Ontogeny, Life History, and Maternal Investment in Baboons

  • Steven R. Leigh
  • Robin M. Bernstein
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Chapter Summary

This chapter compares the ontogeny of Papio baboons to other papionin primates through a theoretical perspective that prioritizes ontogeny in the study of life history. This viewpoint anticipates that life history variables are dissociable, or capable of responding to selection independent of one another. The result is diversity in how primate life histories unfold. Papio baboons provide excellent evidence for this view of life history, illustrating a mode of life history with clear ties to female reproduction. Specifically, relative to other papionins, life history in Papio baboons involves tightly coordinated patterns of development for somatic variables, including body mass, skeletal dimensions, and dental eruption. Growth hormones in Papio baboons are highly intercorrelated. However, brain growth follows a distinct pattern from other systems, ceasing very early in Papio baboons.

This life history mode reflects heavy metabolic burdens on baboon mothers to produce “high-quality” offspring that can cope with intense select during early postnatal development. Brain growth is dissociated from development of other somatic systems, inducing high maternal gestational costs, but possibly reflecting the neural capabilities to survive the infant period. These costs appear to have selectively favored an integrated pattern of somatic, dental, and hormonal development, along with large female adult size. Ties between reproduction and life history are integral to understanding baboon evolution.


Life History Rhesus Macaque Brain Size Brain Growth Maternal Investment 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alberts, S. C. and Altmann, J., 2002, Matrix models for primate life history analysis, in: Primate Life Histories and Socioecology, P. M. Kappeler and M. E. Pereira, eds., Unversity of Chicago Press, Chicago, pp. 66–102.Google Scholar
  2. Allman, J. and Hasenstaub, A., 1999, Brains, maturation times, and parenting, Neurobiol. Aging 20:447–454.PubMedCrossRefGoogle Scholar
  3. Altmann, J., 1980, Baboon Mothers and Infants, Harvard University Press, Cambridge, MA.Google Scholar
  4. Altmann, J., 1983, Costs of reproduction in baboons (Papio cynocephalus), in: Energetics: The Costs of Survival in Vertebrate, W. P. Aspey, and S. I. Lustick, eds., Ohio State University Press, Columbus, OH, pp. 67–88.Google Scholar
  5. Altmann, S. A., 1998, Foraging for Survival, University of Chicago Press, Chicago.Google Scholar
  6. Altmann, J. and Alberts, S. C., 1987, Body mass and growth rates in a wild primate population, Oecologia 72:15–20.CrossRefGoogle Scholar
  7. Altmann, J. and Alberts, S. C., 2003, Variability in reproductive success viewed from a life-history perspective in baboons, Am. J. Hum. Biol. 15:401–409.PubMedCrossRefGoogle Scholar
  8. Altmann, J., Altmann, S. A., Hausfater, G., and McCuskey, S. A., 1977, Life history of yellow baboons: Physical development, reproductive parameters, and infant mortality, Primates 18:315–330.CrossRefGoogle Scholar
  9. Altmann, J., Altmann, S. A., and Hausfater, G., 1978, Primate infant’s effects on mother’s future reproduction, Science 201:1028–1029.PubMedCrossRefGoogle Scholar
  10. Altmann, J., Altmann, S. A., and Hausfater, G., 1981, Physical maturation and age estimates of yellow baboons, Papio cynocephalus, in Amboseli National Park, Kenya, Am. J. Primatol. 1:389–399.CrossRefGoogle Scholar
  11. Altmann, J., Hausfater, G., Altmann, S. A., 1988, Determinates of reproductive success in savannah baboons (papio cynocephalus), in: Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems, T. H. Clutton-Brock, ed., University of Chicago Press, Chicago, pp. 403–418.Google Scholar
  12. Altmann, J., Schoeller, D., Altmann, S. A., Muruthi, P. and Sapolsky, R. M., 1993, Body size and fatness of free-living baboons reflect food availability and activity levels, Am. J. Primatol. 30:149–161.CrossRefGoogle Scholar
  13. Arditio, G., 1976, Check-list of the data on the gestation length of primates. J. Hum. Evol. 5:213–222.CrossRefGoogle Scholar
  14. Baxter, R. C., 2000, Insulin-like growth factor (IGF)-binding proteins: interactions with IGFs and intrinsic bioactivities, Am. J. Physiol. Endocrinol. Metab. 278: E967–E976.PubMedGoogle Scholar
  15. Bentley, P., 1998, Comparative Vertebrate Endocrinology, third edition, Cambridge University Press, Cambridge.Google Scholar
  16. Bercovitch, F. B. and Berard, J. D., 1993, Life history costs and consequences of rapid reproductive maturation in female macaques, Beh. Ecol. Sociobiol. 32: 103–109.CrossRefGoogle Scholar
  17. Bercovitch, F. B. and Strum, S. C., 1993, Dominance rank, resource availability, and reproductive maturation in female savanna baboons, Beh. Ecol. Sociobiol. 33:313–318.CrossRefGoogle Scholar
  18. Bernstein, R. M., Rowan, K., Leigh, S. R., 2000, New dental age standards for baboons (Papio hamadryas anubus) and mangabeys (Cercocebus atys). Am. J. Phys. Anthropol. 30:107–107.Google Scholar
  19. Bernstein, R. M., 2004, Hormones and Evolution in Papionin Primates. Ph.D. Dissertation, University of Illinois, Urbana, IL.Google Scholar
  20. Buchanan, L. S., 2006, The evolution of primate growth spurts. Ph.D. Dissertation, University of Illinois, Urbana, IL (in preparation).Google Scholar
  21. Carman, M., 1979, The gestation and rearing periods of the mandrill, Mandrillus sphinx, Int. Zoo Yrbk. 19:159–160.Google Scholar
  22. Cerroni, A. M., Tomlinson, G. A., Turnquist, J. E., Grynpas, M. D., 2003, Effect of parity on bone mineral density in female rhesus macaques from Cayo Santiago, Am. J. Phys. Anthropol. 121:252–269.PubMedCrossRefGoogle Scholar
  23. Charnov, E. L. and Berrigan, D., 1993, Why do female primates have such long lifespans and so few babies? Or Life in the slow lane, Ev. Anthropol. 1:191–194.CrossRefGoogle Scholar
  24. Cheek, D. B., 1975, Appendix II. Data on normal fetal and postnatal Macaca mulatta, in: Fetal and Postnatal Cellular Growth: Hormones and Nutrition, Cheek, D. B., ed., John Wiley & Sons, New York, pp. 521–534.Google Scholar
  25. Cheverud, J. M., 1981, Epiphyseal union and dental eruption in Macaca mulatta, Am. J. Phys. Anthropol. 56:157–167.PubMedCrossRefGoogle Scholar
  26. Cheverud, J. M., Dittus, W. P. J., and Wilson, P., 1992, Primate population studies at Polonnaruwa. III. Somatometric growth in a natural population of toque macaques (Macaca sinica), J. Hum. Evol. 23:51–78.CrossRefGoogle Scholar
  27. Cole, L. C., 1954, The population consequences of life history phenomena, Q. Rev. Biol. 29:103–137.PubMedCrossRefGoogle Scholar
  28. Deaner, R. O., Barton, R. A., and van Schaik, C. P., 2002, Primate brains and life histories: Renewing the connection, in: Primate Life Histories and Socioecology, P. M. Kappeler and M. E. Pereira, eds., Unversity of Chicago Press, Chicago, pp. 233–265.Google Scholar
  29. Deputte, B. L., 1991, Reproductive parameters of captive grey-cheeked mangabeys, Folia Primatol. (Basel) 57:57–69.CrossRefGoogle Scholar
  30. DeRousseau, C. J., 1990, Life history thinking in perspective, in: Primate Life History and Evolution, C. J. DeRousseau, ed., Alan R. Liss, New York, pp. 1–13.Google Scholar
  31. Efron B. and Tibshirani R., 1991, Statistical data analysis in the computer age, Science 253:390–395.CrossRefPubMedGoogle Scholar
  32. Finch, C. E. and Rose, M. R., 1995, Hormones and the physiological architecture of life history evolution, Q. Rev. Biol. 70:1–52.PubMedCrossRefGoogle Scholar
  33. Garber, P. A. and Leigh, S. R., 1997, Ontogenetic variation in small-bodied New World Primates: Implications for patterns of reproduction and infant care, Folia Primatol. 68:1–22.PubMedGoogle Scholar
  34. Garland, T. and Adolf, S. C., 1994, Why not to do two species comparative studies: Limitations on inferring adaptation, Physiol. Zool. 67:797–828.Google Scholar
  35. Godfrey, L. R., Samonds, K. E., Jungers, W. L., Sutherland, M. R., and Irwin, M. T., 2003, Ontogenetic correlates of diet in Malagasy lemurs, Am. J. Phys. Anthropol. 123:250–276CrossRefGoogle Scholar
  36. Gordon, T. P., Gust, D. A., Busse, C. D., Wilson, M. E., 1991, Hormones and sexual behavior associated with postconception perineal swelling in the sooty mangabey (cercocebus atys), Int. J. Primatol. 12:585–597.Google Scholar
  37. Gould, S. J., 1977, Ontogeny and Phylogeny, Belknap Press, Cambridge, MA.Google Scholar
  38. Gould, S. J., 1971, Geometric similarity in allometric growth: A contribution to the problem of scaling in the evolution of size, Am. Nat. 105:113–136.CrossRefGoogle Scholar
  39. Hadley, M., 2000, Endocrinology, fifth edition, Prentice Hall, New Jersey.Google Scholar
  40. Hall, K., Hilding, A., Thoren, M., 1999, Determinants of circulating insulin-like growth factor-I. J. Endocrinol. Invest. 22:48–52.Google Scholar
  41. Harvey, P. H., Martin, R. D., and Clutton-Brock, T. H., 1987, Life histories in comparative perspective, in: Primate Societies, B. B., Smuts, D. L., Cheney, R. M., Seyfarth, R. M., Wrangham, and T. T. Struhsaker, eds., University of Chicago Press, Chicago, pp. 181–196.Google Scholar
  42. Hendrickx, A. G., 1967, Studies in the development of the baboon, in: The Baboon in Medical Research, Volume II, H. Vagtborg, ed., University of Texas Press, Austin, TX, pp. 283–307.Google Scholar
  43. Hendrickx, A. G. and Houston, M. L., 1971, Appendix: Fetal growth, in: Embryology of the Baboon, A. G. Hendrickx, ed., University of Chicago Press, Chicago, pp. 173–196.Google Scholar
  44. Hughes, K. A. and Burleson, M. H., 2000, Evolutionary causes of variation in fertility and other fitness traits, in: Genetic Influences on Human Sexuality and Fertility, J. L. Rodgers, D. C. Rowe, and W. Miller, eds., Kluwer Academic Press, Dordrecht, The Netherlands, pp. 7–34.Google Scholar
  45. Janson, C. and van Schaik, C., 1993, Ecological risk aversion in juvenile primates: Slow and steady wins the race, in: Juvenile Primates: Life History, Development and Behavior, M. E. Pereira and L. A. Fairbanks, eds., Oxford University Press, New York, pp. 57–76.Google Scholar
  46. Johnson, S. E., 2003, Life histories and the competitive environment: Trajectories of growth maturation and reproductive output among chacma baboons, Am. J. Phys. Anthropol. 120:83–98.PubMedCrossRefGoogle Scholar
  47. Leigh, S. R., 1992, Patterns of variation in the ontogeny of primate body size dimorphism, J. Hum. Evol. 23:27–50.CrossRefGoogle Scholar
  48. Leigh, S. R., 1994, Ontogenetic correlates of diet in anthropoid primates, Am. J. Phys. Anthropol. 99:499–522.CrossRefGoogle Scholar
  49. Leigh, S. R., 1996, Evolution of human growth spurts, Am. J. Phys. Anthropol. 101:455–474.PubMedCrossRefGoogle Scholar
  50. Leigh, S. R., 2001, Evolution of human growth, Evol. Anthropol. 10:223–236.CrossRefGoogle Scholar
  51. Leigh, S. R., 2004, Brain growth, life histories, and cognition in primate and human evolution, Am. J. Primatol. 62:139–164.PubMedCrossRefGoogle Scholar
  52. Leigh, S. R., 2006, Growth and development, in: The Baboon in Biomedical Research, J. L. VandeBerg, S. Williams-Blangero, and S. Tardiff, eds., Kluwer Academic Press, New York (in press).Google Scholar
  53. Leigh, S. R. and Blomquist, G. E., 2006, Life history, in: Primates in Perspective, C. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, and S. Bearder, eds., Kluwer Academic/Plenum Press, New York (in press).Google Scholar
  54. Leigh, S. R., and Park, P. B., 1998, Evolution of human growth prolongation, Am. J. Phys. Anthropol. 107:331–350.PubMedCrossRefGoogle Scholar
  55. Leigh, S. R. and Terranova, C. J., 1998, Comparative perspectives on bimaturism, ontogeny, and dimorphism in lemurid primates, Int. J. Primatol. 19:723–749.CrossRefGoogle Scholar
  56. Leigh, S. R., Shah, N., and Buchanan, L. S., 2003, Ontogeny and phylogeny in papionin primates, J. Hum. Evol. 45:285–316.PubMedCrossRefGoogle Scholar
  57. Liu, J. and LeRoith, D., 1999, Insulin-like growth factor I is essential for postnatal growth in response to growth hormone, Endocrinol. 140:5178–5184.CrossRefGoogle Scholar
  58. Mahaney, M. C., Leland, M. M., Williams-Blangero, S., and Marinez, Y. N., 1993a, Cross-sectional growth standards for captive baboons: I. Organ weight by chronological age, J. Med. Primatol. 22:400–414.PubMedGoogle Scholar
  59. Mahaney, M. C., Leland, M. M., Williams-Blangero, S., Marinez, Y. N., 1993b, Cross-sectional growth standards for captive baboons: II. Organ weight by body weight, J. Med. Primatol. 22:415–427.PubMedGoogle Scholar
  60. Martin, R. D., 2002, Foreward, in: Primate Life Histories and Socioecology, P. M. Kappeler and M. E. Pereira, eds., Unversity of Chicago Press, Chicago, pp. xi–xx.Google Scholar
  61. Martin, R. D. and MacLarnon, A. M., 1990, Reproductive patterns in primates and other mammals: The dichotomy between altricial and precocial offspring, in: Primate Life History and Evolution, C. J. DeRousseau, ed., Alan R. Liss, New York, pp. 47–80.Google Scholar
  62. Moses, L. E., Gale, L. C., and Altmann, J., 1992, Methods for analysis of unbalanced, longitudinal growth data, Am. J. Primatol. 28:39–59.CrossRefGoogle Scholar
  63. Needham, J., 1933, On the dissociability of the fundamental processes of ontogenesis, Biol. Rev. 8:180–223.Google Scholar
  64. Pazos, F., Sanchez-Franco, F., Balsa, J., Escalada, J. Palacios, N., and Cacicedo, L., 2000, Mechanisms of reduced body growth in the pubertal feminized male rat: unbalanced estrogen and androgen action on the somatotropic axis. Ped. Res. 48: 96–103.Google Scholar
  65. Pereira, M. E. and Altmann, J., 1985, Development of social behavior in free-living nonhuman primates, in: Nonhuman Models for Human Growth and Development, E. S. Watts, ed., Alan R. Liss, New York, pp. 217–309.Google Scholar
  66. Pereira, M. E. and Leigh, S. R., 2002, Modes of primate development, in: Primate Life Histories and Socioecology, P. M. Kappeler and M. E. Pereira, eds., Unversity of Chicago Press, Chicago, pp. 149–176.Google Scholar
  67. Raff, R., 1996, The Shape of Life, University of Chicago Press, Chicago.Google Scholar
  68. Ross, C., 1988, The intrinsic rate of natural increase and reproductive effort in primates, J. Zool. (Lond.) 214:199–219.Google Scholar
  69. Ross C., 1998, Primate life histories, Evol Anthropol. 6:54–63.CrossRefGoogle Scholar
  70. Ross, C. and Jones, K. E., 1999, Socioecology and the evolution of primate reproductive rates, in: Comparative Primate Socioecology, P. C. Lee, ed., Cambridge University Press, New York, pp. 73–110.Google Scholar
  71. Sacher, G.A., 1959, The relation of life span to brain weight and body weight in mammals, in: CIBA Foundation Colloquia on Aging. Vol. 5. The Lifespan of Animals, G. E. W. Wolstenholme, and M. O’Connor, eds., Churchill, London, pp. 115–133.Google Scholar
  72. Sacher, G. and Staffeldt, E., 1974, Relation of gestation time to brain weight for placental mammals: Implications for the theory of vertebrate growth, Am. Nat. 108:593–615.CrossRefGoogle Scholar
  73. Sade, D. S., 1990, Intrapopulation variation in life-history parameters, in: Primate Life History and Evolution, C. J. DeRousseau, ed., Alan R. Liss, New York, pp. 181–194.Google Scholar
  74. Setchell, J. M., Lee, P. C., Wickings, E. J., and Dixson, A. F., 2001, Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx), Am. J. Phys. Anthropol. 115:337–348.CrossRefGoogle Scholar
  75. Setchell, J. M., Lee, P. C., Wickings, E. J., and Dixson, A. F., 2001, Growth and ontogeny of sexual size dimorphism in the mandrill (Mandrillus sphinx), Am. J. Phys. Anthropol. 115:349–360.PubMedCrossRefGoogle Scholar
  76. Setchell, J. M., Lee, P. C., Wickings, E. J., and Dixson, A. F., 2002, Reproductive parameters and maternal investment in mandrills (Mandrillus sphinx), Int. J. Primatol. 23:51–68.CrossRefGoogle Scholar
  77. Shea, B. T., 1990, Dynamic morphology: Growth, life history, and ecology in primate evolution, in: Primate Life History and Evolution, C. J. DeRousseau, ed., Alan R. Liss, New York, pp. 325–352.Google Scholar
  78. Sigg, H., Stolba, A., Abegglen, J.-J., Dasser, V., 1982, Life history of hamadryas baboons: Physical development, infant mortality, reproductive parameters and family relationships, Primates 23:473–487.CrossRefGoogle Scholar
  79. Smith, K. K., 2002, Sequence heterochrony and the evolution of development, J. Morphol. 252:82–97.PubMedCrossRefGoogle Scholar
  80. Strum, S. C., 1991, Weight and age in wild olive baboons, Am. J. Primatol. 25:219–237.CrossRefGoogle Scholar
  81. Stucki, B. R., Dow, M. M., and Sade, D. S., 1991, Variance in intrinsic rates of growth among free-ranging rhesus monkey groups, Am. J. Phys. Anthropol. 84:181–192.Google Scholar
  82. Tame, J. D., Winter, J. A., Li, C., Jenkins, S., Giussani, D. A., Nathanielsz, P. W., 1998, Fetal growth in the baboon during the second half of pregnancy, J. Med. Primatol. 27:234–239.PubMedGoogle Scholar
  83. Turnquist, J. E., and Kessler, M. J., 1989, Free-ranging Cayo Santiago rhesus monkeys (Macaca mulatta): I. Body size, proportion, and allometry, Am. J. Primatol. 19:1–13.CrossRefGoogle Scholar
  84. Watts, E. S., 1985, Adolescent growth and development of monkeys, apes and humans, in: Nonhuman Primate Models of Human Growth and Development, E. S. Watts, ed., Alan R. Liss, New York, pp. 41–66.Google Scholar
  85. Watts, E. S., 1990, Evolutionary trends in primate growth and development, in: Primate Life History and Evolution, C. J. DeRousseau, ed., Alan R. Liss, New York, pp. 89–104.Google Scholar
  86. Williams-Blangero, S. and Blangero, J., 1995, Heritability of age at first birth in captive olive baboons, Am. J. Primatol. 37:233–240.CrossRefGoogle Scholar
  87. Wilkinson L. 1999. Systat for Windows, Version 9. Systat, Inc, Evanston, IL.Google Scholar
  88. Yu, H., Mistry, J., Nicar, M., Khosrab, M., Diamandis, A., van Doom, J., and Juul, A., 1999, Insulin-like growth factors (IGF-I, free IGF-I and IGF-II) and insulinlike growth factor binding proteins (IGFBP-2, IGFBP-3, IGFBP-6, and ALS) in blood circulation, J. Clin. Lab. Anal. 13:166–172.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2006

Authors and Affiliations

  • Steven R. Leigh
    • 1
  • Robin M. Bernstein
    • 2
  1. 1.Department of AnthropologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of AnthropologyGeorge Washington UniversityWashington D.C.USA

Personalised recommendations