Genome size variation and evolution during invasive range expansion in an introduced plant

Abstract

Plants demonstrate exceptional variation in genome size across species, and their genome sizes can also vary dramatically across individuals and populations within species. This aspect of genetic variation can have consequences for traits and fitness, but few studies attributed genome size differentiation to ecological and evolutionary processes. Biological invasions present particularly useful natural laboratories to infer selective agents that might drive genome size shifts across environments and population histories. Here, we test hypotheses for the evolutionary causes of genome size variation across 14 invading populations of yellow starthistle, Centaurea solstitialis, in California, United States. We use a survey of genome sizes and trait variation to ask: (1) Is variation in genome size associated with developmental trait variation? (2) Are genome sizes smaller toward the leading edge of the expansion, consistent with selection for "colonizer" traits? Or alternatively, does genome size increase toward the leading edge of the expansion, consistent with predicted consequences of founder effects and drift? (3) Finally, are genome sizes smaller at higher elevations, consistent with selection for shorter development times? We found that 2C DNA content varied 1.21-fold among all samples, and was associated with flowering time variation, such that plants with larger genomes reproduced later, with lower lifetime capitula production. Genome sizes increased toward the leading edge of the invasion, but tended to decrease at higher elevations, consistent with genetic drift during range expansion but potentially strong selection for smaller genomes and faster development time at higher elevations. These results demonstrate how genome size variation can contribute to traits directly tied to reproductive success, and how selection and drift can shape that variation. We highlight the influence of genome size on dynamics underlying a rapid range expansion in a highly problematic invasive plant.

Keywords: flow cytometry; intraspecific genome size variation; invasive species; yellow starthistle.

FIGURE 1

Map of 14 YST populations sampled in 2016 from the invasion in California, United States. Shaded areas indicate the invaded range in western North America.

FIGURE 2

Histogram of 2C genome sizes sampled from the Californian invasion (N = 335), with a mean size of 1.72 pg (blue dashed line). For individuals with repeat measurements (N = 24), only the means of estimated genome sizes are included.

FIGURE 3

Partial residuals from best‐fitting linear models explaining patterns of genome size variation using the full genome size data set of California individuals (N = 335) by (a) population age and (c) elevation. (b) Partial residuals by population age using a reduced dataset of only individuals with repeat flow cytometry measurements (N = 24). Solid lines indicate significant associations (p < 0.1).

FIGURE 4

Principal component analysis of traits where each point indicates an individual plant in the common garden (N = 391) with PC1 and PC2 explaining 67.3% of all variation. PC1 is associated with variation in growth traits and PC2 is associated with variation in development an.

FIGURE 5

(a) Partial residual plot from best‐fitting model explaining variation in PC1 scores due to fixed effect of genome size (NS, p = 0.39). (b) Partial residual plot explaining variation in PC2 scores by genome size (p = 0.001).

FIGURE 6

Genome size varies in direction and magnitude of effect on PC1 scores when plotted by greenhouse block. Different colour lines from red to blue indicate greenhouse position with increasing proximity to the cooling pads, where solid lines indicate a significant effect of genome size on PC1 (p < 0.05) Significant and marginally significant positive correlations were found in positions 7 and 8, and position 9, respectively, where local environments were coolest.