Predation, evo-devo, and historical contingency: A nematode predator drives evolution of aggregative multicellularity

Abstract Regulated aggregation and differentiation of cells is an intriguing form of multicellularity that produces diverse morphological forms, resulting from an interplay of complex evolutionary, regulatory, behavioral, and social mechanisms. We investigate the potential for predation to shape aggregative multicellularity evolution across different combinations of three species comprising a multi-trophic food web. The bacterium Myxococcus xanthus , which can develop into spore-filled fruiting bodies, is a mesopredator; the bacterivorous nematode Pristionchus pacificus is an apex predator, and the bacterium Escherichia coli is a shared basal prey for both predators. The number and morphology of M. xanthus fruiting bodies responds evolutionarily to nematodes, regardless of whether E. coli is present. E. coli alone with M. xanthus reduces both fruiting body formation and spore production, but the presence of nematodes eliminates those effects. M. xanthus lineages with an ancestral antibiotic resistance mutation evolved less overall, revealing strong historical contingency and suggesting potential tradeoffs between antibiotic resistance and responsiveness to biotic selection. Our results suggest that predation both of and by mesopredators has played important roles in the evolution of aggregative multicellularity and reveal complex inter-trophic evolutionary interactions in a relatively simple three-species food web.