Testing the adaptive walk model of gene evolution

Understanding the dynamics of species adaptation to their environments has long been a central focus of the study of evolution. Early adaptive theories proposed that populations evolve by “walking” in a fitness landscape. This “adaptive walk” is characterised by a pattern of diminishing returns, where populations further away from their fitness optimum take larger steps than those closer to their optimal conditions. This theory can also be used to understand molecular evolution in time, particularly across genes of different ages. We expect young genes to evolve faster and experience mutations with stronger fitness effects than older genes because they are further away from their fitness optimum. Testing this hypothesis, however, constitutes an arduous task. Young genes are small, encode proteins with a higher degree of intrinsic disorder, are expressed at lower levels, and are involved in species-specific adaptations. Since all these factors lead to increased protein evolutionary rates, they could be masking the effect of gene age. While controlling for these factors, we fitted models of the distribution of fitness effects to population genomic datasets of animals and plants. We found that a gene’s evolutionary age significantly impacts the molecular adaptive rate. Moreover, we observed that substitutions in young genes tend to have larger fitness effects. Our study, therefore, provides the first evidence of an “adaptive walk” model of molecular evolution in large evolutionary timescales.Significant statementHow does molecular adaptation occur? John Maynard Smith was one of the first to address this question by introducing the notion of “adaptive walk”, which defines the “walk” of a gene towards higher fitness. At the start of this walk, genes tend to experience mutations with larger fitness effects than those closer to their fitness peak. Whilst being well-established, this theory has never been tested on large evolutionary timescales. Here, we achieve this by comparing molecular adaptive rates across genes of different ages in plants and animals. We showed that a gene’s age acts as a significant determinant of molecular adaptation, where young genes adapt faster than old ones. We, therefore, provide evidence for an “adaptive walk” through time.

The genetic architecture of a host shift: An adaptive walk protected an aphid and its endosymbiont from plant chemical defenses

Host shifts can lead to ecological speciation and the emergence of new pests and pathogens. However, the mutational events that facilitate the exploitation of novel hosts are poorly understood. Here, we characterize an adaptive walk underpinning the host shift of the aphid Myzus persicae to tobacco, including evolution of mechanisms that overcame tobacco chemical defenses. A series of mutational events added as many as 1.5 million nucleotides to the genome of the tobacco-adapted subspecies, M. p. nicotianae, and yielded profound increases in expression of an enzyme that efficiently detoxifies nicotine, both in aphid gut tissue and in the bacteriocytes housing the obligate aphid symbiont Buchnera aphidicola. This dual evolutionary solution overcame the challenge of preserving fitness of a mutualistic symbiosis during adaptation to a toxic novel host. Our results reveal the intricate processes by which genetic novelty can arise and drive the evolution of key innovations required for ecological adaptation.

Competition and fixation of cohorts of adaptive mutations under Fisher geometrical model

One of the simplest models of adaptation to a new environment is Fisher’s Geometric Model (FGM), in which populations move on a multidimensional landscape defined by the traits under selection. The predictions of this model have been found to be consistent with current observations of patterns of fitness increase in experimentally evolved populations. Recent studies investigated the dynamics of allele frequency change along adaptation of microbes to simple laboratory conditions and unveiled a dramatic pattern of competition between cohorts of mutations, i.e., multiple mutations simultaneously segregating and ultimately reaching fixation. Here, using simulations, we study the dynamics of phenotypic and genetic change as asexual populations under clonal interference climb a Fisherian landscape, and ask about the conditions under which FGM can display the simultaneous increase and fixation of multiple mutations—mutation cohorts—along the adaptive walk. We find that FGM under clonal interference, and with varying levels of pleiotropy, can reproduce the experimentally observed competition between different cohorts of mutations, some of which have a high probability of fixation along the adaptive walk. Overall, our results show that the surprising dynamics of mutation cohorts recently observed during experimental adaptation of microbial populations can be expected under one of the oldest and simplest theoretical models of adaptation—FGM.