Aggregative multicellularity occurs when dispersed cells join together to form a highly cooperative unit, in contrast to clonal multicellular organisms formed by cells that remain in contact after descent from a single cell. Because aggregative groups may include non-relatives, aggregative multicellular organisms should be particularly vulnerable to the rise of cheater cells that take advantage of social goods without paying the costs, reducing cooperation, and even threatening extinction. We review the key mechanisms by which aggregative multicellular organisms control cheaters with a focus on the best studied aggregative organisms, Myxococcus xanthus and Dictyostelium discoideum. These include various passive and active mechanisms to maintain high relatedness within aggregates, to enforce cooperation on aggregate members, and the costs of cheating on other key functions. Ultimately, aggregative multicellular organisms are not that different from clonal organisms descended from a single cell.

Multicellular organisms that form by aggregation of cells arguably do not achieve high levels of complexity. Conflict among the cells is a widely accepted explanation for this, but an alternative hypothesis is that mixing cells of different genotypes leads to failures of coordination, which we call the “coordination hypothesis.” We empirically tested the coordination hypothesis in the social amoeba Dictyostelium discoideum. We mixed D. discoideum clones that had evolved in isolation for generations and acquired mutations that have not been tested against each other by selection. To quantify the effect of incompatibilities, we measured performance in terms of the developmental traits of slug migration and spore production. Importantly, we mixed lines evolved from the same ancestor under conditions that would not select for the evolution of de novo kin recognition. Our results show no evidence of incompatibilities in four traits related to the coordinated movement of slugs toward light in the social amoeba. Spore production was higher than expected in mixtures, in apparent contradiction to the coordination hypothesis. However, we found support for coordination incompatibilities in an interaction between migration and spore production: in mixtures, fewer cells succeeded at both migrating and becoming spores. Most living things that we can see with our naked eyes develop from a single fertilized egg cell. Even dinosaurs hatched from eggs. Why are eggs so successful over the evolutionary history of life? One theory is eggs result in a multicellular body where the daughter cells are genetically identical, and therefore have nothing to gain from conflict with other cells. Another theory is that when individual cells acquire changes independently of other cells, they may become incompatible with each other. Such cells can be thought of as speaking different genetic languages, such that they lose the ability to communicate during a crucial process like the development of the body. Here we have tested this latter theory, which we call the “coordination hypothesis” in a species of social amoeba. Of several traits tested, one showed strong evidence of poorer coordination in mixtures, supporting the coordination hypothesis.

Biological diversity driven by endosymbiosis arises from the intertwined evolution of microbes and their hosts. Each partner affects the fitness and therefore the evolution of the other. Here, we tested a further question: does the history of symbiosis affect evolution even after the partnership is dissolved? We analyzed phenotypic data from experimentally evolved strains of Dictyostelium discoideum hosts, each of which had had its symbiont removed, to study how their traits evolved. We found that host trait evolution was affected by the prior history of infection, specifically by which of three Paraburkolderia bacterial symbionts had been removed. Thus, symbionts affect not only current evolution but also generate path dependence that affects the subsequent evolutionary trajectories even after the symbionts are lost.

Selection for cooperation or conflict in multicellular organisms that develop from a mixture of cells has been widely appreciated, but unselected effects of mixing could also have important fitness consequences to the resulting chimeras. We formalized this idea as the ‘developmental incompatibility hypothesis’ and empirically tested it in the social amoeba Dictyostelium discoideum. We mixed D. discoideum that evolved in isolation for generations and accumulated mutations that have not been tested against each other by selection. To quantify the effect of developmental incompatibilities in experimental lines that evolved in the presumed absence of kin recognition, we measured the developmental traits of slug migration and spore production. Our results show no evidence for incompatibilities in coordinated movement towards light in the social amoeba. We found support for developmental incompatibilities from our spore production result. The effect was especially clear for a small proportion of fruiting bodies that developed after migration. For slugs that did not migrate, mixing could be harmful if they are smaller or if, the stalks of such fruiting bodies are shorter which would hamper dispersal. Our results indicate that the detrimental fitness consequences of developmental incompatibilities may be context-dependent.