Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments.

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.

Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity.

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal-scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full-sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full-sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes.

Understanding the consequences of seed dispersal in a heterogeneous environment.

Plant distributions are in part determined by environmental heterogeneity on both large (landscape) and small (several meters) spatial scales. Plant populations can respond to environmental heterogeneity via genetic differentiation between large distinct patches, and via phenotypic plasticity in response to heterogeneity occurring at small scales relative to dispersal distance. As a result, the level of environmental heterogeneity experienced across generations, as determined by seed dispersal distance, may itself be under selection. Selection could act to increase or decrease seed dispersal distance, depending on patterns of heterogeneity in environmental quality with distance from a maternal home site. Serpentine soils, which impose harsh and variable abiotic stress on non-adapted plants, have been partially invaded by Erodium cicutarium in northern California, USA. Using nearby grassland sites characterized as either serpentine or non-serpentine, we collected seeds from dense patches of E. cicutarium on both soil types in spring 2004 and subsequently dispersed those seeds to one of four distances from their maternal home site (0, 0.5, 1, or 10 m). We examined distance-dependent patterns of variation in offspring lifetime fitness, conspecific density, soil availability, soil water content, and aboveground grass and forb biomass. ANOVA revealed a distinct fitness peak when seeds were dispersed 0.5 m from their maternal home site on serpentine patches. In non-serpentine patches, fitness was reduced only for seeds placed back into the maternal home site. Conspecific density was uniformly high within 1 m of a maternal home site on both soils, whereas soil water content and grass biomass were significantly heterogeneous among dispersal distances only on serpentine soils. Structural equation modeling and multigroup analysis revealed significantly stronger direct and indirect effects linking abiotic and biotic variation to offspring performance on serpentine soils than on non-serpentine soils, indicating the potential for soil-specific selection on seed dispersal distance in this invasive species.