Advertisement

Behavioral Ecology and Sociobiology

, Volume 63, Issue 9, pp 1345–1352 | Cite as

Environmental and genetic causes of maturational differences among rhesus macaque matrilines

  • Gregory E. BlomquistEmail author
Original Paper

Abstract

Females of many cercopithecine primates live in stable dominance hierarchies that create long-term asymmetries among sets of female relatives (matrilines) in access to limiting resources and shelter from psychosocial stress. Rank-related differences in fitness components are widely documented, but their causes are unclear. Predicted breeding values from an animal model for female age of first reproduction are used to discriminate between shared additive genetic and shared environmental effects among the members of matrilines in a population of free-ranging rhesus macaques (Macaca mulatta). While age of first reproduction has a modest heritability (≈0.2), breeding values are distributed in a largely random fashion among matrilines and contribute little to the observed rank-related differences in average age of first reproduction. These results support the long-held, but previously unverified, contention that rank-related life history differences in female cercopithecine primates are the result of environmental rather than genetic differences among them.

Keywords

Social dominance Breeding value Quantitative genetics Heritability Female maturation Cayo Santiago 

Notes

Acknowledgements

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 report 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, the Harry Frank Guggenheim Foundation, the 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 on this project. Comments from Martin Kowalewski, Melissa Raguet, the associate editor, and two anonymous referees also improved the manuscript.

References

  1. Altmann J (1980) Baboon mothers and infants. Harvard University Press, CambridgeGoogle 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, Hausfater G, Altmann SA (1988) Determinants of reproductive success in savannah baboons, Papio cynocephalus. In: Clutton-Brock TH (ed) Reproductive success: studies of individiual variation in contrasting breeding systems. University of Chicago Press, Chicago, pp 405–418Google Scholar
  4. 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
  5. Bercovitch FB, Lebron MR, Martinez HS, Kessler MJ (1998) Primigravidity, body weight, and costs of rearing first offspring in rhesus macaques. Am J Primatol 46:135–144PubMedCrossRefGoogle Scholar
  6. Bercovitch FB, Widdig A, Nurnberg P (2000) Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons. Behav Ecol Sociobiol 48:1–11CrossRefGoogle Scholar
  7. Berman CM (1983) Matriline differences and infant development. In: Hinde RA (ed) Primate social relationships: an integrated approach. Sinauer, Sunderland, pp 132–134Google Scholar
  8. 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
  9. Blomquist GE (2009) Fitness-related patterns of genetic variation in rhesus macaques. Genetica 135:209–219PubMedCrossRefGoogle Scholar
  10. Boyce AJ (1983) Computation of inbreeding and kinship coefficients on extended pedigrees. J Heredity 73:400–404Google Scholar
  11. Canli T, Lesch KP (2007) Long story short: the serotonin transporter in emotion regulation and social cognition. Nat Neurosci 10:1103–1109PubMedCrossRefGoogle Scholar
  12. Chapais B (2001) Primate nepotism: what is the explanatory value of kin selection? Int J Primatol 22:203–229CrossRefGoogle Scholar
  13. 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, chap 9. Cambridge University Press, New York, pp 3–10Google Scholar
  14. Charlesworth B (1994) Evolution in age-structured populations, 2nd edn. Cambridge University Press, New YorkGoogle Scholar
  15. Charpentier MJE, Tung J, Altmann J, Alberts SC (2008) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17:2026–2040PubMedCrossRefGoogle Scholar
  16. Chauvin C, Berman CM (2004) Intergenerational transmission of behavior. In: Thierry B, Singh M, Kaumanns W (eds) Macaque societies: a model for the study of social organization, chap 10. Cambridge University Press, New York, pp 209–230Google Scholar
  17. 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, chap 4. University of Chicago Press, Chicago, pp 67–100Google Scholar
  18. Datta SB, Beauchamp G (1991) Effects of group demography on dominance relationships among female primates. I. Mother-daughter and sister-sister relations. Am Nat 138(1):201–226CrossRefGoogle Scholar
  19. Dyke B (1996) PEDSYS: a pedigree database management system users manual. Population Genetics Laboratory, Department of Genetics, Southwest Foundation for Biomedical Research, San AntonioGoogle Scholar
  20. Ellis L (1995) Dominance and reproductive success among nonhuman animals: a cross-species comparison. Ethol Sociobiol 16:257–333CrossRefGoogle Scholar
  21. Galloway LF, Etterson JR (2007) Transgenerational plasticity is adaptive in the wild. Science 318:1134–1136PubMedCrossRefGoogle Scholar
  22. Garant D, Kruuk LEB, Wilkin TA, McCleery RH, Sheldon BC (2005) Evolution driven by differential dispersal within a wild bird population. Nature 433:60–65PubMedCrossRefGoogle Scholar
  23. Groeneveld E, Kovac M (1990) A generalized computing procedure for setting up and solving mixed linear models. J Dairy Sci 73:513–531CrossRefGoogle Scholar
  24. Harcourt AH (1987) Dominance and fertility among female primates. J Zool 213:471–487CrossRefGoogle Scholar
  25. Kappeler PM, Pereira ME (2003) Primate life histories and socioecology. University of Chicago Press, ChicagoGoogle Scholar
  26. Kawai M (1965) On the system of social ranks in a natural troop of Japanese monkeys. I. Basic rank and dependent rank. In: Imanishi K, Altmann SA (eds) Japanese monkeys. Altmann, Chicago, pp 66–86Google Scholar
  27. Kendall MG (1948) Rank correlation methods. Charles Griffin, LondonGoogle Scholar
  28. Kennedy BW, Trus D (1993) Considerations on genetic connectedness between management units under an animal model. J Dairy Sci 71:2341–2352Google Scholar
  29. Kirk KM, Blomberg SP, Duffy DL, Heath AC, Owens IP, Martin NG (2001) Natural selection and quantitative genetics of life-history traits in Western women: a twin study. Evolution 55:423–435PubMedGoogle Scholar
  30. Koenig A (2002) Competition for resources and its behavioral consequences among female primates. Int J Primatol 23:759–783CrossRefGoogle Scholar
  31. Kruuk LEB (2004) Estimating genetic parameters in natural populations using the ‘animal model’. Philos Trans R Soc Lond B Biol Sci 359(1446):873–890PubMedCrossRefGoogle Scholar
  32. Kruuk LEB, Slate J, Pemberton JM, Brotherstone S, Guinness FE, Clutton-Brock TH (2002) Antler size in red deer: heritability and selection but no evolution. Evolution 56:1683–1695PubMedGoogle Scholar
  33. Kruuk LEB, Merilä J, Sheldon BC (2003) When environmental variation short-circuits natural selection. Trends Ecol Evol 18(5):207–209CrossRefGoogle Scholar
  34. Laland KN, Odling-Smee J, Feldman MW (2000) Niche construction, biological evolution, and cultural change. Behav Brain Sci 23(1):131–146; discussion 146–175CrossRefGoogle Scholar
  35. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits. Sinauer, SunderlandGoogle Scholar
  36. Maestripieri D (2003) Similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers. Dev Psychobiol 43:321–327PubMedCrossRefGoogle Scholar
  37. Mrode RA (1996) Linear models for the prediction of animal breeding values, 1st edn. CAB, WallingfordGoogle Scholar
  38. 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
  39. Packer C, Collins DA, Sindimwo A, Goodall J (1995) Reproductive constraints on aggressive competition in female baboons. Nature 373:60–63PubMedCrossRefGoogle Scholar
  40. Pettay JE, Helle S, Jokela J, Lummaa V (2007) Natural selection on female life-history traits in relation to socio-economic class in pre-industrial human populations. PLoS ONE 2(7):e606PubMedCrossRefGoogle Scholar
  41. Pettay JI, Kruuk LEB, Jokela J, Lummaa V (2005) Heritability and genetic constraints of life-history trait evolution in preindustrial humans. Proc Natl Acad Sci U S A 102(8):2838–2843PubMedCrossRefGoogle Scholar
  42. Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, BaltimoreGoogle Scholar
  43. Postma E (2006) Implications of the difference between true and predicted breeding values for the study of natural selection and micro-evolution. J Evol Biol 19:309–320PubMedCrossRefGoogle Scholar
  44. Postma E, Charmantier A (2007) What ‘animal models’ can tell ornithologists about the genetics of wild populations. J Ornithol 148:S633–S642CrossRefGoogle Scholar
  45. Price T, Schluter D (1991) On the low heritability of life history traits. Evolution 45:853–861CrossRefGoogle Scholar
  46. R Development Core Team (2007) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org
  47. Rawlins RG, Kessler MJ (1985) Climate and seasonal reproduction in the Cayo Santiago macaques. Am J Primatol 9:87–99CrossRefGoogle Scholar
  48. Rawlins RG, Kessler MJ (eds) (1986) The Cayo Santiago macaques: history, behavior, and biology. SUNY, AlbanyGoogle Scholar
  49. Roff DA, Mouseau TA (1987) Quantitative genetics of fitness: lessons from Drosophila. Heredity 58:103–118PubMedCrossRefGoogle Scholar
  50. Rossiter MC (1996) Incidence and consequences of inherited environmental effects. Ann Rev Ecolog Syst 27:451–476CrossRefGoogle Scholar
  51. Sade DS (1967) Determinants of dominance in a group of free-ranging rhesus monkeys. In: Altmann SA (ed) Social communication in primates. University of Chicago Press, Chicago, pp 99–114Google Scholar
  52. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308:648–652PubMedCrossRefGoogle Scholar
  53. Silk JB (1984) Measurement of the relative importance of individual selection and kin selection among females of the genus Macaca. Evolution 38(3):553–559CrossRefGoogle Scholar
  54. Silk JB (2002) Kin selection in primate groups. Int J Primatol 23:849–875CrossRefGoogle Scholar
  55. Stearns SC (1989) Trade-offs in life history evolution. Funct Ecol 3:259–268CrossRefGoogle Scholar
  56. 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
  57. Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, HobokenCrossRefGoogle Scholar
  58. Thierry B, Singh M, Kaumanns W (2004) Macaque societies: a model for the study of social organization. Cambridge University Press, New YorkGoogle Scholar
  59. 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
  60. Uller T (2008) Developmental plasticity and the evolution of parental effects. Trends Ecol Evol 23(8):432–438CrossRefGoogle Scholar
  61. van Noordwijk MA, van Schaik CP (1999) The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques, Macaca fascicularis. Primates 40:105–130CrossRefGoogle Scholar
  62. 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
  63. West-Eberhard MJ (2003) Developmental plasticity and evolution. Oxford University Press, New YorkGoogle Scholar
  64. Whitten PL (1983) Diet and dominance among female vervet monkeys Cercopithecus aethiops. Am J Primatol 5:139–159CrossRefGoogle Scholar
  65. Williams-Blangero S, Blangero J (1995) Heritability of age of first birth in captive olive baboons. Am J Primatol 37:233–239CrossRefGoogle Scholar
  66. Wilson AJ (2008) Why h 2 does not always equal V A/V P? J Evol Biol 21(3):647–650PubMedCrossRefGoogle Scholar
  67. Wilson AJ, Pemberton JM, Pilkington JG, Coltman DW, Mifsud DV, Clutton-Brock TH, Kruuk LEB (2006) Environmental coupling of selection and heritability limits evolution. PLoS Biol 4(7):e216PubMedCrossRefGoogle Scholar
  68. Wolf JB, Brodie III ED, Cheverud JM, Moore AJ, Wade MJ (1998) Evolutionary consequences of indirect genetic effects. Trends Ecol Evol 13(2):64–69CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of AnthropologyUniversity of MissouriColumbiaUSA

Personalised recommendations