Predictions of Patterns of Response to Artificial Selection in Lines Derived from Natural Populations
Zhang, Xu-Sheng, Hill, William G., Genetics
The pattern of response to artificial selection on quantitative traits in laboratory populations can tell us something of the genetic architecture in the natural population from which they were derived. We modeled artificial selection in samples drawn from natural populations in which variation had been maintained by recurrent mutation, with genes having an effect on the trait, which was subject to real stabilizing selection, and a pleitropic effect on fitness (the joint-effect model). Natural selection leads to an inverse correlation between effects and frequencies of genes, such that the frequency distribution of genes increasing the trait has an extreme U-shape. In contrast to the classical infinitesimal model, an early accelerated response and a larger variance of response among replicates were predicted. However, these are reduced if the base population has been maintained in the laboratory for some generations by random sampling prior to artificial selection. When multiple loci and linkage are also taken into account, the gametic disequilibria generated by the Bulmer and Hill-Robertson effects are such that little or no increase in variance and acceleration of response in early generations of artificial selection are predicted; further, the patterns of predicted responses for the joint-effect model now become close to those of the infinitesimal model. Comparison with data from laboratory selection experiments shows that, overall, the analysis did not provide clear support for the joint-effect model or a clear case for rejection.
MANY artificial selection experiments have been applied to populations maintained in the laboratory or recently derived from natural populations. Although mainly directed to problems in animal and plant improvement, they also have implications for evolutionary biology and have the advantage over analyses of natural populations in that parameters such as selection pressures are known (HILL and CABALLERO 1992; FALCONER and MACKAY 1996). Information can be extracted from these experiments to infer the genetic architecture of quantitative traits and to check the validity of theoretical models of the maintenance of polygenic variation.
To interpret the observed levels of quantitative genetic variation in natural populations, the two classical models based on mutation-selection balance are real stabilizing selection and pleiotropic selection. In the former, natural selection is assumed to act directly and solely on the quantitative trait (KIMURA 1965; TURELLI 1984; BURGER 2000), while in the latter natural selection is assumed to act through pleiotropic side effects of mutant alleles on fitness (ROBERTSON 1967; HILL and KEIGHTLEY 1988; BARTON 1990). The response to directional selection for a quantitative trait under the pleiotropic model has been considered in several theoretical studies (HILL and KEIGHTLEY 1988; BARTON 1990; HILL and MBAGA 1998). The conclusion is that artificial selection is likely to overwhelm natural selection against mutations due to their deleterious effects, and large and sustained response is possible despite the associated loss of fitness from the fixation of deleterious mutations (BARTON 1990; HILL and MBAGA 1998). This is generally in line with observations from selection experiments. We have recently constructed models in which mutants have effects both on the trait, which is subject to some stabilizing selection, and on overall fitness due to directional or stabilizing selection through pleiotropic effects on all other traits (ZHANG and HILL 2002; ZHANG et al. 2004a). With typical estimated values of mutation and selection parameters, the joint-effect model of pleiotropic and real stabilizing selection provides a plausible explanation for the high levels of genetic variation observed in quantitative traits. Furthermore, the joint-effect model can explain data from laboratory experiments on the effect of bottlenecking on fitness and morphological traits (ZHANG et al. …