Hidden genetic variation in plasticity provides the potential for rapid adaptation to novel environments

Abstract

Rapid environmental change is forcing populations into environments where plasticity will no longer maintain fitness. When populations are exposed to novel environments, evolutionary theory predicts that genetic variation in fitness will increase and should be associated with genetic differences in plasticity. If true, then genetic variation in plasticity can increase adaptive potential in novel environments, and population persistence via evolutionary rescue is more likely.To test whether genetic variation in fitness increases in novel environments and is associated with plasticity, we transplanted 8149 clones of 314 genotypes of a Sicilian daisy (Senecio chrysanthemifolius) within and outside its native range, and quantified genetic variation in fitness, and plasticity in leaf traits and gene expression.Although mean fitness declined by 87% in the novel environment, genetic variance in fitness increased threefold and was correlated with plasticity in leaf traits. High fitness genotypes showed greater plasticity in gene expression, but lower plasticity in most leaf traits. Interestingly, genotypes with the highest fitness in the novel environment had the lowest fitness at the native site.These results suggest that standing genetic variation in plasticity could help populations to persist and adapt to novel environments, despite remaining hidden in native environments.

Identifying the proximate mechanisms that generate variation in nutritional plasticity for fecundity inDrosophila melanogaster

“…Having detected significant genotype-by-environment interactions for relative fecundity, we next determined the origin of this variation. GxE can be due to increased variation in relative fecundity on specific diets across genotypes (Walter et al, 2022; Sheth et al, 2018).…”

“…We then went on to reveal the cause of this within-population G×E. Significant G×E can arise as the result of differences in the expression of genetic variation across environments and/or cross-environment genetic correlations that are less than one (Falconer 1952; Via & Lande 1985; Walter et al, 2022; Sheth et al, 2018). While some studies have found that exposure to environmental stress may increase the expression of genetic variance for life-history traits, including fecundity (Service & Rose, 1985; Van Noordwijk et al, 1988; Etges, 1993; Holloway et al, 1990; Larsson et al, 1997; Jenkins et al, 1997; Sgrò & Hoffmann, 1998), other studies suggest that this might depend on the trait and the environmental condition studied.…”

“…To obtain coefficients of plasticity across the isogenic lines, we calculated the best linear unbiased prediction (BLUP), obtained from the MCMCglmm model, between the 5% and 100% yeast content diets for each genotype (Walter et al, 2022). These BLUPs estimate how genotypes rank relative to each other and the mean.…”

Combined empirical techniques reveal key role for variation in plasticity in a novel environment

“…The dramatic reduction in mean fitness beyond the range suggests that the novel conditions posed a challenge for most genotypes. However, a few genotypes with low fitness at the home site appeared ‘pre‐adapted’ to the new environment and enjoyed the highest fitness (nonsignificant correlation = −0.1; Walter et al ., 2023). Fitness trade‐offs between within‐ and beyond‐range environments could limit species' ranges if selection in native habitats quickly eliminated alleles that would be beneficial beyond the range, but this has rarely been tested in the field (Angert et al ., 2008).…”

“…A novel approach examining the impact of variation in plasticity on the adaptive capacity of a population is used by Walter et al . (2023; pp. 374–387) in a new article published in this issue of New Phytologist .…”