Fitness effects of mutation in natural populations of
            <i>Arabidopsis thaliana</i>
            reveal a complex influence of local adaptation

Weng, Mao‐Lun; Ågren, Jon; Imbert, Éric; Nottebrock, Henning; Rutter, Matthew T.; Fenster, Charles B.

doi:10.1111/evo.14152

Cited by 21 publications

(31 citation statements)

References 87 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…To validate our predictive model of the mutation probability score, we used a second A. thaliana mutation accumulation experiment descended from eight founders collected in natural environments 50 . The lines were grown for seven to ten generations of single-seed descent before 150-bp paired-end read Illumina sequencing of pools of 40 seedlings.…”

Section: Methodsmentioning

confidence: 99%

Mutation bias reflects natural selection in Arabidopsis thaliana

Monroe

Srikant

Carbonell‐Bejerano

et al. 2022

Nature

Self Cite

290

403

View full text Add to dashboard Cite

Since the first half of the twentieth century, evolutionary theory has been dominated by the idea that mutations occur randomly with respect to their consequences1. Here we test this assumption with large surveys of de novo mutations in the plant Arabidopsis thaliana. In contrast to expectations, we find that mutations occur less often in functionally constrained regions of the genome—mutation frequency is reduced by half inside gene bodies and by two-thirds in essential genes. With independent genomic mutation datasets, including from the largest Arabidopsis mutation accumulation experiment conducted to date, we demonstrate that epigenomic and physical features explain over 90% of variance in the genome-wide pattern of mutation bias surrounding genes. Observed mutation frequencies around genes in turn accurately predict patterns of genetic polymorphisms in natural Arabidopsis accessions (r = 0.96). That mutation bias is the primary force behind patterns of sequence evolution around genes in natural accessions is supported by analyses of allele frequencies. Finally, we find that genes subject to stronger purifying selection have a lower mutation rate. We conclude that epigenome-associated mutation bias2 reduces the occurrence of deleterious mutations in Arabidopsis, challenging the prevailing paradigm that mutation is a directionless force in evolution.

show abstract

Section: Methodsmentioning

confidence: 99%

Mutation bias reflects natural selection in Arabidopsis thaliana

Monroe

Srikant

Carbonell‐Bejerano

et al. 2022

Nature

Self Cite

290

403

View full text Add to dashboard Cite

show abstract

“…The high f b values we observe (Fig 1) contradict the general expectation that beneficial mutations should be rare (32). However, many other studies – including with microbes and plants – have also reported a large number of beneficial mutations (33–39). The large f b has been partially attributed to an improved ability to measure small-effect beneficial mutations (36, 40, 41) that are more common than expected (42), especially at low effective population sizes (38).…”

Section: Resultsmentioning

confidence: 99%

Shifts in mutation spectra enhance access to beneficial mutations

Sane

Diwan

Bhat

et al. 2020

Preprint

View full text Add to dashboard Cite

SUMMARYMutations are critical for evolutionary change. Although mutation spectra (mutational biases) vary greatly across organisms, we lack direct evidence of their evolutionary consequences. Here, we show experimentally that a biased spectrum alters the distribution of fitness effects in a bacterium, and should facilitate adaptation by increasing beneficial mutations and reducing genetic load. Adaptive walk simulations show that this advantage arises via better sampling of mutational classes that were poorly explored by the ancestor. Hence, reversing the spectrum of a biased ancestor is generally advantageous, while introducing bias in an unbiased ancestor is selectively neutral. Indeed, across bacterial lineages, evolutionary transitions in DNA repair enzymes – which shape spectra – typically reverse ancestral bias. These broad consequences of mutation spectra imply a major role in shaping evolutionary dynamics.

show abstract

“…Moreover, Fisher's Geometric Model (FGM) (Fisher 1930) predicts a higher absolute number (although not a higher frequency) of beneficial mutations when populations are far away from their adaptive peaks, such as in stressful or novel environments (Svensson and Berger 2019). Fisher's model is largely congruent with laboratory experiments and field studies on mutation accumulation (MA) lines, which have showed that mutation rates, fitness effects of novel mutations and mutational variances are highly context-and environment-dependent, and that fitness-effects of mutations are often larger in more stressful environments (Galhardo et al 2007;Rutter et al 2010;MacLean et al 2013;Weng et al 2021) An emerging view is therefore that evolution is not solely driven by the deterministic fitness-enhancing force of natural selection (Svensson and Berger 2019). Evolutionary biology today therefore recognizes historical contingencies such as the arrival order of mutations and mutational history (Losos et al 1998;Huey et al 2000;Svensson and Berger 2019), as exemplified in models of "mutation-order speciation" (Schluter 2009;Mendelson et al 2014).…”

Section: Introductionmentioning

confidence: 74%

Multivariate selection and the making and breaking of mutational pleiotropy

Svensson

2022

Evol Ecol

View full text Add to dashboard Cite

The role of mutations have been subject to many controversies since the formation of the Modern Synthesis of evolution in the early 1940ties. Geneticists in the early half of the twentieth century tended to view mutations as a limiting factor in evolutionary change. In contrast, natural selection was largely viewed as a “sieve” whose main role was to sort out the unfit but which could not create anything novel alone. This view gradually changed with the development of mathematical population genetics theory, increased appreciation of standing genetic variation and the discovery of more complex forms of selection, including balancing selection. Short-term evolutionary responses to selection are mainly influenced by standing genetic variation, and are predictable to some degree using information about the genetic variance–covariance matrix (G) and the strength and form of selection (e. g. the vector of selection gradients, β). However, predicting long-term evolution is more challenging, and requires information about the nature and supply of novel mutations, summarized by the mutational variance–covariance matrix (M). Recently, there has been increased attention to the role of mutations in general and M in particular. Some evolutionary biologists argue that evolution is largely mutation-driven and claim that mutation bias frequently results in mutation-biased adaptation. Strong similarities between G and M have also raised questions about the non-randomness of mutations. Moreover, novel mutations are typically not isotropic in their phenotypic effects and mutational pleiotropy is common. Here I discuss the evolutionary origin and consequences of mutational pleiotropy and how multivariate selection directly shapes G and indirectly M through changed epistatic relationships. I illustrate these ideas by reviewing recent literature and models about correlational selection, evolution of G and M, sexual selection and the fitness consequences of sexual antagonism.

show abstract

Fitness effects of mutation in natural populations of Arabidopsis thaliana reveal a complex influence of local adaptation

Cited by 21 publications

References 87 publications

Mutation bias reflects natural selection in Arabidopsis thaliana

Mutation bias reflects natural selection in Arabidopsis thaliana

Shifts in mutation spectra enhance access to beneficial mutations

Multivariate selection and the making and breaking of mutational pleiotropy

Contact Info

Product

Resources

About