Evolution of cooperation and control of cheating in a social microbe

Abstract

Much of what we know about the evolution of altruism comes from animals. Here, we show that studying a microbe has yielded unique insights, particularly in understanding how social cheaters are controlled. The social stage of Dictylostelium discoideum occurs when the amoebae run out of their bacterial prey and aggregate into a multicellular, motile slug. This slug forms a fruiting body in which about a fifth of cells die to form a stalk that supports the remaining cells as they form hardy dispersal-ready spores. Because this social stage forms from aggregation, it is analogous to a social group, or a chimeric multicellular organism, and is vulnerable to internal conflict. Advances in cell labeling, microscopy, single-gene knockouts, and genomics, as well as the results of decades of study of D. discoideum as a model for development, allow us to explore the genetic basis of social contests and control of cheaters in unprecedented detail. Cheaters are limited from exploiting other clones by high relatedness, kin discrimination, pleiotropy, noble resistance, and lottery-like role assignment. The active nature of these limits is reflected in the elevated rates of change in social genes compared with nonsocial genes. Despite control of cheaters, some conflict is still expressed in chimeras, with slower movement of slugs, slightly decreased investment in stalk compared with spore cells, and differential contributions to stalk and spores. D. discoideum is rapidly becoming a model system of choice for molecular studies of social evolution.

Fig. 1.

D. discoideum fruiting bodies on an agar plate.

Fig. 2.

Colony cycles of D. discoideum. This study focuses on the social cycle, but the sexual cycle is a promising area for future study.

Fig. 3.

In the social stage, clones may take advantage of their partner in three different ways. They may allocate cells to spore and stalk in the same proportions as alone but allocate less to stalk than their partner, fixed cheating. They may modify their behavior in chimera to take advantage of their partner, facultative cheating. Third, a social parasite can only make fruiting bodies in chimera with a victim.

Fig. 4.

Conflict is manifested in chimeras in the form of shorter stalk lengths, shorter migration distances, and unequal spore/stalk ratios.

Fig. 5.

Cheating can be controlled in the social stage if fruiting bodies are clonal, as might happen if they arise from different patches. They may mix but then sort into nearly clonal fruiting bodies through kin discrimination. Pleiotropic effects may prevent cheating genes from spreading. Caste fate may be determined through a lottery, with cells in the M or S stage of the cell cycle becoming stalk and those in the G2 stage becoming spore. D. discoideum apparently has no G1 stage, although this is controversial.