Mutability and evolvability: Indirect selection for mutability

Abstract

How readily does mutability evolve? Petrie and Roberts (2007) have recently described a theoretical example of increased mutation rate based on female choice. Mutator alleles can also be favored by strong selection for phenotypic variation, such as that imposed by immunological attack against pathogens, together with stable linkage to beneficial mutations, provided by haploidy in microorganisms. But the special conditions required for these examples highlight two assumptions that have framed discussion of mutation-rate evolution for most of the past century (for example, Bataillon, 2000; Bell, 2005; Cotton and Pomiankowski, 2007). First, although close linkage may allow a mutator to hitchhike on selection for a beneficial allele, recombination, at least in sexually reproducing populations, will eventually separate the two. Second, because most non-neutral mutations are deleterious, the net effect of any mutator must be fitness reduction. Thus, 'natural selection of mutation rates has only one possible direction, that of reducing the frequency of mutation to zero' (Williams, 1966). Regrettably, this classic but overstated conclusion remains influential. Even well-established exceptions like the 'contingency loci' of some bacteria are routinely marginalized as special cases that depend on extreme and/or unusual circumstances (Sniegowski and Murphy, 2006).