(Epi)mutation Rates and the Evolution of Composite Trait Architectures.

Publisher: University of Chicago Press Country of Publication: United States NLM ID: 2984688R Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1537-5323 (Electronic) Linking ISSN: 00030147 NLM ISO Abbreviation: Am Nat Subsets: MEDLINE

Publication: Chicago, IL : University of Chicago Press
Original Publication: Salem, Mass. : Essex Institute

Models, Genetic* ; Mutation Rate* ; Biological Evolution*; Phenotype ; Selection, Genetic ; Epistasis, Genetic ; Mutation

AbstractMutation 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 a 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, which itself depends on 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 identified phenomenon coined "sign inversion."

Keywords: adaptive dynamics; fluctuating environment; genetic architecture; mutation rate; nongenetic inheritance; sign inversion

Date Created: 20240823 Date Completed: 20240823 Latest Revision: 20240823

20240826

10.1086/731461

39179232