Adaptive plasticity increases population persistence, but can slow adaptation to changing environments by hiding the effects of different alleles on fitness. However, if plastic responses are no longer adaptive in novel environments, then differences among alleles can emerge and increase genetic variation in fitness that allows rapid adaptation. We tested this hypothesis by transplanting cuttings and seeds of a Sicilian daisy within and outside its native range, and quantifying variation in morphology, physiology, gene expression and fitness. We show that genetic variance in plasticity increases the potential for rapid adaptation to novel environments. Genetic variation in fitness was low across native environments where plasticity effectively tracked familiar environments. In the novel environment however, genetic variation in fitness increased threefold, and correlated with genetic variation in plasticity. Furthermore, genetic variation that can increase fitness in the novel environment had the lowest fitness at the native site, suggesting that adaptation to novel environments relies on genetic variation in plasticity that is selected against in native environments.
The evolution of plastic responses to external cues allows species to maintain fitness in response to the environmental variations they regularly experience. However, it remains unclear how plasticity evolves during adaptation. To test whether distinct patterns of plasticity are associated with adaptive divergence, we quantified plasticity for two closely related but ecologically divergent Sicilian daisy species (Senecio, Asteraceae). We sampled 40 representative genotypes of each species from their native range on Mt. Etna and then reciprocally transplanted multiple clones of each genotype into four field sites along an elevational gradient that included the native elevational range of each species, and two intermediate elevations. At each elevation, we quantified survival and measured leaf traits that included investment (specific leaf area), morphology, chlorophyll fluorescence, pigment content, and gene expression. Traits and differentially expressed genes that changed with elevation in one species often showed little changes in the other species, or changed in the opposite direction. As evidence of adaptive divergence, both species performed better at their native site and better than the species from the other habitat. Adaptive divergence is, therefore, associated with the evolution of distinct plastic responses to environmental variation, despite these two species sharing a recent common ancestor.
Genetic correlations between traits are expected to constrain the rate of adaptation by concentrating genetic variation in certain phenotypic directions, which are unlikely to align with the direction of selection in novel environments. However, if genotypes vary in their response to novel environments, then plasticity could create changes in genetic variation that will determine whether genetic constraints to adaptation arise. We tested this hypothesis by mating two species of closely related, but ecologically distinct, Sicilian daisies (Senecio, Asteraceae) using a quantitative genetics breeding design. We planted seeds of both species across an elevational gradient that included the native habitat of each species and two intermediate elevations, and measured eight leaf morphology and physiology traits on established seedlings. We detected large significant changes in genetic variance across elevation and between species. Elevational changes in genetic variance within species were greater than differences between the two species. Furthermore, changes in genetic variation across elevation aligned with phenotypic plasticity. These results suggest that to understand adaptation to novel environments we need to consider how genetic variance changes in response to environmental variation, and the effect of such changes on genetic constraints to adaptation and the evolution of plasticity.
Maternal effects can maintain fitness across environmental conditions regularly experienced by a population. However, the consequences of maternal effects for ecological resilience in novel environments remain poorly understood. We produced seeds by breeding field-collected individuals of two closely related, but ecologically distinct, species of Sicilian daisy (Senecio, Asteraceae) in a quantitative genetics design. Using siblings of the same families, we quantified seedling root morphology in the laboratory, and planted seeds at four elevations that included the native elevation of each species. Seedling survival of both species was high at their native elevations, but declined at the novel elevation furthest from their native range, demonstrating adaptive divergence. Seedling development rate changed with elevation similarly for both species, and aligned with selection for faster development at lower elevation and slower development at higher elevation. Selection on paternal (sire) variance in development rate was consistent across elevation, and opposed phenotypic selection in the novel elevations. By contrast, selection on maternal variance in development rate changed with elevation and aligned with the direction of selection at both the native and novel elevations, suggesting that maternal effects underlying plasticity in development rate can increase fitness in novel environments. Selection on root morphology was only strong for the high elevation species, and occurred in the direction of the native phenotype for maternal variance, but not for sire variance. Together, these results suggest that maternal variation in development time plasticity and root architecture can increase ecological resilience in novel habitats, despite theory suggesting that they may reduce fitness in such situations.
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.
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