.CrossRefGoogle ScholarPubMed
Kurita, H., Shimomura, T. & Fujita, T. (2002). Temporal variation in Japanese macaque bodily mass. International Journal of Primatology, 23, 411–28.CrossRefGoogle Scholar
Lee, P. C. (1983). Effects of parturition on the mother's relationship with older offspring. In Primate Social Relationships: An Integrated Approach, ed. Hinde, R. A., pp. 134–9. Oxford: Blackwell Scientific.Google Scholar
Lee, P. C. (1984). Ecological constraints on the social development of vervet monkeys. Behaviour, 91, 245–62.CrossRefGoogle Scholar
Lee, P. C. (1996). The meaning of weaning: growth, lactation, and life history. Evolutionary Anthropology, 5, 87–96.3.0.CO;2-T>CrossRefGoogle Scholar
Lee, P. C. (1999). Comparative ecology of postnatal growth and weaning among haplorhine primates. In Comparative Primate Socioecology, ed. Lee, P. C., pp. 111–39. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Lee, P. C. & Kappeler, P. M. (2003). Socio-ecological correlates of phenotypic plasticity in primate life history. In: Primate Life Histories, ed. Kappeler, P. M. and Pereira, M., pp. 41–65. Chicago, IL: University of Chicago Press.Google Scholar
Lee, P. C., Majluf, P. & Gordon, I. J. (1991). Growth, weaning and maternal investment from a comparative perspective. Journal of Zoology, 225, 99–114.CrossRefGoogle Scholar
Lee, P. C. & Moss, C. J. (1995). Statural growth in known-age African elephants (Loxodonta africana). Journal of Zoology, 236, 29–41.CrossRefGoogle Scholar
Leigh, S. R. (1995). Socioecology and the ontogeny of sexual size dimorphism in anthropoid primates. American Journal of Physical Anthropology, 97, 339–56.CrossRefGoogle ScholarPubMed
Leigh, S. R. (1996). Evolution of human growth spurts. American Journal of Physical Anthropology, 101, 455–74.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Leigh, S. R. (2001). Evolution of human growth. Evolutionary Anthropology 10, 223–36.CrossRefGoogle Scholar
Leigh, S. R. (2004). Brain growth, life history, and cognition in primate and human evolution. American Journal of Primatology, 62, 139–64.CrossRefGoogle ScholarPubMed
Leigh, S. R. & Park, P. B. (1998). Evolution of human growth prolongation. American Journal of Physical Anthropology, 107, 331–50.3.0.CO;2-#>CrossRefGoogle ScholarPubMed
Leigh, S. R., Shahb, N. F. & Buchanan, L. S. (2003). Ontogeny and phylogeny in papionin primates. Journal of Human Evolution, 45, 285–316.CrossRefGoogle ScholarPubMed
Mangel, M. & Munch, S. B. (2005). A life-history perspective on short- and long-term consequences of compensatory growth. American Naturalist, 166, E155–76.CrossRefGoogle Scholar
Martin, R. D. (1996). Scaling of the mammalian brain: the maternal energy hypothesis. News in Physiological Sciences, 11, 149–56.Google Scholar
Martin, R. D. & MacLarnon, A. M. (1985). Gestation period, neonatal size, and maternal investment in placental mammals. Nature, 313, 220–3.CrossRefGoogle Scholar
Martin, R., Willner, L. & Dettling, A. (1994). The evolution of sexual size dimorphism in primates. In The Differences Between the Sexes, ed. Short, R. and Balabar, E., pp. 159–200. Cambridge: Cambridge University Press.Google ScholarPubMed
McLaren, I. A. (1993). Growth in pinnipeds. Biological Reviews of the Cambridge Philosophical Society, 68, 1–79.CrossRefGoogle ScholarPubMed
Nieuwenhuijsen, K., Bonke-Jansen, M., Neef, K. J., Werff ten Bosch, J. J. & Slob, A. K. (1987). Physiological aspects of puberty in group-living stumptail monkeys (Macaca arctoides). Physiology & Behavior, 41, 37–45.CrossRefGoogle Scholar
Núñez-de la Mora, A., Chatterton, R. T., Choudhury, O. A., Napolitano, D. A. & Bentley, G. R. (2007). Childhood conditions influence adult progesterone levels. PLoS Medicine, 4, 813–21.CrossRefGoogle ScholarPubMed
Ojeda, S. R., Lomniczi, A., Mastroniardi, C.et al. (2006). Minireview: the neuroendocrine regulation of puberty: is the time ripe for a systems biology approach? Endocrinology, 147, 1166–74.CrossRefGoogle ScholarPubMed
Painter, R. C., Osmond, C., Gluckman, P.et al. (2008). Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life. British Journal of Obstetrics and Gynaecology, 115, 1243–9.CrossRefGoogle ScholarPubMed
Patterson, J. L., Ball, R. O., Willis, H. J., Aherne, F. X. & Foxcroft, G. R. (2002). The effect of lean growth rate on puberty attainment in gilts. Journal of Animal Science, 80, 1299–310.CrossRefGoogle ScholarPubMed
Periera, M. E. & Leigh, S. R. (2002). Modes of primate development. In Primate Life Histories, ed. Kappeler, P.M. and Pereira, M., pp. 149–79. Chicago, IL: University of Chicago Press.Google Scholar
Pusey, A. E., Oehlert, G. W., Williams, J. M. & Goodall, J. (2003). Influence of ecological and social factors on body mass of wild chimpanzees. International Journal of Primatology, 26, 3–31.CrossRefGoogle Scholar
Roche, A. & Sun, S. (2003). Human Growth: Assessment and Interpretation. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Rosendo, A., Druet, T., Gogué, J., Canario, L. & Bidanel, J. P. (2007). Correlated responses for litter traits to six generations of selection for ovulation rate or prenatal survival in French Large White pigs. Journal of Animal Science, 85, 1615–24.CrossRefGoogle ScholarPubMed
Ross, C. (1988). The intrinsic rate of natural increase and reproductive effort in primates. Journal of Zoology, 214, 199–219.CrossRefGoogle Scholar
Ross, C. (1998). Primate life histories. Evolutionary Anthropology, 6, 54–63.3.0.CO;2-W>CrossRefGoogle Scholar
Sellen, D. W. (2001). Comparison of infant feeding patterns reported for non-industrial populations with current recommendations. Journal of Nutrition, 131, 2707–15.CrossRefGoogle Scholar
Sellen, D. & Smay, D. (2000). Relationship between subsistence and age at weaning in “preindustrial” societies. Human Nature, 12, 47–87.CrossRefGoogle Scholar
Setchell, J. M. (2003). Behavioural development in male mandrills (Mandrillus sphinx): puberty to adulthood. Behaviour, 140, 1053–89.CrossRefGoogle Scholar
Setchell, J. & Lee, P. C. (2004). Development and sexual selection in primates. In Sexual Selection in Primates: Causes, Mechanisms and Consequences, ed. Kappeler, P. M. and Schaik, C. P., pp. 175–95. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Setchell, J., Lee, P. C., Wickings, E. & Dixson, A. (2001). Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx). American Journal of Physical Anthropology, 115, 349–60.CrossRefGoogle ScholarPubMed
Setchell, J., Lee, P. C., Wickings, E. & Dixson, A. (2002). Reproductive parameters in female mandrills (Mandrillus sphinx). International Journal of Primatology, 23, 51–68.CrossRefGoogle Scholar
Skuse, D., Wolke, D., Reilly, S. & Chan, I. (1995). Failure to thrive in human infants: the significance of maternal well-being and behaviour. In Motherhood in Human and Nonhuman Primates, ed. Pryce, C. R., Marin, R. D. and Skuse, D., pp. 162–70, Basel: Karger.Google Scholar
Smucny, D. A., Abbott, D. H., Mansfield, K. G.et al. (2004). Reproductive output, maternal age, and survivorship in captive common marmoset females (Callithrix jacchus). American Journal of Primatology, 64, 107–21.CrossRefGoogle Scholar
Stearns, S. C. (1992). The Evolution of Life Histories. Oxford: Oxford University Press.Google Scholar
Ulijaszek, S. J. (2002). Serum insulin-like growth factor-I, insulin-like growth factor binding protein-3, and the pubertal growth spurt in the female rhesus monkey. American Journal of Physical Anthropology, 118, 77–85.CrossRefGoogle ScholarPubMed
Utami-Atmoko, S. S. & Hooff, J. A. R. A. M. (2004). Alternative male reproductive strategies: male bimaturism in orangutans. In Sexual Selection in Primates: New and Comparative Perspectives, ed. Kappeler, P. M. and Schaik, C. P., pp. 196–207. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Noordwijk, M. A. & Schaik, C. P. (2004). Development of ecological competence in Sumatran orangutans. American Journal of Physical Anthropology, 127, 79–94.CrossRefGoogle Scholar
Watson, J. C., Payne, R. C., Chamberlain, A. T., Jones, R. K. & Sellers, W. I. J. (2008). The energetic costs of load-carrying and the evolution of bipedalism. Human Evolution, 54, 675–83.CrossRefGoogle ScholarPubMed
Wells, J. C. K. (2006). The role of cultural factors in human breastfeeding: adaptive behaviour or biopower? Human Ecology, Special Issue No. 14, 39–47.
Wilner, L. A. & Martin, R. D. (1985). Some basic principles of mammalian sexual dimorphism. In Human Sexual Dimorphism, ed. Ghesquiere, J., Martin, R. D. and Newcombe, F., pp. 1–42. London: Taylor and Francis.Google Scholar
Wilson, M. E. (1997). Administration of IGF-I affects the GH axis and adolescent growth in normal monkeys. Journal of Endocrinology, 153, 327–35.CrossRefGoogle ScholarPubMed
Wilson, M. E. (1998). Premature elevation in serum insulin-like growth factor-I advances first ovulation in rhesus monkeys. Journal of Endocrinology, 158, 247–57.CrossRefGoogle ScholarPubMed
Wilson, M. E. & Kinkead, B. (2008). Gene–environment interactions, not neonatal growth hormone deficiency, time puberty in female rhesus monkeys. Biology of Reproduction, 78, 736–43.CrossRefGoogle Scholar
Wilson, M. E., Walker, M. L. & Gordon, T. P. (1983). Consequences of first pregnancy in rhesus monkeys. American Journal of Physical Anthropology, 61, 103–10.CrossRefGoogle ScholarPubMed
Wilson, M. E., Walker, M. L.,Pope, N. S. & Gordon, T. P. (1988). Prolonged lactational infertility in adolescent rhesus monkeys. Biology of Reproduction, 38, 163–74.CrossRefGoogle ScholarPubMed
Wrangham, R., Jones, J., Laden, G., Pilbeam, D. & Conklin-Brittain, N. (1999). The raw and the stolen: cooking and the ecology of human origins. Current Anthropology, 40, 567–94.Google ScholarPubMed
Wyshak, G. & Frisch, R. E. (1982). Evidence of a secular trend in age of menarche. New England Journal of Medicine, 306, 1033–5.CrossRefGoogle ScholarPubMed

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