Redundant Gene Functions and Natural Selection

Redundant gene functions are ubiquitous, and they are a potentially important source of evolutionary innovations on the biochemical level. It is therefore highly desirable to understand the mechanisms governing their evolution. Gene duplication is clearly a prominent mechanism generating redundant genes. However, because redundancy provides a protective effect against deleterious mutations, natural selection might be involved in generating and maintaining partial redundancy. Although much experimental data on redundant genes has been accumulated, no data is available that could elucidate what role selection has in their evolution. As a first step towards answering this question, a conceptually simple mathematical model for the evolution of redundancy is introduced. Its main result is that selection can not only maintain, but also increase redundancy among genes in a population provided (i) that mutation generates sufficient variation in redundancy, and (ii) that populations are large. The population biological process at work is somewhat unusual. Selection does not act on the (nonexisting) differential fitness between individuals with different degrees of redundancy. Rather, it acts through the low number of offspring with deleterious mutations that individuals with redundant genes will generate. Moreover, even if populations are small and variation in redundancy is low, selection will substantially slow the ``decay'' of redundancy caused by mutation and genetic drift. Methodological problems in determining degrees of redundancy experimentally are discussed, as well as issues concerning the relation of redundancy to genetic canalization. The latter two phenomena necessitate a differentiated view of neutral mutations necessary, where some neutral mutations are only neutral because their effects on gene products are absorbed by the epigenetic system.