Quantitative Genetic Perspectives on Female Macaque Life Histories

Heritability, Plasticity, and Trade-Offs
  • Gregory E. Blomquist
Part of the Developments in Primatology: Progress and Prospects book series (DIPR, volume 37)


All life histories are a complex of trade-offs that depend on individual conditions—including size, age, and sex—and adaptively mold suites of traits through the biased intergenerational transmission of successful physiological strategies. I explore intrapopulation variation in how female rhesus macaques on Cayo Santiago have negotiated a central life history trade-off: when to start reproducing. I emphasize how evolutionary quantitative genetic models require explicit links between hypothesized or measured patterns of selection and the genetic substrates that influence phenotypes and change intergenerationally. Perhaps counterintuitively, I also show how genetic models offer valuable insights on how environments, including those provided by mothers and other kin, affect offspring development and later female life histories. The emerging picture of female macaque maturation is one of the great flexibility and environmental responsiveness coupled with an important genetic component that is significantly entangled with later life history events.


Life History Variance Component Infant Death Rate Genetic Correlation Life History Trait 
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.



Thanks to Kate Clancy, Katie Hinde, and Julienne Rutherford for the invitation to contribute to this chapter. Cayo Santiago is part of the Caribbean Primate Research Center (CPRC) which is supported by the University of Puerto Rico, Medical Sciences Campus and the National Institutes of Health (NIH). The facility is also supported by Grant Number CM-5 P40 RR003640-20 from the National Center for Research Resources (NCRR), a component of NIH. The contents of this chapter are solely the responsibility of the author and do not necessarily represent the official views of NCRR or NIH. Additional funding for this research came from the University of Illinois Graduate College and the University of Missouri. Melissa Gerald, John Cant, Terry Kensler, Benedikt Hallgrimsson, and Jean Turnquist were all helpful resources while working with CPRC materials. Donald Sade, Richard Rawlins, John Berard, and Melissa Gerald must be credited for the upkeep of the demographic records on Cayo Santiago and Angel “Guelo” Figueroa, Edgar Davila, and Elizabeth Maldonado for their day-to-day maintenance. I also want to thank my wife, Rachel, who was busy building a baby and tackling the rest of life while I wrote this chapter.


  1. Altmann J (1980) Baboon mothers and infants. Cambridge, Harvard University PressGoogle Scholar
  2. Altmann J, Alberts SC (2005) Growth rates in a wild primate population: ecological influences and maternal effects. Behav Ecol Sociobiol 57:490–501CrossRefGoogle Scholar
  3. Altmann J, Altmann SA, Hausfater G, McCuskey SA (1977) Life history of yellow baboons: physical development, reproductive parameters, and infant mortality. Primates 18:315–330CrossRefGoogle Scholar
  4. Arnold SJ (1994) Multivariate inheritance and evolution: a review of concepts. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, p 17–48Google Scholar
  5. Bell G, Kofoupanou V (1986) The cost of reproduction. Oxf Surv Evol Biol 3:83–131Google Scholar
  6. Bercovitch FB, Berard JD (1993) Life history costs and consequences of rapid reproductive maturation in female rhesus macaques. Behav Ecol Sociobiol 32:103–109CrossRefGoogle Scholar
  7. Bijma P (2006) Estimating maternal genetic effects in livestock. J Anim Sci 84:800–806PubMedGoogle Scholar
  8. Blomquist GE (2009a) Environmental and genetic causes of maturational differences among rhesus macaque matrilines. Behav Ecol Sociobiol 63:1345–1352CrossRefGoogle Scholar
  9. Blomquist GE (2009b) Female age of first reproduction at Cayo Santiago: heritability and shared environments. Am J Phys Anthropol 138:94CrossRefGoogle Scholar
  10. Blomquist GE (2009c) Fitness-related patterns of genetic variation in rhesus macaques. Genetica 135:209–219PubMedCrossRefGoogle Scholar
  11. Blomquist GE (2009d) Trade-off between age of first reproduction and survival in a female ­primate. Biol Lett 5:339–342PubMedCrossRefGoogle Scholar
  12. Blomquist GE, Sade DS, Berard JD (2011) Rank-related fitness differences and their demographic pathways in semi-free ranging rhesus macaques (Macaca mulatta). Int J Primatol 31:193–208CrossRefGoogle Scholar
  13. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135PubMedCrossRefGoogle Scholar
  14. Brommer JE, Wilson AJ, Gustafsson L (2007) Exploring the genetics of aging in a wild passerine bird. Am Nat 170:643–650PubMedCrossRefGoogle Scholar
  15. Busse C (1982) Social dominance and offspring mortality among female chacma baboons. Int J Primatol 3:267CrossRefGoogle Scholar
  16. Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  17. Chapais B (2004) How kinship generates dominance structures: a comparative perspective. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization. Cambridge University Press, New York, pp 3–10Google Scholar
  18. Charlesworth B (1994) Evolution in age-structured populations. 2nd edn. Cambridge University Press, New YorkCrossRefGoogle Scholar
  19. Charnov EL, Berrigan D (1993) Why do female primates have such long lifespans and so few babies? or life in the slow lane. Evol Anthropol 1:191–194CrossRefGoogle Scholar
  20. Cheney DL, Seyfarth RM, Fischer J, Beehner JC, Bergman TJ, Johnson SE, Kitchen DM, Palombit RA, Rendall D, Silk JB (2006) Reproduction, mortality, and female reproductive success in chacma baboons of the Okavango Delta, Botswana. In: Swedell L, Leigh SR (eds) Reproduction and fitness in baboons: behavioral, ecological, and life history perspectives. Springer, New York, pp 147–176CrossRefGoogle Scholar
  21. Cheverud JM, Moore AJ (1994) Quantitative genetics and the role of the environment provided by relatives in behavioral evolution. In: Boake CRB (ed) Quantitative genetic studies of behavioral evolution. University of Chicago Press, Chicago, pp 67–100Google Scholar
  22. Cheverud JM, Wolf JB (2009) The genetics and evolutionary consequences of maternal effects. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 11–37Google Scholar
  23. de Jong G, van Noordwijk AJ (1992) Acquisition and allocation of resources: genetic (co)variances, selection, and life histories. Am Nat 139:749–770CrossRefGoogle Scholar
  24. Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ecol Sociobiol 16:257–333Google Scholar
  25. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, OxfordGoogle Scholar
  26. Gagliardi C, Falkenstein KP, Franke DE, Kubisch HM (2010) Estimates of heritability for reproductive traits in captive rhesus macaque females. Am J Primatol 72:811–819PubMedCrossRefGoogle Scholar
  27. Gilmour AR, Gogel BJ, Cullis BR, Thompson R (2009) ASReml User Guide, version 3.0. VSN InternationalGoogle Scholar
  28. Grafen A (1988) On the uses of data on lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 454–471Google Scholar
  29. Ha JC, Ha RR, Almasy L, Dyke B (2002) Genetics and caging type affect birth weight in captive pigtailed macaques (Macaca nemestrina). Am J Primatol 56:207–213PubMedCrossRefGoogle Scholar
  30. Harvey PH, Martin RD, Clutton-Brock TH (1987) Life histories in comparative perspective. In: Smuts B (ed) Primate societies. University of Chicago Press, Chicago, pp 181–196Google Scholar
  31. Hird DW, Henrickson RV, Hendrickx AG (1975) Infant mortality in Macaca mulatta: neonatal and post-neonatal mortality at the California Primate Research Center, 1968–1972. A retrospective study. J Med Primatol 4:4–22Google Scholar
  32. Hoffman CL, Higham JP, Mas-Rivera A, Ayala JE, Maestripieri D (2010) Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago. Behav Ecol 21:972–978PubMedCrossRefGoogle Scholar
  33. Houle D (1991) Genetic covariance of fitness correlates: what genetic correlations are made of and why it matters. Evolution 45:630–645CrossRefGoogle Scholar
  34. Hrdy SB (1999) Mother nature: a history of mothers, infants, and natural selection. Pantheon Books, New YorkGoogle Scholar
  35. Hughes KA, Alipaz JA, Drnevich JM, Reynolds RM (2002) A test of evolutionary theories of aging. Proc Natl Acad Sci USA 99:14286–14291PubMedCrossRefGoogle Scholar
  36. Jaquish CE, Cheverud JM, Tardif SD (1996) Genetic and environmental impacts on litter size and early infant survival in three species of callitrichids. J Hered 87:74–77PubMedCrossRefGoogle Scholar
  37. Jaquish CE, Dyer T, Williams-Blangero S, Dyke B, Leland M, Blangero J (1997) Genetics of adult body mass and maintenance of adult body mass in captive baboons (Papio hamadryas subspecies). Am J Primatol 42:281–288PubMedCrossRefGoogle Scholar
  38. Jones JH, Wilson ML, Murray C, Pusey A (2010) Phenotypic quality influences fertility in gombe chimpanzees. J Anim Ecol 79:1262–1269PubMedCrossRefGoogle Scholar
  39. Kappeler PM, Pereira ME (2003) Primate life histories and socioecology. University of Chicago Press, ChicagoGoogle Scholar
  40. Kessler MJ, Berard JD, Rawlins RG, Bercovitch FB, Gerald MS, Laudenslager ML, Gonzalez-Martinez J (2006) Tetanus antibody titers and duration of immunity to clinical tetanus infections in free-ranging rhesus monkeys (Macaca mulatta). Am J Primatol 68:725–731PubMedCrossRefGoogle Scholar
  41. Kevles D (1985) In the name of eugenics. UCLA Press, Los AngelesGoogle Scholar
  42. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783CrossRefGoogle Scholar
  43. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Phil Trans Roy Soc Lond Ser B 359:873–890CrossRefGoogle Scholar
  44. Kruuk LEB, Hadfield JD (2007) How to separate genetic and environmental causes of similarity between relatives. J Evol Biol 20:1890–1903PubMedCrossRefGoogle Scholar
  45. Kruuk LEB, Slate J, Wilson AJ (2008) New answers for old questions: the evolutionary quantitative genetics of wild animal populations. Annu Rev Ecol Systemat 39:525–548CrossRefGoogle Scholar
  46. Lande R (1982) A quantitative genetic theory of life history evolution. Ecology 63:607–615CrossRefGoogle Scholar
  47. Lande R, Arnold SJ (1983) Measurement of selection on correlated characters. Evolution 37:1210–1226CrossRefGoogle Scholar
  48. Law R (1979) Optimal life histories under age-specific predation. Am Nat 114:399–417CrossRefGoogle Scholar
  49. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer Associates, SunderlandGoogle Scholar
  50. Maestripieri D (2003) Similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers. Dev Psychobiol 43:321–327PubMedCrossRefGoogle Scholar
  51. Maestripieri D (2009) Maternal influences on offspring growth, reproduction, and behavior in primates. In: Maestripieri D, Mateo JM (eds) Maternal effects in mammals. University of Chicago Press, Chicago, pp 256–291Google Scholar
  52. Martin LJ, Mahaney MC, Bronikowski AM, Dee CK, Dyke B, Comuzzie AG (2002) Lifespan in captive baboons is heritable. Mech Ageing Dev 123:1461–1467PubMedCrossRefGoogle Scholar
  53. Merilä J, Sheldon BC (1999) Genetic architechture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109PubMedCrossRefGoogle Scholar
  54. Meyer K (2001) Estimates of direct and maternal covariance functions for growth of australian beef calves from birth to weaning. Genet Sel Evol 33:487–514PubMedCrossRefGoogle Scholar
  55. Nickerson SC (1995) Milk production: factors affecting milk composition. In: Harding F (ed) Milk quality. Blackie Academic and Professional, London, pp 3–24CrossRefGoogle Scholar
  56. Nurnberg P, Saurmann U, Kayser M, Lanfer C, Manz E, Widdig A, Berard J, Bercovitch FB, Kessler M, Schmidtke J, Krawczak M (1998) Paternity assessment in rhesus macaques (Macaca mulatta): Multilocus DNA fingerprinting and PCR marker typing. Am J Primatol 44:1–18PubMedCrossRefGoogle Scholar
  57. Price T, Schluter D (1991) On the low heritability of life history traits. Evolution 45:853–861CrossRefGoogle Scholar
  58. Provine, WB (1971) The origins of theoretical population genetics. University of Chicago Press, ChicagoGoogle Scholar
  59. Quinn JL, Charmantier A, Garant D, Sheldon BC (2006) Data depth, data completeness, and their influence on quantitative genetic estimation in two contrasting bird populations. J Evol Biol 19:994–1002PubMedCrossRefGoogle Scholar
  60. Ralls K, Ballou J (1982) Effects of inbreeding on infant mortality in captive primates. Int J Primatol 3:491–505CrossRefGoogle Scholar
  61. Räsänen K, Kruuk LEB (2007) Maternal effects and evolution at ecological time scales. Funct Ecol 21:408–421CrossRefGoogle Scholar
  62. Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99CrossRefGoogle Scholar
  63. Rawlins RG, Kessler MJ (eds) (1986a) The Cayo Santiago macaques: history, behavior, and bio­logy. SUNY Press, AlbanyGoogle Scholar
  64. Rawlins RG, Kessler MJ (1986b) The history of the Cayo Santiago colony. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago macaques: history, behavior, and ecology. State University of New York Press, Albany, pp 47–72Google Scholar
  65. Reznick D (1985) Costs of reproduction: an evaluation of the empirical evidence. Oikos 44:257–267CrossRefGoogle Scholar
  66. Rice SH (2004) Developmental associations between traits: covariance and beyond. Genetics 166:513–526PubMedCrossRefGoogle Scholar
  67. Ricklefs RE, Wikelski M (2002) The physiology/life-history nexus. Trends Ecol Evol 17:462–468CrossRefGoogle Scholar
  68. Robson EB (1978) The genetics of birth weight. In: Falkner F, Tanner JM (eds) Human growth: 1 principles and prenatal growth. Plenum Press, New York, pp 285–297Google Scholar
  69. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkCrossRefGoogle Scholar
  70. Roff DA (2002) Life history evolution. 2nd edn. Sinauer Associates, SunderlandGoogle Scholar
  71. Roff DA, Fairbairn DJ (2007) The evolution of trade-offs: where are we? J Evol Biol 20:433–447PubMedCrossRefGoogle Scholar
  72. Rogers J (2005) Genetics: a survey of nonhuman primate genetics, genetic management and applications to biomedical research. In: Coote SW (ed) The laboratory primate. Academic Press, New York, pp 487–501CrossRefGoogle Scholar
  73. Sade DS, Chepko-Sade BD, Schneider JM, Roberts SS, Richtsmeier JT (1985) Basic demographic observations on free-ranging rhesus monkeys. Human Relations Area Files, New HavenGoogle Scholar
  74. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652PubMedCrossRefGoogle Scholar
  75. Schino G, Troisi A (2005) Neonatal abandonment in Japanese macaques. Am J Phys Anthropol 126:447–452PubMedCrossRefGoogle Scholar
  76. Silk JB, Alberts SC, Altmann J (2003) Social bonds of female baboons enhance infant survival. Science 302:1231–1234PubMedCrossRefGoogle Scholar
  77. Smith DG (1986) Incidence and consequences of inbreeding in three captive groups of rhesus macacques (Macaca mulatta). In: Benirschke K (ed) Primates: the road to self-sustaining ­populations. Springer, New York, pp 857–874Google Scholar
  78. Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  79. Stearns SC (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  80. Stearns SC, Magwene P (2003) The naturalist in the world of genomics. Am Nat 161:171–180PubMedCrossRefGoogle Scholar
  81. Strier KB, Altmann J, Brockman DK, Bronikowski AM, Cords M, Fedigan LM, Lapp H, Liu X, Morris WF, Pusey AE, Stoinski TS, Alberts SC (2010) The primate life history database: a unique shared ecological data resource. Meth Ecol Evol 1:199–211CrossRefGoogle Scholar
  82. Stucki BR, Dow MM, Sade DS (1991) Variance in intrinsic rates of growth among free-ranging rhesus monkeys. Am J Phys Anthropol 84:181–191CrossRefGoogle Scholar
  83. Takahata Y, Suzuki S, Agetsuma N, Okayasu N, Sugiura H, Takahashi H, Yamagiwa J, Izawa K, Furuichi T, Hill DA, Maruhashi T, Saito C, Sato S, Sprague DS (1998) Reproduction of wild Japanese macaque females of Yakushima and Kinkazan islands: A preliminary report. Primates 39:339–349CrossRefGoogle Scholar
  84. Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, HobokenCrossRefGoogle Scholar
  85. Towne B, Czerwinski SA, Demerath EW, Blangero J, Roche AF, Siervogel RM (2005) Heritability of age at menarche in girls from the Fels longitudinal study. Am J Phys Anthropol 128:210–219PubMedCrossRefGoogle Scholar
  86. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142CrossRefGoogle Scholar
  87. van Schaik CP, Janson CH (eds) (2000) Infanticide by males and its implications. Cambridge University Press, New YorkGoogle Scholar
  88. Visscher PM, Hill WG, Wray NR (2008) Heritability in the genomics era—concepts and misconceptions. Nat Rev Genet 9:255–266PubMedCrossRefGoogle Scholar
  89. Vitzthum VJ (2003) A number no greater than the sum of its parts: the use and abuse of heritability. Hum Biol 75:539–558PubMedCrossRefGoogle Scholar
  90. Williams GC (1957) Pleiotropy, natural selection, and the evolution of senescence. Evolution 11:398–411CrossRefGoogle Scholar
  91. Williams-Blangero S, Blangero J (1995) Heritability of age of first birth in captive olive baboons. Am J Primatol 37:233–239CrossRefGoogle Scholar
  92. Wilson AJ, Réale D (2006) Ontogeny of additive and maternal genetic effects: lessons from domestic mammals. Am Nat 167:E23–E38PubMedCrossRefGoogle Scholar
  93. Wilson AJ, Reale D, Clements MN, Morrissey MM, Postma E, Walling CA, Kruuk LEB, Nussey DH (2010) An ecologist’s guide to the animal model. J Anim Ecol 79:13–26PubMedCrossRefGoogle Scholar
  94. Wilson ME, Gordon TP, Bernstein IS (1978) Timing of births and reproductive success in rhesus monkey social groups. J Med Primatol 7:202–212PubMedGoogle Scholar
  95. Wolf JB, Brodie III ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13:64–69PubMedCrossRefGoogle Scholar
  96. Wolf JB, Brodie III ED, Moore AJ (1999) Interacting phenotypes and the evolutionary process, II. Selection resulting from social interactions. Am Nat 153:254–266Google Scholar
  97. Wolf JB, Wade MJ (2009) What are maternal effects (and what are they not)? Phil Trans Roy Soc Lond Ser B 364:1107–1115CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of MissouriColumbiaUSA

Personalised recommendations