Edited by Boris I. Shraiman, University of California, Santa Barbara, CA, and approved September 21, 2018 (received for review May 1, 2018)
Most mutations are subject to competitive exclusion: Their descendants will either take over the population or go extinct. In special cases, a mutant may evade competitive exclusion by exploiting a different ecological niche. Both types of mutations can be found in large microbial populations, yet little is known about how they interact. By generalizing consumer-resource theory to include heritable beneficial mutations, we show that interactions between diversification and competitive exclusion can produce dramatic departures from existing models of evolution or ecology alone. These results suggest that short-term evolutionary processes could play an important role in shaping the structure of microbial communities.
Microbial communities can evade competitive exclusion by diversifying into distinct ecological niches. This spontaneous diversification often occurs amid a backdrop of directional selection on other microbial traits, where competitive exclusion would normally apply. Yet despite their empirical relevance, little is known about how diversification and directional selection combine to determine the ecological and evolutionary dynamics within a community. To address this gap, we introduce a simple, empirically motivated model of eco-evolutionary feedback based on the competition for substitutable resources. Individuals acquire heritable mutations that alter resource uptake rates, either by shifting metabolic effort between resources or by increasing the overall growth rate. While these constitutively beneficial mutations are trivially favored to invade, we show that the accumulated fitness differences can dramatically influence the ecological structure and evolutionary dynamics that emerge within the community. Competition between ecological diversification and ongoing fitness evolution leads to a state of diversification–selection balance, in which the number of extant ecotypes can be pinned below the maximum capacity of the ecosystem, while the ecotype frequencies and genealogies are constantly in flux. Interestingly, we find that fitness differences generate emergent selection pressures to shift metabolic effort toward resources with lower effective competition, even in saturated ecosystems. We argue that similar dynamical features should emerge in a wide range of models with a mixture of directional and diversifying selection.
Author contributions: B.H.G., S.M., and O.H. designed research, performed research, and wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1807530115/-/DCSupplemental.
Published under the PNAS license.
