The evolution of evolvability in genetic linkage patterns.

A number of factors have been proposed that may affect the capacity for an evolutionary system to generate adaptation. One that has received little recent attention among biologists is linkage patterns, or the ordering of genes on chromosomes. In this study, a simple model of genetic interactions, implemented in an evolutionary simulation, demonstrates that clustering of epistatically interacting genes increases the rate of adaptation. Moreover, long-term evolution with inversion can reorganize linkage patterns from random gene ordering into this more modular organization, thereby facilitating adaptation. These results are consistent with a large body of biological observations and some mathematical theory. Although linkage patterns are neutral with respect to individual fitness in this model, they are subject to lineage level selection for evolvability. At least two candidate mechanisms may contribute to improved evolvability under epistatic clustering: clustering may reduce interference between selection on different traits, and it may allow the simultaneous optimization of different recombination rates for gene pairs with additive and epistatic fitness effects.