SYNTHESIS Adaptation, extinction and global change Graham Bell1,2 and Sinead �� Collins3 1 Biology Department, McGill University, Montreal, �� QC, Canada 2 NERC Centre for Population Biology, Imperial College London, Silwood Park Campus, Ascot, Berks, UK 3 Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, UK Global change presents a clear, immediate and urgent challenge for evolutionary biology. The transformation of environments by agriculture and industry has created, and continues to create, a wide range of unintentional experiments in which populations are exposed to severe and novel perturbations, and either adapt to them or cease to exist. The greatest of these experiments is now under way: the alteration of the atmosphere and climate of the Earth, with consequences for every living thing. In this opening article of a new journal, we shall not attempt to offer a review of the whole field, which would be too intricate and extensive to fit within the confines of a short paper. We shall instead try to sketch the main tasks that we think that evolutionary biologists should undertake to contribute to our understanding of the future. Our account is organized into three sections. The first deals with the variability that is commonly experienced by nat- ural populations, and how they respond to it. The second is concerned with whether or not populations can adapt to a novel and severe stress before being extinguished by it. The final section describes how phytoplankton popula- tions may adapt to the prime mover of change, the increase in atmospheric concentration of carbon dioxide. The emphasis throughout is quantitative and experimen- tal. We hope, and we believe, that evolutionary biology is the key to predicting how the world will change, and we see this as the principal task of evolutionary biologists in the next few decades. Keywords carbon cycle, CO2, environmental variability, evolutionary rescue, rapid evolution, stressful environment. Correspondence Graham Bell, Biology Department, McGill University, 1205 ave Docteur Penfield, Montreal, �� QC H3A 1B1, Canada. Tel.: 15143986458 fax: 15143985069 e-mail: graham.bell@mcgill.ca Received: 28 October 2007 Accepted: 5 December 2007 Abstract We discuss three interlinked issues: the natural pace of environmental change and adaptation, the likelihood that a population will adapt to a potentially lethal change, and adaptation to elevated CO2, the prime mover of global change. 1. Environmental variability is governed by power laws showing that ln differ- ence in conditions increases with ln elapsed time at a rate of 0.3���0.4. This leads to strong but fluctuating selection in many natural populations. 2. The effect of repeated adverse change on mean fitness depends on its fre- quency rather than its severity. If the depression of mean fitness leads to population decline, however, severe stress may cause extinction. Evolu- tionary rescue from extinction requires abundant genetic variation or a high mutation supply rate, and thus a large population size. Although natural populations can sustain quite intense selection, they often fail to adapt to anthropogenic stresses such as pollution and acidification and instead become extinct. 3. Experimental selection lines of algae show no specific adaptation to ele- vated CO2, but instead lose their carbon-concentrating mechanism through mutational degradation. This is likely to reduce the effectiveness of the oceanic carbon pump. Elevated CO2 is also likely to lead to changes in phytoplankton community composition, although it is not yet clear what these will be. We emphasize the importance of experimental evolution in understanding and predicting the biological response to global change. This will be one of the main tasks of evolutionary biologists in the coming decade. Evolutionary Applications ISSN 1752-4563 �� 2008 The Authors Journal compilation �� 2008 Blackwell Publishing Ltd 1 (2008) 3���16 3

Selection in variable environments Change is generally for the worse It is widely believed that most populations, most of the time, should have become well adapted to their conditions of life through the past operation of natural selection. Mutation is generally deleterious, at least in natural condi- tions (Keightley and Lynch 2003). Environmental change tends to move the average phenotype of well-adapted pop- ulations further from its optimal value and thereby to reduce mean fitness. Moreover, enemies such as pathogens and predators are likely to be selected to exploit the most frequent types in their target populations, driving a contin- uous reduction in mean fitness (Van Valen 1973). Conse- quently, either genetic or environmental change will be perceived by most individuals as harmful. The natural pace of environmental change A physical factor changes on all time scales, and at any given time scale varies by some characteristic amount. The rate of increase in environmental variance over time provides a quantitative measure of variability. This is often adequately described by a power law, VE = atz, where the exponent z expresses the rate of increase of var- iance over time. This means that the log difference in physical conditions at a site increases with log elapsed time at a rate z/2. For example, Koscielny-Bunde et al. (1998) analysed deviations of daily maximum tempera- ture from their seasonal average values, estimated with very voluminous and exact data taken at weather stations around the world over a period of more than a century. They found that plots of log VE on log elapsed time are almost perfectly linear with slope z = 0.65. Pelletier (1997) obtained z = 0.75 for ice-core samples for periods between 1 month and 2000 years. This environmental variability may drive changes in the growth and abun- dance of populations. Pimm and Redfearn (1988) showed that ln abundance N of animals also follows a power law, and since the ln variance of ln N is equivalent to ln [N(t + 1)/N(t)] this implies that the variance of realized growth rate increases indefinitely over time, apparently with exponent 0.36 (Inchausti and Halley 2002). Spatial variation also increases with distance according to a power law, typically with smaller exponents of z = 0.1���0.2 (Bell et al. 1993). Hence, as a lineage is extended through time the conditions that its members experience will grow steadily more variable. Variable and fluctuating selection Environmental variability will cause the strength and direction of selection to change over time. Studies of natural populations have shown that selection is often strong (Hereford et al. 2004) and that heritability is often high (Mousseau and Roff 1987). One explanation of these apparently contradictory generalizations is that selection often changes direction, because offspring grow up in a different place and at a different time from their parents. The variability of selection among isozyme genotypes in Daphnia populations was documented by Lynch (1987), who found that the standard deviation of the selection coefficient over time was at least 0.1. There are many detailed case studies of selection that varies widely in time (Grant and Grant 2002) or space (Snaydon and Davies 1982), even in within a few square metres of natural envi- ronment (Stewart and Schoen 1987). Hence, populations might often be rather imprecisely adapted to local condi- tions of growth. This can be evaluated by measuring the selection gradient (partial regression of fitness on charac- ter state) and calculating the distance between the optimal phenotype and the population mean, in units of pheno- typic standard deviations. For the studies of stabilizing selection collated by Kingsolver et al. (2001) this distance is exponentially distributed with mean 3.9 that is, the population was further than one phenotypic standard deviation from the optimum in about one-half of all cases, and further than 2 SD in one-third. It can also be evaluated by reciprocal transplant experiments. Where these involve clearly distinct ecotypes or species they usu- ally show that residents are markedly superior to incom- ers (Schluter 2000 Table 5.1). When morphologically undifferentiated populations are transplanted, however, there is little tendency for residents to be superior except at very large distances or between clearly distinct habitats (Bell 2008, Table 5). These facts are consistent with the view that conditions often vary widely in time and space, generating strong but fluctuating selection. Rescue from extinction by adaptation Most individuals are sufficiently versatile to accommo- date the mundane level of variability experienced within a lifetime. Offspring will encounter conditions different from their parents but will adjust to them through phe- notypic plasticity. The perpetual increase of environmen- tal variance, however, may eventually lead to a change in conditions too great for individuals to survive or repro- duce successfully, so that the population begins to decline. Lineages can still persist by migrating or dispers- ing to new sites. If neither plasticity nor dispersal will serve, however, they must either adapt or die out. Natu- ral selection may succeed in restoring adaptedness if types capable of growing in the new conditions exist in the population or arise before it becomes extinct. It is most likely to do so when the change is modest and the Adaption, extinction and global change Bell and Collins �� 2008 The Authors 4 Journal compilation �� 2008 Blackwell Publishing Ltd 1 (2008) 3���16