Environment changes epistasis to alter trade‐offs along alternative evolutionary paths

Abstract

The fitness effect of a mutation can depend on both its genetic background, known as epistasis, and the prevailing external environment. Many examples of these dependencies are known, but few studies consider both aspects in combination, especially as they affect mutations that have been selected together. We examine interactions between five coevolved mutations in eight diverse environments. We find that mutations are, on average, beneficial across environments, but that there is high variation in their fitness effects, including many examples of mutations conferring a cost in some, but not other, genetic background‐environment combinations. Indeed, even when global interaction trends are accounted for, specific local mutation interactions are common and differed across environments. One consequence of this dependence is that the range of trade‐offs in genotype fitness across selected and alternative environments are contingent on the particular evolutionary path followed over the mutation landscape. Finally, although specific interactions were common, there was a consistent pattern of diminishing returns epistasis whereby mutation effects were less beneficial when added to genotypes of higher fitness. Our results underline that specific mutation effects are highly dependent on the combination of genetic and external environments, and support a general relationship between a genotype's current fitness and its potential to increase in fitness.

Mutational robustness changes during long-term adaptation in laboratory budding yeast populations

“…These patterns of idiosyncratic epistasis are not due to outsized contributions from a few populations; the distributions of IM coefficients for YPD 30°C populations are different in the two assay environments across populations (Figure 3 – figure supplement 2). Overall, these results support the hypothesis that GxGxE effects underlie the differences we observe between environments (see also Hall et al 2019), though they do not rule out the possibility that differences in adaptive targets between environments may also contribute.…”

“…The picture that emerges from our data is one in which idiosyncratic epistatic effects are largely unpredictable but have biases that often lead to correlations with background fitness. In both our own work and other studies of microbial evolution, these biases are more often towards negative epistasis: beneficial mutations tend to have negative epistatic interactions with both deleterious (Johnson et al, 2019, this study) and beneficial mutations (Chou et al, 2011; Hall et al, 2019; Karkare et al, 2021; Khan et al, 2011; Kryazhimskiy et al, 2014; Ono et al, 2017; Pearson et al, 2012; Perfeito et al, 2014; Rokyta et al, 2011; Wünsche et al, 2017).…”

Role of bacterial motility in differential resistance mechanisms of silver nanoparticles and silver ions

“…For example, Haefeli et al and Li et al found that when there was no sodium chloride present in the system, the MIC of Ag decreased significantly for E. coli and Pseudomonas stutzeri 14,15 . Additionally, the mixed observations of resistance to Ag(I) ions within the literature could be due to fitness epistasis, that is, genetic variation within populations, coupled with differences in the external environment, both of which can dictate specific evolutionary paths and mutation effects in evolution experiments 32,33 . In our study, the decreased susceptibility of the hypermotile E. coli (+IS1) to AgNPs compared with Ag(I) ions (controlling for total Ag and Ag(I) content, see Supplementary Discussion 2) suggests a nanoparticle-specific bacterial response similar to the findings of Panacek et al 10 .…”

The mutation effect reaction norm (mu‐rn) highlights environmentally dependent mutation effects and epistatic interactions

“…2013; Li and Zhang 2018; Hall et al. 2019; Lozovsky et al. 2020), there have been few formal attempts to integrate details of the environment into measurements of mutation effects and interactions.…”