Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Abstract

Anthropogenic climate change has already altered the timing of major life-history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change, but their relative contributions are poorly understood. Here, we combine a continuous 38 year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the US Rocky Mountains. Flowering phenology advanced significantly from 1973 to 2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favoured earlier flowering in contemporary environments (2010-2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20 per cent of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.

Figure 1.

Conceptual model of natural selection on flowering phenology in the context of anthropogenic climate change. (a) Prior to industrialization: stabilizing selection could have favoured intermediate flowering time owing to seasonal constraints on growth and reproduction. (b) Contemporary conditions: climate change causes growing seasons to begin earlier, shifting the fitness landscape and resulting in directional selection for earlier flowering. (c) Future conditions: under continued warming, natural populations with limited genetic variation could fall far from the fitness optimum, have severely depressed fitness, and risk extinction. Further details are available in electronic supplementary material, S1.

Figure 2.

Long-term trends in flowering phenology in Boechera stricta. (a) The timing of first flowering has advanced significantly since 1973, and (b) is tightly related to the timing of snowmelt and (c) late winter temperatures. Grey bands represent 95% CI.

Figure 3.

Environmental change through time. (a) The timing of snowmelt has advanced significantly from 1935 to 2012 (open circles are estimated values from river runoff, 1935–1974; closed circles are observed data from 1975 to 2012). (b) Average April and May temperature increased only marginally from 1973 to 2011. (c) Minimum April and May average temperatures increased significantly from 1973 to 2011.

Figure 4.

(a) Selection on flowering time: in recombinant inbred lines; (b) experimental population at Carpenter Meadow; and endogenous population at Carpenter Meadow in (c) 2010 and (d) 2011. All datasets show significant directional selection for earlier flowering (see text). Analyses were conducted using phenotypic data standardized to a mean of 0 and a s.d. of 1, but figure panels present unstandardized flowering time data.