Fisher's geometric model predicts the effects of random mutations when tested in the wild

Abstract

Fisher's geometric model of adaptation (FGM) has been the conceptual foundation for studies investigating the genetic basis of adaptation since the onset of the neo Darwinian synthesis. FGM describes adaptation as the movement of a genotype toward a fitness optimum due to beneficial mutations. To date, one prediction of FGM, the probability of improvement is related to the distance from the optimum, has only been tested in microorganisms under laboratory conditions. There is reason to believe that results might differ under natural conditions where more mutations likely affect fitness, and where environmental variance may obscure the expected pattern. We chemically induced mutations into a set of 19 Arabidopsis thaliana accessions from across the native range of A. thaliana and planted them alongside the premutated founder lines in two habitats in the mid-Atlantic region of the United States under field conditions. We show that FGM is able to predict the outcome of a set of random induced mutations on fitness in a set of A. thaliana accessions grown in the wild: mutations are more likely to be beneficial in relatively less fit genotypes. This finding suggests that FGM is an accurate approximation of the process of adaptation under more realistic ecological conditions.

The effect of induced mutations on quantitative traits in Arabidopsis thaliana: Natural versus artificial conditions

“…In the more benign conditions of the growth room, the difference between founder and mutant lines was much less pronounced. Previous work on an earlier generation of these mutant lines derived from EMS mutagenesis found a similar result: In two of three field plantings, mutations reduced fitness on average relative to the founder (Stearns & Fenster, 2016). …”

“…This has been corroborated experimentally (Davies, Peters, & Keightley, 1999) and most recently by Heilbron, Toll‐Reira, Kojadinovic, and MacLean (2014) who found that 42.3% of the decrease in fitness in Pseudomonas aeruginosa mutation accumulation lines was explained by only 4.5% of the mutational steps that had a highly deleterious effect on fitness, only 0.5% of all mutations fixed. Previous work with an earlier generation of these mutant lines (and the mutant lines of several other A. thaliana ecotypes) suggested that beneficial mutations occurred, but that the magnitude of deleterious mutations was greater (Stearns & Fenster, 2016). This study, when considered in the context of the previous A. thaliana mutation accumulation studies, suggests that high magnitude deleterious mutations are more common than high magnitude beneficial mutations and that adaptation likely occurs due to small or intermediate effect beneficial mutations, as suggested by Fisher (1930) and Kimura (1983) and supported experimentally (Barrett, MacLean, & Bell, 2006; Heilbron et al., 2014; Sousa, Magalhaes, & Gordo, 2012).…”

Quantifying natural seasonal variation in mutation parameters with mutation accumulation lines

“…In this case, the assayed population may be far from its optimum in the new environment, increasing the likelihood a mutation will be beneficial, as has been observed with experimental studies of microorganisms (Burch & Chao, 1999; Khan, Dinh, Schneider, Lenski, & Cooper, 2011; Kryazhimskiy, Rice, Jerison, & Desai, 2014; MacLean, Perron, & Gardner, 2010; Perfeito, Sousa, Bataillon, & Gordo, 2014) and in one field study with A. thaliana (Stearns & Fenster, 2016). It is also possible that there was within‐plant selection during the propagation of the mutation accumulation lines (Otto & Orive, 1995).…”

“…If we scale up our estimates of V g to 25 generations of MA, then mutations have contributed on the order of 2 × 10 −3 V g scaled to V e for fitness. In contrast, studies of accessions grown in fieldlike settings, or RILs generated from an extreme cross of Italian and Swedish A. thaliana populations, similarly measured for fitness or fitness proxies found V g scaled to V e is much higher, on the order of 0.05-0.1 (Ågren, Oakley, McKay, Lovell, & Schemske, 2013;Rutter & Fenster, 2007;Samis et al, 2012;Stearns & Fenster, 2016), as one might expect. However, to put this into the context of mutational contributions to fitness variance, after only 25 generations of MA, the 100 lines have diverged such that this population of 100 MA lines has on the order of 25-fold less fitness variation than found in a survey of 21 worldwide A. thaliana accessions grown at a single site (Rutter & Fenster, 2007).…”

“…Given that our founder genotype originates from Northern Germany and has experienced a series of inbreeding events throughout its laboratory cultivation, and our experiments were conducted in the novel environment of the Virginia Blue Ridge, our observation of a lack of an overall deleterious effect of mutation may be consistent with Fisher's (1930) geometric model. In this case, the assayed population may be far from its optimum in the new environment, increasing the likelihood a mutation will be beneficial, as has been observed with experimental studies of microorganisms (Burch & Chao, 1999;Khan, Dinh, Schneider, Lenski, & Cooper, 2011;Kryazhimskiy, Rice, Jerison, & Desai, 2014;MacLean, Perron, & Gardner, 2010;Perfeito, Sousa, Bataillon, & Gordo, 2014) and in one field study with A. thaliana (Stearns & Fenster, 2016). It is also possible that there was within-plant selection during the propagation of the mutation accumulation lines (Otto & Orive, 1995).…”