Rapid evolution of flowering time by an annual plant in response to a climate fluctuation

Abstract

Ongoing climate change has affected the ecological dynamics of many species and is expected to impose natural selection on ecologically important traits. Droughts and other anticipated changes in precipitation may be particularly potent selective factors, especially in arid regions. Here we demonstrate the evolutionary response of an annual plant, Brassica rapa, to a recent climate fluctuation resulting in a multiyear drought. Ancestral (predrought) genotypes were recovered from stored seed and raised under a set of common environments with descendant (postdrought) genotypes and with ancestorxdescendant hybrids. As predicted, the abbreviated growing seasons caused by drought led to the evolution of earlier onset of flowering. Descendants bloomed earlier than ancestors, advancing first flowering by 1.9 days in one study population and 8.6 days in another. The intermediate flowering time of ancestorxdescendant hybrids supports an additive genetic basis for divergence. Experiments confirmed that summer drought selected for early flowering, that flowering time was heritable, and that selection intensities in the field were more than sufficient to account for the observed evolutionary change. Natural selection for drought escape thus appears to have caused adaptive evolution in just a few generations. A systematic effort to collect and store propagules from suitable species would provide biologists with materials to detect and elucidate the genetic basis of further evolutionary shifts driven by climate change.

Fig. 1.

Early and late winter precipitation at the Irvine Ranch Water District (<3 km from the study sites) from the National Climate Data Center. We calculated cumulative precipitation during the growing season (100 days after the first 72-h period with rainfall ≥1 cm). Mean cumulative precipitation for days 1–50 and days 51–100 for each of the five growing seasons leading up to 1997 and 2004 were calculated, and values are plotted as deviation from this mean. Shaded bars indicate cumulative precipitation during the first 50 days after rainfall. Black bars show cumulative precipitation in the subsequent 50 days.

Fig. 2.

Box plots of the evolution of time to first flowering. Shown are box plots of FT for B. rapa plants from the Wet Site (Wet) and Dry Site (Dry) populations from the ancestral 1997 × 1997 (97), descendant 2004 × 2004 (04), and hybrid (H) crosses in the long season treatment. Days to first flowering is the number of days between germination (first emergence of cotyledons) and first flowering (first full opening of first flower). The center bar is the median, and the boxes, lines, and dots represent the 25th to 75th, 10th to 90th, and 5th to 95th percentiles, respectively. Descendants flowered earlier than ancestors in both populations and across all treatments.

Fig. 3.

Local adaptation across space and time. Shown is the percentage (mean ± SE) of B. rapa plants surviving from Wet Site (Wet) and Dry Site (Dry) populations from ancestral 1997 (97), descendant 2004 (04), and hybrid (H) crosses in the short (black bars), medium (dark gray bars), and long (light gray bars) season treatments. Higher survival of postdrought (2004) than predrought (1997) genotypes under short season conditions in the Wet Site shows adaptation to recent conditions. Higher survival of Dry Site than Wet Site genotypes under the short season treatment shows adaptation to local conditions. Survival was analyzed with a categorical model using a linear response function.