Evolutionary Ecology

, Volume 12, Issue 6, pp 739–750 | Cite as

Good genes, old age and life-history trade-offs

  • Hanna Kokko


The possibility of using old age of a mate as an indicator of genetic quality is currently controversial. Early verbal models as well as a recent simulation study noted that female choice for old mates is beneficial because longevity indicates viability in the current environment. In contrast, a quantitative genetic model of the relationship between age and breeding value of fitness casts strong doubts on the mechanism. The present analysis shows, however, that these doubts are mainly the result of assuming that all variation among individuals arises from differences in allocation between components of fitness. This neglects the possibility of variability in condition as a whole. Instead, when allowing for persistent variability in condition and assuming optimal reaction norms in allocation, it is shown that correlations between survival and genetic quality or fitness can easily be established at all ages. On the other hand, the results also suggest that the validity of verbal arguments is limited, and counterexamples can be generated where low-quality individuals should invest more in survival. Therefore, resolution of the old age indicator problem requires specification of the constraints acting on life-history characteristics.

age indicator mechanism good genes life-history trade-offs mate choice sexual selection 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Alatalo, R.V., Lundberg, A. and Glynn, C. (1986) Female pied flycatchers choose territory quality and not male characteristics. Nature 323, 152–153.Google Scholar
  2. Alatalo, R.V., Gustafsson, L. and Lundberg, A. (1990) Phenotypic selection of heritable size traits: Environmental variance and genotypic response. Am. Nat. 135, 464–471.Google Scholar
  3. Andersson, M. (1986) Evolution of condition-dependent sex ornaments and mating preferences: Sexual selection based on viability differences. Evolution 40, 804–816.Google Scholar
  4. Andersson, M. (1994) Sexual Selection. Princeton University Press, Princeton, NJ.Google Scholar
  5. Bellman, R.E. and Dreyfus, S.E. (1962) Applied Dynamic Programming. Princeton University Press, Princeton, NJ.Google Scholar
  6. Berven, K.A. (1981) Mate choice in the wood frog, Rana sylvatica. Evolution 35, 707–722.Google Scholar
  7. Burley, N. (1981) Mate choice by multiple criteria in a monogamous species. Am. Nat. 117, 515–526.Google Scholar
  8. Charlesworth, B. (1990) Optimization models, quantitative genetics and mutation. Evolution 44, 520–538.Google Scholar
  9. Clinton, W.L. and Le Boeuf, B.J. (1993) Sexual selection's effects on male life-history and the pattern of male mortality. Ecology 74, 1884–1892.Google Scholar
  10. Clutton-Brock, T.H. (ed.) (1988) Reproductive Success. University of Chicago Press, Chicago, IL.Google Scholar
  11. Conner, J. (1989) Older males have higher insemination success in a beetle. Anim. Behav. 38, 503–509.Google Scholar
  12. Cordts, R. and Partridge, L. (1996) Courtship reduces longevity of male Drosophila melanogaster. Anim. Behav. 52, 269–278Google Scholar
  13. Côté, I.M. and Hunte, W. (1993) Female redlip blennies prefer older males. Anim. Behav. 46, 203–205.Google Scholar
  14. Enstrom, D.A. (1993) Female choice for age-specific plumage in the orchard oriole: Implications for delayed plumage maturation. Anim. Behav. 45, 435–442.Google Scholar
  15. Falconer, D.S. and Mackay, T.F.C. (1996) Introduction to Quantitative Genetics, 4th edn. Longman, Harlow.Google Scholar
  16. Grafen, A. (1990) Sexual selection unhandicapped by the Fisher process. J. Theor. Biol. 144, 475–516.Google Scholar
  17. Grant, B.R. and Grant, D.P.R (1987) Mate choice in Darwin's finches. Biol. J. Linn. Soc. 32, 247–270.Google Scholar
  18. Gustafsson, L., Qvarnström, A. and Sheldon, B. (1995) Trade-offs between life-history traits and a secondary sexual character in male collared flycatchers. Nature 375, 311–313.Google Scholar
  19. Halliday, T.R. (1978) Sexual selection and mate choice. In Behavioral Ecology: An Evolutionary Approach (J.R. Krebs and N.B. Davies, eds), pp. 180–213. Blackwell, London.Google Scholar
  20. Halliday, T.R. (1983) The study of mate choice. In Mate Choice (P. Bateson, ed.), pp. 3–32. Cambridge University Press, Cambridge.Google Scholar
  21. Halliday, T.R. and Verrell, P.A. (1988) Body size and age in amphibians and reptiles. J. Herpetol. 22, 253–265.Google Scholar
  22. Hansen, T.F. and Price, D.K. (1995) Good genes and old age: Do old mates provide superior genes? J. Evol. Biol. 8, 759–778.Google Scholar
  23. Hasselquist, D., Bensch, S. and von Schantz, T. (1996) Correlation between male song repertoire, extra-pair paternity and offspring survival in the great reed warbler. Nature 381, 229–232.CrossRefGoogle Scholar
  24. Hill, G.E. (1990) Female house finches prefer colourful males: Sexual selection for a condition-dependent trait. Anim. Behav. 40, 563–572.Google Scholar
  25. Houle, D. (1991) Genetic covariance of fitness correlates: What genetic correlations are made of and why it matters. Evolution 45, 630–648.Google Scholar
  26. Houle, D., Morikawa, B. and Lynch, M. (1996) Comparing mutational variabilities. Genetics 143, 1467–1483.PubMedGoogle Scholar
  27. Howard, R.D., Whiteman, H.H. and Schueller, T.I. (1994) Sexual selection in American toads: A test of a good-genes hypothesis. Evolution 48, 1286–1300.Google Scholar
  28. Iwasa, Y., Pomiankowski, A. and Nee, S. (1991) The evolution of costly mate preferences. II. The ‘handicap’ principle. Evolution 45, 1431–1442.Google Scholar
  29. Johnstone, R.A. (1995) Sexual selection, honest advertisement and the handicap principle: Reviewing the evidence. Biol. Rev. 70, 1–65.PubMedGoogle Scholar
  30. Koenig, W.D. (1991) Levels of female choice in the white-tailed skimmer Plathemis lydia (Odonata: Libellulidae). Behaviour 119, 193–224.Google Scholar
  31. Kokko, H. (1997) Evolutionarily stable strategies of age-dependent sexual advertisement. Behav. Ecol. So ciobiol. 41, 99–107.Google Scholar
  32. Kokko, H. and Lindström, J. (1996) Evolution of female preference for old mates. Proc. R. Soc. Lond. B 263, 1533–1538.Google Scholar
  33. Komers, P.E. and Dhindsa, M.S. (1989) Influence of dominance and age on mate choice in black-billed magpies: An experimental study. Anim. Behav. 37, 645–655.Google Scholar
  34. Korpimäki, E. (1989) Mating system and mate choice of Tengmalm's owls Aegolius funerus. Ibis 131, 41–50.Google Scholar
  35. Manning, J.T. (1985) Choosy females and correlates of male age. J. Theor. Biol. 116, 349–395.Google Scholar
  36. Medawar, P.B. (1946) Old age and natural death. Mod. Q. 1, 30–56.Google Scholar
  37. Nur, N. and Hasson, O. (1984) Phenotypic plasticity and the handicap principle. J. Theor. Biol. 110, 275–297.Google Scholar
  38. Olsson, M. and Madsen, T. (1995) Female choice on male quantitative traits in lizards-Why is it so rare? Behav. Ecol. Sociobiol. 36, 179–184.Google Scholar
  39. Partridge, L. and Endler, J.A. (1987) Life-history constraints on sexual selection. In Sexual Selection: Testing the Alternatives (J.W. Bradbury and M.B. Andersson, eds), pp. 265–277. Wiley, Berlin.Google Scholar
  40. Partridge, L. and Sibly, R. (1991) Constraints in the evolution of life histories. Phil. Trans. R. Soc. Lond. B 332, 3–13.Google Scholar
  41. Petrie, M. (1993) Do peacock's trains advertise age? J. Evol. Biol. 6, 443–448.Google Scholar
  42. Pomiankowski, A. and Møller, A.P. (1995) A resolution of the lek paradox. Proc. R. Soc. Lond. B 260, 21–29.Google Scholar
  43. Poole, J.H. (1989) Mate guarding, reproductive success and female choice in African elephants. Anim. Behav. 37, 842–849.Google Scholar
  44. Price, T. and Schluter, D. (1991) On the low heritability of life-history traits. Evolution 45, 853–861.Google Scholar
  45. Price, T., Schluter, D. and Heckman, N.E. (1993) Sexual selection when the female directly benefits. Biol. J. Linn. Soc. 48, 187–211.Google Scholar
  46. Roff, D.A. (1992) The Evolution of Life Histories. Chapman & Hall, London.Google Scholar
  47. Rose, M.R. (1985) The evolution of senescence. In Evolution: Essays in Honour of John Maynard Smith (P.J. Greenwood, P.H. Harvey and M. Slatkin, eds), pp. 117–128. Cambridge University Press, Cambridge.Google Scholar
  48. Rose, M.R. (1991) The Evolutionary Biology of Aging. Oxford University Press, Oxford.Google Scholar
  49. Rowe, L. and Houle, D. (1996) The lek paradox and the capture of genetic variance by condition-dependent traits. Proc. R. Soc. Lond. B 263, 1415–1421.Google Scholar
  50. Schluter, D., Price, T.D. and Rowe, L. (1991) Conflicting selection pressures and life-history trade-offs. Proc. R. Soc. Lond. B 246, 11–17.Google Scholar
  51. Sundberg, J. and Dixon, A. (1996) Old, colourful male yellowhammers, Emberiza citrinella, benefit from extra-pair copulations. Anim. Behav. 52, 113–122.Google Scholar
  52. Trivers, R. (1972) Parental investment and sexual selection. In Sexual Selection and the Descent of Man 1871–1971 (B. Campbell, ed.), pp. 139–179. Aldine Press, Chicago, IL.Google Scholar
  53. van Noordwijk, A.J. and de Jong, G. (1986) Acquisition and allocation of resources: Their influence on variation in life-history tactics. Am. Nat. 128, 137–142.CrossRefGoogle Scholar
  54. van Rhijn, J. and Groothuis, T. (1987) On the mechanism of mate selection in black-headed gulls. Behaviour 100, 134–169.Google Scholar
  55. Watt, W.B., Carter, P.A. and Donohue, K. (1986) Females’ choice of ‘good genotypes’ as mates is promoted by an insect mating system. Science 233, 1187–1190.PubMedGoogle Scholar
  56. Williams, C.G. (1957) Pleiotropy, natural selection and the evolution of senescence. Evolution 11, 398–411.Google Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Hanna Kokko
    • 1
  1. 1.Department of Ecology and Systematics, Division of Population BiologyUniversity of HelsinkiHelsinkiFinland

Personalised recommendations