Environmental fluctuations have been suggested to select for genotypes that are capable of performing well across a wide range of different environments (e.g., Levins 1968; Lynch and Gabriel 1987; Gomulkiewicz and Kirkpatrick 1992; Scheiner 1993; Kassen 2002). This evolved tolerance could also decrease or increase the ability to inhabit other, novel, environments (e.g., Huey and Hertz 1984; Hoffmann and Parsons 1993a,b; Cullum et al. 2001; Bubliy and Loeschcke 2005). Thus, in some cases, preadaptation to a novel environment could play a key role in species invasions and in the emergence of new pathogens (Arnold et al. 2007; Lee and Gelembiuk 2008).
Environmental fluctuations have the potential to cause several changes in populations and individuals. For example, fluctuating selection could maintain genetic variation and polymorphism (Levene 1953; MacKay 1980, see also Kassen 2002) and potentially lead to divergent evolution between populations (Cooper and Lenski 2010). Moreover, rapidly and especially unpredictably fluctuating environments could select for reversible phenotypic plasticity and bet-hedging (e.g., Cohen 1966; Arnoldini et al. 2012). However, most of the theoretical work has concentrated on the changes in tolerance curve: fluctuating environments are suggested to select for individuals with increased tolerance over the most frequently experienced conditions, as their tolerance curve width evolves to match the width of the environmental fluctuations (Levins 1968; Lynch and Gabriel 1987; Gomulkiewicz and Kirkpatrick 1992; Scheiner 1993; Kassen 2002). However, the outcome of evolution might be affected by the frequency of environmental fluctuations relative to organism's generation time; depending on theoretical assumptions, generalism might be more likely to evolve if the environmental fluctuations occur within generation (Lynch and Gabriel 1987) or if it happens between generations (Levins 1968, p. 20; Gilchrist 1995). Yet, many of the experimental studies to date demonstrate that generalism emerges when populations are evolving in fluctuating environments regardless of the frequency of the variation (reviewed in Kassen 2002 and Buckling et al. 2006, but see: Jasmin and Kassen 2007). Despite the several attempts to test evolution of generalism, only few studies have addressed the impact of fluctuating temperatures on evolution of thermal tolerance (Bennet and Lenski 1993; Ketola et al. 2004; Duncan et al. 2011). Testing evolution of generalism in fluctuating temperatures is important considering the predictions of climate change scenarios that predict not only increased mean temperatures but also increased thermal variation (IPCC 2007).
Adaptation to environmental fluctuations (e.g., temperature fluctuations) can also lead to general environmental tolerance. For example, expression of heat shock proteins, which have been associated with resistance against several kinds of stresses (reviewed in Sørensen et al. 2003), can evolve as a response to fluctuating temperature (Ketola et al. 2004). Moreover, growing and reproducing in a varying environment can be energetically expensive, and therefore, selection could simply favor energetic efficiency and better growth or viability (van Noordwijk and de Jong 1986; Parsons 1990, 2005; Scheiner and Yampolsky 1998; see also Whitlock 1996). This, in turn, can translate directly to increased tolerance to any kind of stressful environment. However, adapting to fluctuating environment might also be costly. For example, evolution of broad tolerance could lead to lowered performance in optimal environments (e.g., Levins 1968; Huey and Kingsolver 1993). Alternatively, the costs of changed tolerance could correlate negatively with fitness in some other ecological context in some other environment (Huey and Hertz 1984; Friman et al. 2009). In addition, the lowered fitness in other environments could also result from mutation accumulation on characters that are not used in fluctuating environment (Whitlock 1996; Hall and Colegrave 2008; Mikonranta et al. 2012). The “hidden” fitness costs, evident only in different ecological contexts, could potentially explain why the cost of generalism is not often found in the selective environment (reviewed in Kassen 2002).
Thus, evolution in fluctuating environments could also be an important determinant for population's performance when species are exposed to a novel environment, either due to changes in local conditions, or because of introduction to a new habitat. Interestingly, evidence from the wild suggests that the source areas of invasive species are often characterized by disturbance. For example, this seems to hold for weedy plants, invasive argentine ants experiencing repeated flooding in their native areas, and for species that invaded the Great Lakes from disturbed habitats of the old world (reviewed in Lee and Gelembiuk 2008). Evolution of species invasiveness is also analogous to the emergence of new virulent microorganisms. There is growing evidence that a range of ecological and environmental factors such as predation or temperature can affect the virulence of opportunistic pathogens (e.g., Brüssow 2007; Casadevall and Pirofski 2007; Friman et al. 2009, 2011; Barrett et al. 2011; Mikonranta et al. 2012). Specifically, Arnold et al. (2007) have suggested that environmental fluctuations play an important role in preselecting virulence traits of bacterial pathogens. Despite the indirect evidence of correlative changes with invasiveness and virulence, there is no study explicitly testing if environmental fluctuations concurrently select for generalism, invasiveness (i.e., general tolerance across many different environments), and virulence.
Here, we set up a replicated evolution experiment where populations of a common, broad-spectrum opportunistic bacterial pathogen Serratia marcescens were propagated under constant or daily fluctuating temperatures for about 1000 generations. First, we tested if clones from populations experiencing fluctuating temperature had evolved temperature generalism (e.g., Levins 1968; Huey and Kingsolver 1993). Second, we tested how evolution in fluctuating versus constant environment affected the growth and yield of the bacteria in several novel environments including the presence of chemicals, the presence of natural microbial enemies (ciliate predator Tetrahymena thermophila and lytic bacteriophage PPV (Podoviridae; Friman et al. 2011). Moreover, we tested if virulence in its natural host Drosophila melanogaster (Flyg et al. 1980) had changed because of fluctuating environments. Finally, we tested if selection by fluctuating environments leads to more divergent evolution between replicate populations (Cooper and Lenski 2010).