Lack of ecological context can create the illusion of social success in Dictyostelium discoideum

TL;DR

This study demonstrates that ecological context and tradeoffs among multiple traits explain the apparent social success of Dictyostelium discoideum, challenging previous interpretations based solely on spore production.

Contribution

It introduces a unifying ecological framework that accounts for multiple trait tradeoffs, resolving paradoxes in social behavior interpretations of Dictyostelium discoideum.

Findings

Tradeoffs between spore production and vegetative growth, development time, spore size, and viability.

Existing experimental results can be explained without social interactions.

Ecological context is crucial for understanding complex life histories.

Abstract

Studies of cooperation in microbes often focus on one fitness component, with little information about or attention to the ecological context, and this can lead to paradoxical results. The life cycle of the social amoeba Dictyostelium discoideum includes a multicellular stage in which not necessarily clonal amoebae aggregate upon starvation to form a possibly chimeric (genetically heterogeneous) fruiting body made of dead stalk and spores. The lab-measured reproductive skew in the spores of chimeras indicates strong social antagonism; this should result in low genotypic diversity, which is inconsistent with observations from nature. Two studies have suggested that this inconsistency stems from the one-dimensional assessment of fitness (spore production) and that the solution lies in tradeoffs between multiple traits, e.g.: spore size versus viability; and staying vegetative versus becoming dormant. We theoretically explore different tradeoff-implementing mechanisms and provide a unifying ecological framework in which the two tradeoffs above, as well as novel ones, arise collectively in response to characteristics of the environment. We find that spore production comes at the expense of vegetative cell production, time to development, and, depending on the experimental setup, spore size and viability. Furthermore, we find that all existing experimental results regarding chimeric mixes can be qualitatively recapitulated without needing to invoke social interactions, which allows for simple resolutions to previously paradoxical results. We conclude that the complexities of life histories, including social behavior and multicellularity, can only be understood in the appropriate multidimensional ecological context.