Rapid evolution of cold tolerance in stickleback

Abstract

Climate change is predicted to lead to increased average temperatures and greater intensity and frequency of high and low temperature extremes, but the evolutionary consequences for biological communities are not well understood. Studies of adaptive evolution of temperature tolerance have typically involved correlative analyses of natural populations or artificial selection experiments in the laboratory. Field experiments are required to provide estimates of the timing and strength of natural selection, enhance understanding of the genetics of adaptation and yield insights into the mechanisms driving evolutionary change. Here, we report the experimental evolution of cold tolerance in natural populations of threespine stickleback fish (Gasterosteus aculeatus). We show that freshwater sticklebacks are able to tolerate lower minimum temperatures than marine sticklebacks and that this difference is heritable. We transplanted marine sticklebacks to freshwater ponds and measured the rate of evolution after three generations in this environment. Cold tolerance evolved at a rate of 0.63 haldanes to a value 2.5°C lower than that of the ancestral population, matching values found in wild freshwater populations. Our results suggest that cold tolerance is under strong selection and that marine sticklebacks carry sufficient genetic variation to adapt to changes in temperature over remarkably short time scales.

Figure 1.

Temperature tolerance of wild stickleback. Circles and squares indicate individual fish from marine and freshwater populations, respectively. (a) Cold tolerance of wild stickleback acclimated to 17°C in the laboratory. (b) Heat tolerance of laboratory-acclimated wild stickleback. Lines show the (a) minimum and (b) maximum temperatures from 11 marine sites (solid line) and 14 freshwater lakes (dashed line) in British Columbia (see electronic supplementary material, table S2, for locations). Bars indicate population mean values. All fish were tested within 5 days of each other. Marine 1, Little Campbell; marine 2, Oyster Lagoon; fresh 1, Cranby Lake; fresh 2, Hoggan Lake.

Figure 2.

Cold tolerance of laboratory-raised stickleback. Symbols indicate family averages using three or four fish from pure marine (circles), pure freshwater (squares) or marine by freshwater (triangles) crosses. Bars indicate population mean values. All fish were tested within 5 days of each other. Marine 1, Little Campbell; marine 2, Oyster Lagoon; hybrid 1, Oyster Lagoon female crossed to Cranby Lake male; hybrid 2, Cranby Lake female crossed to Oyster Lagoon male; fresh 1, Cranby Lake; fresh 2, Hoggan Lake.

Figure 3.

Rapid evolution of cold tolerance in a marine population of stickleback transplanted to freshwater. Circles indicate individuals from the ancestral population (Oyster Lagoon) for the selection experiment and the F₃ generation in the ponds. Lines show the minimum temperature from Oyster Lagoon, British Columbia (solid line), and averaged from three ponds located at the University of British Columbia, Vancouver, British Columbia (dashed line). All fish were sampled in September 2008, acclimated for six weeks in the laboratory at 17°C and tested within 5 days of each other. Bars indicate population mean values.