Slower environmental change hinders adaptation from standing genetic variation

Evolutionary responses to environmental change depend on the time available for adaptation before environmental degradation leads to extinction. Explicit tests of this relationship are limited to microbes where adaptation usually depends on the sequential fixation of de novo mutations, excluding standing variation for genotype-by-environment fitness interactions that should be key for most natural species. For natural species evolving from standing genetic variation, adaptation at slower rates of environmental change may be impeded since the best genotypes at the most extreme environments can be lost during evolution due to genetic drift or founder effects. To address this hypothesis, we perform experimental evolution with self-fertilizing populations of the nematode Caenorhabditis elegans and develop an inference model to describe natural selection on extant genotypes under environmental change. Under a sudden environmental change, we find that selection rapidly increases the frequency of genotypes with high fitness in the most extreme environment. In contrast, under a gradual environmental change selection first favors genotypes that are worse at the most extreme environment. We demonstrate with a second set of evolution experiments that, as a consequence of slower environmental change and thus longer periods to reach the most extreme environments, genetic drift and founder effects can lead to the loss of the most beneficial genotypes. We further find that maintenance of standing genetic variation can retard the fixation of the best genotypes in the most extreme environment because of interference between them. Taken together, these results show that slower environmental change can hamper adaptation from standing genetic variation and they support theoretical models indicating that standing variation for genotype-by-environment fitness interactions critically alters the pace and outcome of adaptation under environmental change.


Introduction
With human activities predicted to increase rates of climate change (Stocker et al. unable to migrate to their favored habitats. In all these cases, survival and adaptation to 49 changing environments will depend on pre-existing genetic diversity, and less so on 50 mutation accumulation (Hill 1982, Matuszewski et al. 2015. 51 Adaptation to changing environments from pre-existing genetic diversity is 52 conditional on how each genotype performs within the environments that may be 53 encountered in the near future (Fig. 1A). Depending on the shape of these "fitness reaction  more extreme environments. Short-term adaptation will therefore be determined by the 58 amount of heritable genotype-by-environment fitness variance. Two predictions arise from 59 this hypothesis. The first is that slower environmental change can restrict adaptation 60 because all populations are finite and the best genotypes may be lost by genetic drift (Crow 61 and Kimura 1970). The second prediction is that slower environmental change can limit 62 adaptation by favoring the maintenance of similarly fit genotypes for longer periods, 63 leading to a reduction in the mean population fitness and weaker selection for the genotypes 64 with the highest fitness in the most extreme environments (Fisher 1930). Whether or not an 65 adapting population has standing genetic diversity will profoundly affect the tempo and 66 mode of evolution in changing environments (Matuszewski et al. 2015). 67 Here we show that heritable genotype-by-environment fitness variance is crucial for

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Experimental evolution in changing environments 82 We performed replicated experimental evolution for 50 generations in the nematode 83 C. elegans under different rates of change in the NaCl (salt) concentration that individuals 84 experience from early larvae to adulthood ( Fig. 1B and Table S1). In one regime,      corresponding to the L28 and L11 lineages that we inferred ( Fig S7 and Table S2). Our showed rapid sweeping of L28, indicating that L28 was initially at a high frequency. When 195 comparing responses in this first category, we conclude that there was a founder effect, in 196 that L28 was present at different initial frequencies, and that selection was more efficient 197 when L28 was initially at high frequency and when evolution in high salt occurred at large 198 population sizes.

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In the second category, corresponding to three ancestrals, the L28 lineage was most that adaptation would be deterred under slower environmental changes. We found with the 259 continued evolution experiments in high salt that slower environmental change will indeed 260 maintain polymorphism (Fig. 2) and compromise adaptation (Fig. 4). This is because small  The ancestral population (before salt adaptation) was thawed from frozen stocks and 326 individuals reared for two generations at 25 mM before they were exposed to the three 327 assay NaCl treatments (Fig. 3B). On the third generation, five Petri dishes per NaCl 328 treatment were seeded with 10 3 L1s per plate. These five plates constituted one technical 329 replicate, and there were four of these for each salt treatment. After 66 h, individuals were 330 harvested and exposed to a 1 M KOH:5% NaOCl solution (to which only embryos survive).

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L28 and L11 were also assayed in head-to-head competitions (Fig. 3C). They were 349 thawed from frozen stocks and reared for two generations at 25 mM NaCl before they were control, we retained 29 SNPs, 18 of which differentiating L28 and L11 (Fig. 3D). We  (Fig. 4), the function prcomp in R was used. the NaCl concentration. We assume an infinite population size, such that any given lineage 397 never goes extinct (although the frequency may become very small), that there are no 398 density-or frequency-dependencies, and that trans-generational effects are absent.

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A population is composed of lineages, such that the frequency of the -th lineage 400 in generation + 1, denoted by , is given by: , [.] , ⋯ , D