Evolutionary rescue and adaptation to abrupt environmental change depends upon the history of stress

Andrew Gonzalez 0 1 Graham Bell 0 1 0 Biology Department, McGill University , 1205 Avenue Docteur Penfield, Montreal, Quebec , Canada H3A 1B1 1 Subject Areas: evolution , ecology Whether evolution will be rapid enough to rescue declining populations will depend upon population size, the supply of genetic variation, the degree of maladaptation and the historical direction of selection. We examined whether the level of environmental stress experienced by a population prior to abrupt environmental change affects the probability of evolutionary rescue (ER). Hundreds of populations of two species of yeast, Saccharomyces cerevisiae and Saccharomyces paradoxus were exposed to a range of sublethal concentrations of salt for approximately a hundred generations before transfer to a concentration of salt lethal to the ancestor (150 g l - 1 NaCl). The fitness of surviving populations of both species was a quadratic function of yield: fitness was greatest for large populations that had been selected on low salt concentrations (less than 20 g l21 NaCl) and small populations that had adapted to high salt (more than 80 g l21 NaCl). However, differences occurred between species in the probability of ER. The frequency of ER was positively correlated with salt concentration for S. cerevisiae, but negatively correlated with salt concentration in S. paradoxus. These results not only demonstrate that past environmental conditions can determine the probability of ER after abrupt environmental change, but also suggest that there may even be differences between closely related species that are worth further exploration. Research 1. Introduction Biodiversity loss is projected to increase over the next 50 years as drivers of population extinction increase in rate and magnitude. Predicting the regions where populations are most at risk of extinction owing to environmental change requires a theory of extinction that combines both ecological and evolutionary processes [1 7]. Current theory suggests that evolution may have no effect, enhance, or even hamper long-term population persistence in the face of environmental change [4]. Here, we are concerned with evolutionary rescue (ER), the case where evolution can reverse population decline owing to environmental stress, and prevent otherwise inevitable extirpation. The experimental basis of this theory is currently in development [8 11]. Outstanding questions include the extent of variation among species in the rate and probability of ER, and the effects of past selective conditions on the evolutionary and demographic response to abrupt environmental change. In particular, can adaptation to past stress increase the probability of ER when abruptly exposed to acute levels of environmental stress? We addressed these questions here through experimental evolution in which the fate of many hundreds of populations were followed across a range of selective conditions prior to and following abrupt environmental change, using robot liquid-handling technology. The probability of ER after environmental change depends upon the initial population size [8], the rate of decline (the degree of maladaptation) and the supply of useful genetic variation. Differences between populations in these characteristics, and their tolerance to stress, are expected to depend upon the history of prior selective conditions. Population tolerance will have arisen as a combination of physiological acclimation and adaptation by natural selection [12,13]. We expect that the frequency of ER will be increased by prior selection in a stressful environment because beneficial mutations conferring tolerance to lethal conditions will spread because of their correlated advantage at sublethal levels of stress. If future environmental change is an extension of stressful conditions found within the current range then a genetic correlation between prevailing and future conditions may be expected to facilitate rapid adaptation and ER. Given population-to-population variation in the harshness of historical patterns of selection, what is the expectation for the response to selection, and the likelihood of ER when all populations are suddenly exposed to lethal stress? Our previous experiments [9] provide us with an expectation. The rate of adaptation depends upon the supply rate of beneficial mutations, the effect of beneficial mutation on population fitness and the correlation between the effect of a mutation in sublethal and lethal conditions. Bell & Gonzalez [9] hypothesized that the overall supply rate of mutations will be lower in smaller populations, and that the fraction of all mutations that are beneficial for population fitness is likely to be low in populations that have experienced little or no stress, but higher in populations that have experienced stressful conditions [14,15]. The supply of beneficial mutations will also be affected by the prior adaptive state of a strain. A strain which is initially more tolerant of a stress will maintain a larger population size in the presence of severe stress and will have a shorter adaptive walk in order to adapt to that stress, relative to a strain that is initially less tolerant. Given these two arguments, fitness will be a quadratic function of stress, with populations subjected to little or no stress adapting slowly, populations at intermediate levels of stress failing to adapt at all, whereas those subjected to severe stress will adapt more rapidly. Bell & Gonzalez [9] provide evidence for this quadratic response in metapopulations of Saccharomyces cerevisiae under gradual and rapidly increasing salt stress. We report here a test of three aspects of this theory: (i) that historical selection can establish a genetic correlation for fitness in past and future environmental conditions that will increase the probability of ER; (ii) that strains of species with lower tolerance to salt stress will have a lower probability of ER at lethal salt concentrations; (iii) the response to selection under harsh environmental conditions will be a quadratic function of the population yield. We used two species of yeast, S. cerevisiae and Saccharomyces paradoxus, grown at high concentrations of salt (NaCl) as a model system [16]. We use methods in experimental evolution, and a robotic liquid-handling system to attain high levels of population replication required to measure changes in population fitness (as measured by the change in population yield) and estimate extinction probability as a function of increasing salt concentration. Our previous work with this system has shown that the probability of ER following abrupt severe stress is directly related to population size [8,10] and dispersal pattern in metapopulations of yeast [8,10]. Here, we report the effect of historical environmental stress on population fitness and the probability of ER following abrupt environment change. 2. Methods was asexual during these experiments because there was only a (...truncated)