Metabolic evolution in response to interspecific competition in a eukaryote

Competition can drive rapid evolution which, in turn, alters the trajectory of ecological communities. The role of eco-evolutionary dynamics in ecological communities is increasingly well-appreciated, but a mechanistic framework for identifying the types of traits that will evolve, and their trajectories, is required. Metabolic theory makes explicit predictions about how competition should shape the evolution of metabolism and size but these predictions have gone largely untested, particularly in eukaryotes. We use experimental evolution of a eukaryotic phototroph to examine how metabolism, size, and demography coevolve under both inter- and intra-specific competition. We find that the focal species evolves a smaller body size in response to competition, reducing density-dependence and maximizing carrying capacity. Metabolic theory successfully predicted most of these adaptations, but we also find important departures from theory. Longer-term evolution (70 generations) led to Pareto improvements in both population growth rate and carrying capacity, suggesting that classic r-K trade-offs observed among species can be evaded within species. The evasion of this trade-off appeared to arise due to the rapid evolution of enhanced metabolic plasticity: lineages exposed to competition evolved more labile metabolisms that tracked resource availability more effectively than lineages that were competition-free. We predict that rapid evolution in both size and metabolism may be a ubiquitous feature of adaptation to changing resource regimes that occur via species invasions and environmental change.