Evolutionary Capacitance May Be Favored by Natural Selection
Masel, Joanna, Genetics
Evolutionary capacitors phenotypically reveal a stock of cryptic genetic variation in a reversible fashion. The sudden and reversible revelation of a range of variation is fundamentally different from the gradual introduction of variation by mutation. Here I study the invasion dynamics of modifiers of revelation. A modifier with the optimal rate of revelation m^sub opt^ has a higher probability of invading any other population than of being counterinvaded. m^sub opt^ varies with the population size N and the rate θ at which environmental change makes revelation adaptive. For small populations less than a minimum cutoff N^sub min^, all revelation is selected against. N^sub min^ is typically quite small and increases only weakly, with θ^sup -1/2^. For large populations with N > 1/θ, m^sub opt^ is ~1/ N. Selection for the optimum is highly effective and increases in effectiveness with larger N [much greater than] 1/θ. For intermediate values of N, m^sub opt^ is typically a little less than θ and is only weakly favored over less frequent revelation. The model is analogous to a two-locus model for the evolution of a mutator allele. It is a fully stochastic model and so is able to show that selection for revelation can be strong enough to overcome random drift.
ONE of the major puzzles of evolutionary biology is how sufficient phenotypic variation can be generated and maintained to form the basis of an adaptive response to novel environments. A population with very little phenotypic variation will be well adapted to a stable environment in the short term, but may be unable to respond to a change in the environment.
In a well-adapted population almost all newly introduced variation is likely to be deleterious. Variation is eliminated through selection, at the cost of a mutation load. Selective pressure to reduce the load tends to favor the reduction of variation by a variety of means, including reducing the mutation rate (SNIEGOWSKI et al. 2000) and buffering against the effects of mutations that do occur (WAGNER 1996; NOWAK et al. 1997; ESHEL and MATESSI 1998; RICE 1998, 2002; VAN NIMWEGEN et al. 1999; WILKE et al. 2001; RRAKAUER and PLOTKIN 2002; DE VISSER et al. 2003). This last mechanism is known as canalization and can lead to the buildup of hidden or cryptic genetic variation.
In recent years, a number of mechanisms have been shown to tap into the pool of cryptic genetic variation, revealing heritable phenotypic variation. These include partial loss of function of the heat-shock protein Hsp90 (RUTHERFORD and LINDQUIST 1998; QUEITSCH et al. 2002) and the appearance of the yeast prion [PSI+] (TRUE and LINDQUIST 2000). In each case, genetic variation that was previously hidden is "turned on" at a single stroke. It remains on for a number of generations, either because of the continuation of environmental stress or because of epigenetic inheritance, but it can be turned off later.
These mechanisms have the potential to promote evolvability, in the sense of revealing potentially adaptive phenotypic variation at a time when it might most be needed. They act as "capacitors." Following this analogy, variation gradually produced by mutation is stored in a hidden form by the capacitor. When needed, this variation can be released, and the occasional revelation of latent variation may lead to evolutionary innovations.
It is very controversial, however, whether evolutionary capacitors may be the product of natural selection for increased evolvability (DiCKiNSON and SEGER 1999; WAGNER et al. 1999; PARTRIDGE and BARTON 2000; BROOKFIELD 2001; PAL 2001; MEIKLEJOHN and HARTL 2002; RUDEN et al. 2003). Any costs of an evolutionary capacitor are borne immediately, while benefits typically lie in the future. Based largely on work on mutator alleles, the general consensus among population geneticists is that it is very difficult for natural selection to favor an evolvability allele (SNIEGOWSKI et al. …