The evolution of adhesiveness as a social adaptation

Abstract

Cellular adhesion is a key ingredient to sustain collective functions of microbial aggregates. Here, we investigate the evolutionary origins of adhesion and the emergence of groups of genealogically unrelated cells with a game-theoretical model. The considered adhesiveness trait is costly, continuous and affects both group formation and group-derived benefits. The formalism of adaptive dynamics reveals two evolutionary stable strategies, at each extreme on the axis of adhesiveness. We show that cohesive groups can evolve by small mutational steps, provided the population is already endowed with a minimum adhesiveness level. Assortment between more adhesive types, and in particular differential propensities to leave a fraction of individuals ungrouped at the end of the aggregation process, can compensate for the cost of increased adhesiveness. We also discuss the change in the social nature of more adhesive mutations along evolutionary trajectories, and find that altruism arises before directly beneficial behavior, despite being the most challenging form of cooperation.

DOI: http://dx.doi.org/10.7554/eLife.08595.001

eLife digest

Throughout the living world, organisms work together in groups and help each other to survive. Indeed, multicellular organisms such as plants and animals owe their existence to cooperation. Life on Earth was initially made up of single cells, some of which evolved the ability to stick to each other and work together to form tissues and organs. However, developing the ability to adhere to other cells costs energy that could otherwise be used by the cell to ensure its own survival and proliferation. How multicellularity emerged, despite such costs, remains puzzling, in particular in groups of cells that do not share a common ancestor.

Now, Garcia, Doulcier and De Monte have produced a mathematical model that shows how large cohesive groups of cells can evolve. Over long periods of time, these groups can emerge from a population of non-adhesive cells through a series of small mutations that increase the overall adhesiveness of the cells in the group. Furthermore, the evolution of cohesive groups can arise just through the cells randomly interacting. By contrast, previous models that investigated how social groups form have tended to assume that particular cell types preferentially interact with each other.

The model also suggests that the costs associated with developing adhesiveness can be partially compensated for in groups that contain cells with different abilities to adhere to each other. This means that individual cells that do not join any groups also play a crucial role in the development of cohesive groups. Finally, Garcia, Doulcier and De Monte challenge the popular belief that social behavior arises primarily because it is beneficial to the individual performing those actions. Instead, the model suggests that selfless cooperation may occur first, and only afterwards lead to the evolution of behavior that is mutually beneficial for the individuals involved.

In the future, the plausibility of the evolutionary path suggested by the model could be tested in experiments using single-celled organisms such as some amoebae and bacteria, that, along their life cycle, alternatively live alone and in cohesive groups.

DOI: http://dx.doi.org/10.7554/eLife.08595.002