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.

Fitness variation across subtle environmental perturbations reveals local modularity and global pleiotropy of adaptation

“…Although directional selection may promote multiple mutants that affect similar fitness-relevant phenotypes in the evolution condition, each mutant could have disparate latent phenotypic effects that do not contribute immediately to fitness. When the environment changes, these disparate phenotypic effects may be revealed, imposing fitness costs of different magnitudes or allowing for diverse solutions to a variety of possible new environments ( Bono et al, 2017 ; Chavhan et al, 2020 ; Jerison et al, 2020 ; Li et al, 2019 ). This latent phenotypic complexity also has the potential to alter the future adaptive paths that a population takes even in a constant environment.…”

Asymmetric evolvability leads to specialization without trade-offs

“…A yeast evolution experiment across eight environments showed a general pattern of specialization, but not necessarily trade-offs (Jerison et al 2020); analysis of replicate populations showed a large role for stochastic forces in evolution. Chavhan et al (2020) provide an empirical example in which costs of adaptation increase with population size, underlining the point that trade-offs are an outcome of evolutionary processes as well as a determinant of their course. Replicate experiments that yield trade-offs sometimes but not always are expected if possible mutations vary in their degree of antagonistic pleiotropy (Bono et al 2017).…”

Asymmetric Evolvability Leads to Specialization without Trade-Offs

“…Experimental evolution methods have a long history of application to this question (Kassen 2002;Bono et al 2020), and continue to help uncover complex variation in these costs. For example, costs have been observed to be greater in larger populations (Chavhan et al 2020), highly variable across replicate experiments (Jerison et al 2020), or to appear late in adaptation (Satterwhite & Cooper 2015). In the field, reciprocal transplant experiments with plant and animal species reveal highly variable costs of adaptation with only a weak signal of trade-offs (Hereford 2009).…”