, 135:209 | Cite as

Fitness-related patterns of genetic variation in rhesus macaques

  • Gregory E. Blomquist


The patterning of quantitative genetic descriptions of genetic and residual variation for 15 skeletal and six life history traits was explored in a semi-free-ranging group of rhesus macaques (Macaca mulatta Zimmerman 1780). I tested theoretical predictions that explain the magnitude of genetic and residual variation as a result of 1. strength of a trait’s association with evolutionary fitness, or 2. developmental and physiological relationships among traits. I found skeletal traits had higher heritabilities and lower coefficients of residual variation than more developmentally and physiologically dependent life history traits. Total lifetime fertility had a modest heritability (0.336) in this population, and traits with stronger correlations to fitness had larger amounts of residual variance. Censoring records of poorly-performing individuals on lifetime fertility and lifespan substantially reduced their heritabilities. These results support models for the fitness-related patterning of genetic variation based on developmental and physiological relationships among traits rather than the action of selection eroding variation.


Cayo Santiago Censored data Coefficient of variation Fundamental theorem of natural selection Heritability Life history Macaca mulatta Rhesus macaque Morphology Variance components 





Coefficient of additive genetic variation


Coefficient of residual variation



Cayo Santiago and the Laboratory for Primate Morphology and Genetics are part of the Caribbean Primate Research Center which is supported by the University of Puerto Rico, Medical Sciences Campus and the National Institutes of Health. The project described was supported by Grant Number CM-5 P40 RR003640-20 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH). Its contents are solely the responsibility of the author and do not necessarily represent the official views of NCRR or NIH. The genetic database from which paternity data were provided was originally created by John Berard, Fred Bercovitch, Matt Kessler, Michael Krawczak, Peter Nürnberg, and Jorg Schmidtke. The National Science Foundation, Harry Frank Guggenheim Foundation, University of Berlin, Deutsche Forschungsmeinschaft, Medizinische Hochschule Hannover, NIH, and CPRC funded the creation of the genetic database. Additional funding for this research came from the University of Illinois Graduate College. Melissa Gerald, John Cant, Terry Kensler, Benedikt Hallgrimsson, and Jean Turnquist were all helpful resources while working with CPRC materials. Angel “Guelo” Figueroa, Edgar Davila, and Elizabeth Maldonado must be credited for the completeness and upkeep of the demographic records on Cayo Santiago. John Berard and Donald Sade provided data and discussion on social rank. Steve Leigh, Paul Garber, Charles Roseman, Rebecca Stumpf, and Jim Cheverud all provided helpful insights. The comments of two anonymous reviewers also improved the manuscript.


  1. Ackermann RR, Cheverud JM (2004) Detecting genetic drift versus selection in human evolution. Proc Natl Acad Sci USA 101:17946–17951PubMedCrossRefGoogle Scholar
  2. Bass WM (1995) Human osteology: a laboratory and field manual, 4th edn. Missouri Archeological SocietyGoogle Scholar
  3. Bercovitch FB, Strum SC (1993) Dominance rank, resource availability, and reproductive maturation in female savanna baboons. Behav Ecol Sociobiol 33:313–318CrossRefGoogle Scholar
  4. Blomquist GE (2006) Quantitative genetics of female rhesus macaque age-specific reproductive output: Evidence for trade-offs and their implications. Am J Phys Anthropol 129:66Google Scholar
  5. Blomquist GE (2007) Quantitative Genetics of Life History Microevolution in the Cayo Santiago Rhesus Macaques (Macaca mulatta). Ph.D. thesis, University of Illinois, UrbanaGoogle Scholar
  6. Brown D (1988) Components of lifetime reproductive success. In: Clutton-Brock TH (ed) Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago PressGoogle Scholar
  7. Burns EM, Enns RM, Garrick DJ (2006) The effect of simulated censored data on estimates of heritability of longevity in the Thoroughbred racing industry. Genet Mol Res 5:7–15PubMedGoogle Scholar
  8. Cheverud JM (1982) Phenotypic, genetic, and environmental morphological integration in the cranium. Evolution Int J Org Evolution 36:499–516Google Scholar
  9. Cheverud JM, Buikstra JE (1981) Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. I. single trait heritabilities. Am J Phys Anthropol 54:43–49PubMedCrossRefGoogle Scholar
  10. Cheverud JM, Falk D, Vannier M, et al. (1990) Heritability of brain size and surface features in rhesus macaques (Macaca mulatta). J Hered 81:51–57PubMedGoogle Scholar
  11. Chuang-Stein C, Agresti A (1997) A review of tests for detecting a monotone dose-response relationship with ordinal response data. Stat Med 16:2599–2618PubMedCrossRefGoogle Scholar
  12. Crnokrak P, Roff DA (1995) Dominance variance: associations with selection and fitness. Heredity 75:530–540CrossRefGoogle Scholar
  13. Crow JF (1958) Some possibilities for measuring selection intensities in man. Hum Biol 30:1–13PubMedGoogle Scholar
  14. Crow JF (1962) Population genetics: selection. In: Burdette WJ (ed) Methodology in human genetics. Holden-Day, San FransiscoGoogle Scholar
  15. Datta SB (1983) Relative power and the acquisition of rank. In: Hinde RA (ed) Primate Social Relationships: An Integrated Approach. Sinauer Associates, Inc, Sunderland, MAGoogle Scholar
  16. Duggleby CR, Haseley PA, Rawlins RG, et al (1986) An overview of blood group genetic studies on the Cayo Santiago rhesus monkeys. In: Rawlins RG, Kessler MJ (eds) The Cayo Santiago Macaques: history, behavior, and biology. SUNY Press, Albany, NYGoogle Scholar
  17. Dyke B (1996) PEDSYS: A Pedigree Database Management system users manual. Population Genetics Laboratory, Department of Genetics, Southwest Foundation for Biomedical Research, San Antonio, TXGoogle Scholar
  18. Eshel I, Hamilton WD (1984) Parent-offspring correlation in fitness under fluctuating selection. Proc R Soc Lond B Biol Sci 222:1–14CrossRefGoogle Scholar
  19. Esparza M, Martinez-Abadias N, Sjovold T et al (2006) Selective processes in human reproductive success: heritability of life history traits. Am J Phys Anthropol 42:88Google Scholar
  20. Falconer DS, MacKay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Harlow, EssexGoogle Scholar
  21. Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, OxfordGoogle Scholar
  22. Gustafsson L (1986) Lifetime reproductive success and heritabilities: empirical support for Fisher’s fundamental theorem. Am Nat 128:761–764CrossRefGoogle Scholar
  23. Hallgrimsson B (1999) Ontogenetic patterning of skeletal fluctuating asymmetry in rhesus macaques and humans: evolutionary and developmental implications. Int J Primatol 20:121–151CrossRefGoogle Scholar
  24. Hallgrimsson B, Willmore K, Hall BK (2002) Canalization, developmental stability, and morphological integration in primate limbs. Yearb Phys Anthropol 45:181–158Google Scholar
  25. Houle D (1992) Comparing evolvability and variability of quantitative traits. Genetics 130:195–204PubMedGoogle Scholar
  26. Houle D (1998) How should we explain variation in the genetic variance of traits? Genetica 102/103:241–253CrossRefGoogle Scholar
  27. Kelley MJ (2001) Lineage loss in Serengeti cheetahs: Consequences of high reproductive variance and heritability of fitness on effective population size. Conserv Biol 15:137–147CrossRefGoogle Scholar
  28. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philos Trans R Soc Lond B Biol Sci 359:873–890PubMedCrossRefGoogle Scholar
  29. Kruuk LEB, Slate J, Pemberton JM, et al. (2002) Antler size in red deer: heritability and selection but no evolution Evolution Int J Org Evolution 56:1683–1695Google Scholar
  30. Kruuk LEB, Clutton-Brock TH, Slate J, et al. (2000) Heritability of fitness in a wild mammal population. Proc Natl Acad Sci USA 97:698–703PubMedCrossRefGoogle Scholar
  31. Lande R (1979) Quantitative genetic analysis of multivariate evolution applied to brain:body size allometry. Evolution Int J Org Evolution 33:402–416Google Scholar
  32. Lande R, Arnold SJ (1983) Measurement of selection on correlated characters. Evolution Int J Org Evolution 37:1210–1226Google Scholar
  33. Lawler RR (2006) Sifaka positional behavior: Ontogenetic and quantitative genetic approaches. Am J Phys Anthropol 131:261–271PubMedCrossRefGoogle Scholar
  34. Lee JH, Flaquer A, Costa R, et al. (2004) Genetic influences on life span and survival among elderly African-Americans, Caribbean hispanics, and caucasians. Am J Med Genet 128A:159–164CrossRefPubMedGoogle Scholar
  35. Leigh SR (2001) Evolution of human growth. Evol Anthropol 10:223–236CrossRefGoogle Scholar
  36. Lynch M, Walsh B (1998) Genetics and Analysis of Quantitative Traits. Sinauer Associates, Inc, Sunderland, MAGoogle Scholar
  37. Madrigal L, Relethford JH, Crawford MH (2003) Heritability and anthropometric influences on human fertility. Am J Hum Biol 15:16–22PubMedCrossRefGoogle Scholar
  38. Marriog G, Cheverud JM (2004) Did natural selection or genetic drift produce the cranial diversification of neotropical monkeys? Am Nat 163:417–428CrossRefGoogle Scholar
  39. Martin LJ, Mahaney MC, Bronikowski AM, et al. (2002) Lifespan in captive baboons is heritable. Mech Ageing Dev 123:1461–1467PubMedCrossRefGoogle Scholar
  40. Martin RD (1990) Primate Origins and Evolution: A Phylogenetic Reconstruction. Princeton University Press, PrincetonGoogle Scholar
  41. McLeery RH, Pettifor RA, Armbuster P, et al (2004) Components of variance underlying fitness in a natural population of the great tit Parus major. Am Nat 164:E1–E11CrossRefGoogle Scholar
  42. McGraw JB, Caswell H (1996) Estimation of individual fitness from life-history data. Am Nat 147:47–64CrossRefGoogle Scholar
  43. Merilä J, Sheldon BC (1999) Genetic architechture of fitness and nonfitness traits: empirical patterns and development of ideas. Heredity 83:103–109PubMedCrossRefGoogle Scholar
  44. Merilä J, Sheldon BC (2000) Lifetime reproductive success and heritability in nature. Am Nat 155:301–310PubMedCrossRefGoogle Scholar
  45. Meyer K (2000) Derivative-free restricted maximum likelihood (DFREML) 3.1Google Scholar
  46. Missakian EA (1972) Genealogical and cross-genealogical dominace relations in a group of free-ranging rhesus monkeys (Macaca mulatta). Primates 13:169–180CrossRefGoogle Scholar
  47. Mitchell BD, Hsueh WC, King TM, et al (2001) Heritability of life span in the old order amish. Am J Med Genet 102:346–352PubMedCrossRefGoogle Scholar
  48. Mouseau TA, Roff DA (1987) Natural selection and heritability of fitness components. Heredity 59:181–197CrossRefGoogle Scholar
  49. Pettay JI, Kruuk LEB, Jokela J et al (2005) Heritability and genetic constraints of life-history trait evolution in preindustrial humans. Proc Natl Acad Sci USA 102:2838–2843PubMedCrossRefGoogle Scholar
  50. Price T, Schluter D (1991) On the low heritability of life history traits. Evolution Int J Org Evolution 45:853–861Google Scholar
  51. Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99CrossRefGoogle Scholar
  52. Rawlins RG, Kessler MJ (1986) 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, AlbanyGoogle Scholar
  53. Reale D, Festa-Bianchet M (2000) Mass-dependent reproductive strategies in wild bighorn ewes: a quantitative genetic approach. J Evol Biol 13:679–688CrossRefGoogle Scholar
  54. Robertson A (1966) A mathematical model of the culling process in dairy cattle. Anim Prod 8:95–108Google Scholar
  55. Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New YorkGoogle Scholar
  56. Roff DA, Mouseau TA (1987) Quantitative genetics of fitness: lessons from Drosophila. Heredity 58:103–118PubMedCrossRefGoogle Scholar
  57. 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 YorkGoogle Scholar
  58. Rose M (1982) Antagonistic pleiotropy, dominance, and genetic variation. Heredity 43:63–78CrossRefGoogle Scholar
  59. Sade DS, Chepko-Sade BD, Schneider JM, et al (1985) Basic demographic observations on free-ranging Rhesus monkeys. Human Relations Area Files, New Haven, CTGoogle Scholar
  60. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652PubMedCrossRefGoogle Scholar
  61. SAS Institute (2003) SAS version 9. Cary, NCGoogle Scholar
  62. Schluter D (1996) Adaptive radiation along evolutionary lines of least resistance. Evolution Int J Org Evolution 50:1766–1774Google Scholar
  63. Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, New YorkGoogle Scholar
  64. Silk JB (1984) Measurement of the relative importance of individual selection and kin selection among females of the genus Macaca. Evolution Int J Org Evolution 38:553–559Google Scholar
  65. Smith DG, McDonough J (2005) Mitochondrial DNA variation in Chinese and Indian rhesus macaques (Macaca mulatta) Am J Primatol 65:1–25PubMedCrossRefGoogle Scholar
  66. Sokal RR, Rolf FJ (1994) Biometry. WH Freeman, San FranciscoGoogle Scholar
  67. Stearns SC, Kawecki TJ (1994) Fitness sensitivity and the canalization of fitness components. Evolution Int J Org Evolution 48:1438–1450Google Scholar
  68. Stearns SC, Kaiser M, Kawecki TJ (1995) The differential genetic and environmental canalization of fitness components in Drosophila melanogaster. J Evol Biol 8:539–557CrossRefGoogle Scholar
  69. Stucki BR, Dow MM, Sade DS (1991) Variance in intrinsic rates of growth among free-ranging Rhesus monkeys. Am J Phys Anthropol 84:181–191Google Scholar
  70. Towne B, Czerwinski SA, Demerath EW, et al. (2005) Heritability of age at menarche in girls from the Fels Longitudinal Study. Am J Phys Anthropol 128:210–219PubMedCrossRefGoogle Scholar
  71. van Tienderen PH, de Jong G (1994) A general model of the relation between phenotypic selection and genetic response. J Evol Biol 7:1–12CrossRefGoogle Scholar
  72. Vukasinovic N, Moll J, Kuenzi N (1998) Genetic analysis of productive life with censored records. J Anim Sci 76:59Google Scholar
  73. Williams-Blangero S, Blangero J (1995) Heritability of age of first birth in captive olive baboons. Am J Primatol 37:233–239CrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of MissouriColumbiaUSA

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