Reduced social function in experimentally evolved Dictyostelium discoideum implies selection for social conflict in nature

Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimeric aggregates containing multiple unrelated lineages, cheaters can gain an advantage by undercontributing, but the extent to which wild D. discoideum has adapted to cheat is not fully clear. In this study, we experimentally evolved D. discoideum in an environment where there were no selective pressures to cheat or resist cheating in chimeras. D. discoideum lines grown in this environment evolved reduced competitiveness within chimeric aggregates and reduced ability to migrate during the slug stage. By contrast, we did not observe a reduction in cell number, a trait for which selection was not relaxed. The observed loss of traits that our laboratory conditions had made irrelevant suggests that these traits were adaptations driven and maintained by selective pressures D. discoideum faces in its natural environment. Our results suggest that D. discoideum faces social conflict in nature, and illustrate a general approach that could be applied to searching for social or non-social adaptations in other microbes. SIGNIFICANCE STATEMENT Microbes interact in diverse and important ways, but the difficulty of directly observing microbes in nature can make it challenging to understand the adaptive significance of these interactions. In this study, we present an experimental evolution approach to infer the selective pressures behind an apparently social trait in the microbe Dictyostelium discoideum. We take advantage of the observation that organisms ‘use it or lose it’ – when selective pressures are relaxed, adaptations that evolved in response to those pressures tend to be lost. Our work helps resolve debate over the importance of cheating in D. discoideum, and demonstrates a general approach that could be applied to the study of other microbial traits that are difficult to observe in nature.