, Volume 84, Issue 3, pp 213–219 | Cite as

Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: the limits to natural selection

  • M. R. Macnair
Research Articles


Standard population genetic theory suggests that adaptation should normally be achieved by the spread of many genes each of small effect (polygenes), and that adaptation by major genes should be unusual. Such models depend on consideration of the rates of acquisition of adaptation. In practice, adaptation to pollutants and anthropogenic toxins has most frequently been achieved by the spread of major genes. A simple model is developed to explain this discrepancy, in which the determining factor is not the rate of spread, but the maximum response achievable under the two contrasting models of polygenic or major gene inheritance. In the short term, for a given mean and genetic variance, characters in which the additive genetic variance is produced by the segregation of many genes of small effect at intermediate gene frequencies are unable to produce as large a response to directional selection as characters in which the variance is caused by genes of large effect at low frequency. If the ‘target’ for selection is a long way from the mean prior to selection (as it may well be for adaptation to novel anthropogenic stresses) then adaptation can only be achieved by species possessing major genes. The model is discussed with reference to the example of heavy metal tolerance in plants.

Key words

Pollution heavy metal tolerance major genes 


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  1. Al-Hiyaly, S. A., McNeilly, T. & Bradshaw, A. D., 1988. The effects of zinc contamination from electricity pylons-evolution in a replicated situation. New Phytol. 110: 571–580.Google Scholar
  2. Antonovics, J., 1968. Evolution in closely adjacent plant populations. V. Evolution of self fertility. Heredity 23: 219–238.Google Scholar
  3. Antonovics, J., 1976. The nature of limits to natural selection. Ann. Missouri Bot. Gard. 63: 224–247.Google Scholar
  4. Antonovics, J., Bradshaw, A. D. & Turner, R. J., 1971. Heavy metal tolerance in plants. Adv. Ecol. Res. 7: 1–85.Google Scholar
  5. Baker, A. J. M., 1987. Metal tolerance. New Phytol. 106 (suppl.): 93–111.Google Scholar
  6. Barton, N. H. & Turelli, M., 1989. Evolutionary quantitative genetics: how little do we know? Ann. Rev. Genet. 23: 337–370.Google Scholar
  7. Bradshaw, A. D., 1984. The importance of evolutionary ideas in ecology-and vice versa. Pp 1–26. In: Shorrocks, B. (Ed) Evolutionary Ecology. Blackwell, Oxford.Google Scholar
  8. Coyne, J. A. & Lande, R., 1985. The genetic basis of species differences in plants. Am. Nat. 126: 141–145.Google Scholar
  9. Crow, J. F., 1957. Genetics of insect resistance to chemicals. Ann. Rev. Ent. 2: 227–246.Google Scholar
  10. Gartside, D. W. & McNeilly, T., 1974. The potential for evolution of heavy metal tolerance in plants. II. Copper tolerance in normal populations of different plant species. Heredity 32: 335–348.Google Scholar
  11. Greaves, J. H., Rennison, B. D. & Redfern, R., 1976. Resistance of the ship rat, Rattus rattus L., to warfarin. J. stored Prod. Res. 12: 65–70.Google Scholar
  12. Jacobs, B. F., Duesing, J. H., Antonovics, J. & Patterson, D. T., 1987. Growth performance of triazine-resistant and-susceptible biotypes of Solanum nigrum over a range of temperatures. Can. J. Bot. 66: 847–850.Google Scholar
  13. Kettlewell, H. B. D., 1973. The evolution of melanism. Clarendon Press, Oxford.Google Scholar
  14. Lande, R., 1975. The maintenance of genetic variability by mutation in a polygenic character with linked loci. Genet. Res., Camb. 26: 221–235.Google Scholar
  15. Lande, R., 1981. The minimum number of genes contributing to quantitative variation between and within populations. Genetics 99: 541–553.Google Scholar
  16. Lande, R., 1983. The response to selection on major and minor mutations affecting a metrical trait. Heredity 50: 47–65.Google Scholar
  17. Lees, D. R., 1981. Industrial Melanism: Genetic adaptation of animals to air pollution. Pp 129–176. In: Bishop, J. A. & Cook, L. M. (Eds) The Genetic Consequences of Man Made Change. Academic Press, London.Google Scholar
  18. Macnair, M. R., 1981. Tolerance of Higher plants to toxic materials. Pp 177–207. In: Bishop, J. A. & Cook, L. M., (Eds) The Genetic Consequences of Man Made Change. Academic Press, London.Google Scholar
  19. Macnair, M. R., 1983. The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50: 283–293.Google Scholar
  20. Macnair, M. R., 1987. Heavy metal tolerance in plants: a model evolutionary system. TREE 2: 354–359.Google Scholar
  21. Macnair, M. R., 1989. The genetics of metal tolerance in natural populations. Pp 235–254. In: J. Shaw, (Ed) Heavy metal tolerance in plants: Evolutionary aspects. CRC press, Boca Raton.Google Scholar
  22. Macnair, M. R. & Cumbes, Q. J., 1989. The genetic architecture of interspecific variation in Mimulus. Genetics 122: 211–222.Google Scholar
  23. Mallet, J., 1989. The evolution of insecticides resistance: have the insects won? TREE 4: 336–340.Google Scholar
  24. Mather, K., 1973. Genetical structure of populations. Chapman and Hall, London.Google Scholar
  25. Maynard Smith, J., 1989. Evolutionary Genetics. Oxford University Press, Oxford.Google Scholar
  26. Orr, H. A. & Coyne, J. A., 1991. The genetics of adaptation: a reassessment. (in press).Google Scholar
  27. O'Reilly, R. A., Aggeler, P. M., Hoag, M. S., Leong, L. S. & Kropotkin, B. A., 1964. Hereditary transmissions of exceptional resistance to coumarin anti-coagulant drugs. New Engl. J. Med. 271: 809–815.Google Scholar
  28. Parsons, P. A., 1987. Evolutionary rates under Environmental Stress. Evol. Biol. 21: 311–347.Google Scholar
  29. Schat, H. & ten Bookum, W. M., 1991. Genetic control of copper tolerance in Silene vulgaris Heredity (in press).Google Scholar
  30. Sheppard, P. M., Turner, J. R. G., Brown, K. S., Benson, W. W. & Singer, M. C., 1985. Genetics and the evolution of Muellerian mimicry in Heliconius butterflies. Phil. Trans. Roy Soc. Lond., B. 308: 433–610.Google Scholar
  31. Snape, J. W., Angus, W. J., Parker, B. & Leckie, D., 1987. The chromosomal locations in wheat of genes conferring differential response to the wild oat herbicide, difenzoquat. J. agric. sci., Camb. 108: 543–548.Google Scholar
  32. Turelli, M., 1984. Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle. Theor. Pop. Biol. 25: 138–193.Google Scholar
  33. Turner, J. R. G., 1978. Butterfly mimicry: the genetical evolution of an adaptation. Evol. Biol. 10: 163–206.Google Scholar
  34. Wallace, M. E. & MacSwiney, F. J., 1976. A major gene controlling warfarin resistance in the house mouse. J. Hyg. Camb. 76: 173–181.Google Scholar
  35. Wood, R. J., 1981. Insecticide resistance: genes and mechanisms. Pp 53–96. In: Bishop, J. A. & Cook, L. M. (Eds). The Genetic Consequences of Man Made Change. Academic Press. London.Google Scholar
  36. Wu, L., Bradshaw, A. D. & Thurman, D. A., 1975. The potential for evolution of heavy metal tolerance in plants. III. The rapid evolution of copper tolerance in Agrostis stolonifera. Heredity 34: 165–187.Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • M. R. Macnair
    • 1
  1. 1.Department of Biological SciencesUniversity of Exeter, Hatherly LaboratoriesExeterEngland

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