Microgeographic Patterns of Genetic Divergence and Adaptation across Environmental Gradients in Boechera stricta (Brassicaceae)

Abstract

Abiotic and biotic conditions often vary continuously across the landscape, imposing divergent selection on local populations. We used a provenance trial approach to examine microgeographic variation in local adaptation in Boechera stricta (Brassicaceae), a perennial forb native to the Rocky Mountains. In montane ecosystems, environmental conditions change considerably over short spatial scales, such that neighboring populations can be subject to different selective pressures. Using accessions from southern (Colorado) and northern (Idaho) populations, we characterized spatial variation in genetic similarity via microsatellite markers. We then transplanted genotypes from multiple local populations into common gardens in both regions. Continuous variation in local adaptation emerged for several components of fitness. In Idaho, genotypes from warmer environments (low-elevation or south-facing sites) were poorly adapted to the north-facing garden. In high- and low-elevation Colorado gardens, susceptibility to insect herbivory increased with source elevation. In the high-elevation Colorado garden, germination success peaked for genotypes that evolved at elevations similar to that of the garden and decreased for genotypes from higher and lower elevations. We also found evidence for local maladaptation in survival and fecundity components of fitness in the low-elevation Colorado garden. This approach is a first step in predicting how global change could affect evolutionary dynamics.

Fig. 1

Variation in foliar damage from herbivores in Colorado environments. In low (panels A + B) and high (panel C) elevation gardens, leaf damage was positively correlated with source elevation, indicating that high elevation populations are more susceptible to damage by insect herbivores across test sites. The elevation of the garden is indicated on the X-axis with closed star at 2891m for low elevation, and an open star at 3133m for high elevation (panels A-C). In addition (D), foliar damage varied with geographic distance for the 2012 cohort across both gardens; data points from the low elevation garden are closed triangles and data points from the high elevation garden are open circles. Shading around predicted regression lines indicates 95% Confidence Intervals.

Figure 2

In the high elevation Colorado garden, germination success followed the predicted quadratic fitness function, peaking for genotypes from similar elevations as the common garden (3133 m). Shading around predicted regression lines indicates 95% Confidence Intervals. The open star on the X-axis indicates the elevation of the garden.

Figure 3

Clinal variation in survival in the Colorado gardens as a function of: (A) source elevation for the 2011 cohort in the low elevation garden (2891m), (B) source elevation for the 2012 cohort in the low elevation garden (2891m), and (C) geographic distance for the 2012 cohort across gardens. Closed stars on the X-axis indicate the elevation of the garden. In panel C, data points from the low elevation garden are closed triangles and data points from the high elevation garden are open circles. Shading around predicted regression lines indicates 95% Confidence Intervals.

Figure 4

In the CO low elevation garden (2011 cohort), lifetime fitness varied with linear and quadratic effects of source elevation. The elevation of the garden (2891m) is indicated by a closed star on the X-axis. Fitness declined to a minimum for genotypes from mid-elevation populations and then increased to an unexpected peak in genotypes from high source elevation. The highest elevation family (3682m) is an influential outlier; when removed (small panel) fitness declines with source elevation, as expected. These results suggest local maladaptation, with a foreign high elevation family achieving or exceeding fitness levels of the lowest elevation families. Shading around predicted regression lines indicates 95% Confidence Intervals.

Figure 5

Clinal variation in fitness in the Idaho garden (elevation: 2535). Fitness declined with geographic distance for (A) survival in the 2012 cohort, and (B) first year fecundity in the 2011 cohort. Additionally, (C) first year fecundity of the 2011 cohort increased with source elevation. Shading around predicted lines represents 95% CI, and the star on the X-axis of panel C shows the elevation of the garden (2535m).