(Epi)mutation rates and the evolution of composite trait architectures

Mutation rates vary widely along genomes and across inheritance systems. This suggests that complex traits – resulting from the contributions of multiple determinants – might be composite in terms of the underlying mutation rates. Here we investigate through mathematical modeling whether such an heterogeneity may drive changes in a trait’s architecture, especially in fluctuating environments where phenotypic instability can be beneficial. We first identify a convexity principle, related to the shape of the trait’s fitness function, setting conditions under which composite architectures should be adaptive or, conversely and more commonly, should be selected against. Simulations reveal, however, that applying this principle to realistic evolving populations requires taking into account pervasive epistatic interactions that take place in the system. Indeed, the fate of a mutation affecting the architecture depends on the (epi)genetic background, itself depending upon the current architecture in the population. We tackle this problem by borrowing the adaptive dynamics framework from evolutionary ecology – where it is routinely used to deal with such resident/mutant dependencies – and find that the principle excluding composite architectures generally prevails. Yet, the predicted evolutionary trajectories will typically depend on the initial architecture, possibly resulting in historical contingencies. Finally, by relaxing the large population size assumption, we unexpectedly find that not only the strength of selection on a trait’s architecture, but also its direction, depend on population size, revealing a new occurrence of the recently coined phenomenon of ‘sign inversion’.