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

Abstract

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.

The Association Among Gene Expression Responses to Nine Abiotic Stress Treatments in Arabidopsis thaliana

“…The degree to which stress-resistance traits depend on a large vs. a small number of loci is unclear and has been the subject of long-standing debate (Hoffmann and Parsons 1991). A number of quantitative genetic studies have attributed stress-resistant phenotypes to one or a few genes of major effect (e.g., Fatt and Dougherty 1963;Parsons et al 1969;Blum 1988;Macnair 1991;Lenski and Bennett 1993). However, these findings have often been difficult to interpret, since it is generally difficult to distinguish between the effects of many loci of small effect and a few loci of major effect (Barton and Turelli 1990).…”

Constraints on adaptive mutations in the codling moth Cydia pomonella (L.): measuring fitness trade-offs and natural selection

“…An adapted form may suffer a disadvantage relative to the ancestral form if, when reintroduced in its ancestral environment, the newly favoured character interferes with its ancestral function: a disadvantage regarded as the cost of pleiotropy (Uyenoyama, 1986). Limits to evolution by natural selection therefore arise if pleiotropic effects associated with novel mutations have negative impacts on other fitness-enhancing components (McNair, 1991). Quantitative genetic models provide critical informations on the genetic relationships that may evolve during adaptation in a new environment, but also translate the impact of the pleiotropic effects of newly selected genes on adapted genetic architectures in terms of fitness trade-offs (Holloway et al, 1990;Tienderen, 1997).…”

Change in genetic architecture resulting from the evolution of insecticide resistance: a theoretical and empirical analysis

“…In the field, because of the massive doses used, selection for resistance to pesticides often operates at the very extreme of the phenotypic distribution of resistance (Macnair, 1991;McKenzie & Batterham, 1994). Under such strong selection intensity, genes with major effects are required for individuals to colonize, or to persist in, the pesticide-treated environments (Hedrick & McDonald, 1980;Wright, 1982;Lande, 1983;Charlesworth, 1990;Macnair, 1991; McKenzie & Batterham, 1994;Jasieniuk et a!., 1995).…”

“…Under such strong selection intensity, genes with major effects are required for individuals to colonize, or to persist in, the pesticide-treated environments (Hedrick & McDonald, 1980;Wright, 1982;Lande, 1983;Charlesworth, 1990;Macnair, 1991; McKenzie & Batterham, 1994;Jasieniuk et a!., 1995). Accordingly, in the field, the evolution of resistance to insecticides appears to be mostly the result of the action of one or a few genes with major effects, and secondarily of genes with minor effects (Wood, 1981;Roush & McKenzie, 1987;Tabashnik *Correspondence.…”