Evolution of plant resistance and tolerance to frost damage

Anurag A. Agrawal,* Jeffrey K. Conner and John R. Stinchcombe Department of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON, Canada M5S 3B2 Kellogg Biological Station and Department of Plant Biology, Michigan State University, 3700 East Gull Lake Drive, Hickory Corners, MI 49060, USA Department of Ecology and Evolutionary Biology, Box G-W, Brown University, Providence, RI 02912, USA *Correspondence and present address: Anurag A. Agrawal, Department of Ecology and Evolutionary Biology, Corson Hall, Cornell University, Ithaca, NY 14853, USA. E-mail: [email protected] Abstract Plant defence against any type of stress may involve resistance (traits that reduce damage) or tolerance (traits that reduce the negative fitness impacts of damage). These two strategies have been proposed as redundant evolutionary alternatives. A late-season frost enabled us to estimate natural selection and genetic constraints on the evolution of frost resistance and tolerance in a wild plant species. We employed a genetic selection analysis (which is unbiased by environmental correlations between traits and fitness) on 75 paternal half-sibling families of annual wild radish [Raphanus raphanistrum (Brassicaceae)]. In an experimental population in southern Ontario, we found strong selection favouring plant resistance to frost, but selection against tolerance to frost. The selection against tolerance may have been caused by a cost of tolerance, as we provide evidence for a negative genetic correlation between tolerance and fitness in the absence of frost damage. Although we found no evidence for the theoretically predicted trade-off between frost tolerance and resistance among our families, we did detect negative correlational selection acting on the two traits, indicating that natural selection favoured high resistance combined with low tolerance and low resistance coupled with high tolerance, but not high or low levels of both traits together. There were few genetic correlations between the measured traits overall, but frost tolerance was negatively correlated with initial seed mass, and frost resistance was positively correlated with resistance to insect herbivory. Periodic episodes of strong selection such as that caused by the late-season frost may be disproportionately important in evolution, and are likely becoming more common because of human alterations of the environment.