Larger bacterial populations evolve heavier fitness trade-offs and undergo greater ecological specialization

Abstract

Evolutionary studies over the last several decades have invoked fitness trade-offs to explain why species prefer some environments to others. However, the effects of population size on trade-offs and ecological specialization remain largely unknown. To complicate matters, trade-offs themselves have been visualized in multiple ways in the literature. Thus, it is not clear how population size can affect the various aspects of trade-offs. To address these issues, we conducted experimental evolution with Escherichia coli populations of two different sizes in two nutritionally limited environments, and studied fitness trade-offs from three different perspectives. We found that larger populations evolved greater fitness trade-offs, regardless of how trade-offs are conceptualized. Moreover, although larger populations adapted more to their selection conditions, they also became more maladapted to other environments, ultimately paying heavier costs of adaptation. To enhance the generalizability of our results, we further investigated the evolution of ecological specialization across six different environmental pairs, and found that larger populations specialized more frequently and evolved consistently steeper reaction norms of fitness. This is the first study to demonstrate a relationship between population size and fitness trade-offs, and the results are important in understanding the population genetics of ecological specialization and vulnerability to environmental changes.

Fig. 1. Schematic representation of ecological specialization across two environments.

All the fitness values are scaled by the ancestral value (=1 (horizontal black line)). The error bars represent 95% confidence intervals. Significant ecological specialization occurs when the reaction norms of fitness intersect (which happens when the unambiguous fittest type in one environment is not the unambiguous fittest type in the other environment).

Fig. 2. Correlation between relative fitness values in galactose and thymidine minimal media after evolution in these environments at two different population sizes.

The black line represents the best linear fit (R² = 0.63); the dotted lines represent ancestral levels of fitness.

Fig. 3. Loss of fitness below the ancestral levels in the away environments.

In each case, the loss in relative fitness was computed as the difference between the descendant population’s relative fitness and the ancestor’s relative fitness. L and S represent large and small populations, respectively. The solid lines in the box plots mark the 25th, 50th, and 75th percentiles, while the whiskers mark the 10th and 90th percentiles; the dashed lines represent means (N = 6). The dotted line represents no loss from the ancestral fitness levels. See the text for details.

Fig. 4. Reaction norms of fitness across the six home-away environmental pairs used in our study.

The error bars represent SEM (N = 6). The asterisks represent significant ecological specialization with respect to the ancestor for the corresponding home-away pair; “NS” denotes that the corresponding ecological specialization was not significant (see Table S1 and the text for details). The dotted lines represent ancestral reaction norms. Significant specialization happened when the reaction norms of a treatment population intersected with the ancestral norm. a Reaction norms for populations selected in Thy (TL (large) and TS (small)). b Reaction norms for populations selected in Gal (GL (large) and GS (small)). Also see Fig. 5 for reaction norm slopes across the six environmental pairs.

Fig. 5. Slopes of reaction norms of the fitness of our experimental populations across six environmental pairs.

The asterisks represent significant differences (single-sample t-tests (P < 0.05)) from the ancestral slope (=0); “NS” denotes that the corresponding slopes are not significantly different from 0. The solid lines in the box plots mark the 25th, 50th, and 75th percentiles, while the whiskers mark the 10th and 90th percentiles; the thick horizontal lines represent means (N = 6). See the text and Table S2 for details, and Fig. 4 for reaction norms across the six environmental pairs. a Populations evolved in Thy: reaction norm slopes (L > S (P < 10^–6)). b Populations evolved in Gal: reaction norm slopes (L > S (P < 10^–2)). Overall, the larger populations had steeper reaction norms.