View Program - 2022 Population, Evolutionary, and Quantitative Genetics Conference

If mutations are highly pleiotropic, that is if each mutation affects many traits, it is difficult for natural selection to improve fitness, a phenomenon known as “the cost of complexity”. One solution to this challenge is modularity, where pleiotropy primarily occurs among genes in the same module but is limited between them. However, it was recently suggested that modularity creates a new challenge termed “evolutionary stalling”. In rapidly evolving populations with limited recombination, evolutionary stalling occurs when beneficial mutations in one module are ‘wasted’ because they cannot successfully compete against those in another module. A recent theoretical work shows that evolutionary stalling of a module depends on its rate of adaptation relative to other modules under selection, where faster modules adapt and slower modules stall. However, as the organism adapts, we expect that the rate of adaptation of the initially faster modules would generically decline, due to the depletion of the supply of beneficial mutations and diminishing returns epistasis, suggesting that evolutionary stalling may be alleviated during long-term adaptation. Whether such alleviation indeed occurs and under what conditions has not been investigated, and the impacts of long-term adaptation on evolutionary stalling and vice versa are unknown.
Here, we address this question in the Fisher’s Geometric Model with two modules. We find that whether or not evolutionary stalling is alleviated over the long run depends on the architecture of the organism and the strength of selection. In particular, if module adaptation slows down solely due to the depletion of the supply of beneficial mutation, stalling persists unabated. In contrast, evolutionary stalling is alleviated over long times if modules are under equal selection pressures and their adaptation slows down solely due to the diminishing returns epistasis. In the more realistic cases where modules are not under equal selection pressures and/or both depleting supply of mutations and epistasis are in effect, we find that the degree of evolutionary stalling changes over time, but it is not necessarily alleviated in the long run. These results suggest that evolutionary stalling imposes a fundamental constraint on the speed of adaptation of individual modules in organisms with limited recombination and that this constraint may not be consistently alleviated by natural selection, even over long time scales.

A fundamental constraint on adaptation of a biological module