The Evolution of Genetic Systems Can Be Understood from the Fate of Alleles That Modify Them

The idea of modifier alleles provides a key conceptual tool for understanding how genetic systems evolve through selection between individuals. Modifiers are hypothetical genetic variants that cause no direct effect on fitness, but that do alter some feature of the genetic system. We have already come across this idea when we discussed the evolution of female preferences for mating with different kinds of males (see Chapter 20 Notes). In that case, a modifier allele alters a female’s choice of mate without changing the number of offspring she raises. In reality, alleles are likely to almost always change fitness to some extent. However, understanding modifier alleles identifies the selection that is caused specifically by its effect on the genetic system. This gives a good indication of the direction in which the system evolves, which does not require that we know the actual genetic details.

Selection on modifiers must be indirect because by definition they do not alter fitness directly. Instead, selection acts on them because they become associated with alleles that do affect fitness. In other words, modifier alleles can increase only if they come into linkage disequilibrium with alleles, or combinations of alleles, that are themselves increasing in frequency because they are favored by direct selection. This is an example of a hitchhiking effect in which a neutral allele increases because it is associated with selected alleles. When we discussed hitchhiking on pages 485–486, however, we were concerned with random linkage disequilibrium, produced by random genetic drift. Here, we will be concerned with systematic associations that build up because of the effect of the modifier on the genetic system. Only consistent associations between modifiers and selected alleles can lead to a systematic change in the genetic system. We will see several examples in Chapter 23 (e.g., Figs. 23.3 and 23.13E). One general point is worth making here, however. Because the indirect selection on the modifier depends on linkage disequilibria, which are broken up by recombination (pp. 432–435), it is tightly linked modifiers that are most effective at changing the genetic system. Moreover, because the process depends on genetic factors such as the degree of linkage, it will not in general lead to an optimal outcome. This emphasizes that we need to make detailed population genetic arguments rather than simply finding what would be good for the species as a whole.