Adaptive evolvability through direct selection instead of indirect, second‐order selection

Abstract

Can evolvability itself be the product of adaptive evolution? To answer this question is challenging, because any DNA mutation that alters only evolvability is subject to indirect, “second order” selection on the future effects of this mutation. Such indirect selection is weaker than “first‐order” selection on mutations that alter fitness, in the sense that it can operate only under restrictive conditions. Here I discuss a route to adaptive evolvability that overcomes this challenge. Specifically, a recent evolution experiment showed that some mutations can enhance both fitness and evolvability through a combination of direct and indirect selection. Unrelated evidence from gene duplication and the evolution of gene regulation suggests that mutations with such dual effects may not be rare. Through such mutations, evolvability may increase at least in part because it provides an adaptive advantage. These observations suggest a research program on the adaptive evolution of evolvability, which aims to identify such mutations and to disentangle their direct fitness effects from their indirect effects on evolvability. If evolvability is itself adaptive, Darwinian evolution may have created more than life's diversity. It may also have helped create the very conditions that made the success of Darwinian evolution possible.

Experimental evolution of evolvability

“…The interplay between mutations conferring immediate benefit to cells and evolvability over the longterm [54] is best illustrated by the convoluted mutational history of pflu0185 that preceded its hypermutator status. Critical to obtaining this status were a series of mutations leading to elevated pflu0185 transcription.…”

Evolvability: filling the explanatory gap between adaptedness and the long-term mathematical conception of fitness

“…Studies have shown that some neutral, or even slightly deleterious, changes can increase prospects of long-term evolutionary success by augmenting the capacity to generate new adaptive variation. For example, the accumulation of cryptic variation in robust systems enables further exploration of the adaptive landscape, thus facilitating the acquisition of new adaptive phenotypes (Wagner 2022 , 2023 ). We interpret this to be a case in which long-term fitness is enhanced by an increase in evolvability without affecting adaptedness or even at the expense of it.…”

“…Proponents of evolvability across biology and philosophy use this notion as non-overlapping with fitness but recognize that they are connected in some way. One focal point within the evolvability literature aims to address the ways in which evolvability may enhance fitness and whether evolvability, itself, is an adaptation (Pigliucci 2008 ; Sniegowski and Murphy 2006 ; Wagner 2022 , 2023 ; Wagner and Draghi 2010 ; Wagner and Altenberg 1996 ). However, one might see evolvability and fitness as being at odds with each other, appealing to cases where increases in evolvability seem to involve fitness costs (Chou et al 2011 ; Gibson et al 2017 ; Smith 1971 ).…”

Exploring the expanse between theoretical questions and experimental approaches in the modern study of evolvability

“…This skepticism is understandable as a response to overly broad and untestable speculations about evolvability, but also reflects pessimism in light of the difficulty of assigning causation to disparate factors affecting adaptation. In this issue, Wagner ( 2021 ) revisits the idea that many genetic changes contribute to evolvability alongside more direct, potentially beneficial effects. Inspired by recent work showing that adaptation in one environment can improve evolvability in a second, distinct environment (Zheng et al, 2019 , 2020 ), Wagner argues for an expansion of the evolvability research program beyond evolvability modifiers with neutral or weak direct effects on fitness.…”