Genetic signatures of microbial altruism and cheating in social amoebas in the wild

Abstract

Many microbes engage in social interactions. Some of these have come to play an important role in the study of cooperation and conflict, largely because, unlike most animals, they can be genetically manipulated and experimentally evolved. However, whereas animal social behavior can be observed and assessed in natural environments, microbes usually cannot, so we know little about microbial social adaptations in nature. This has led to some difficult-to-resolve controversies about social adaptation even for well-studied traits such as bacterial quorum sensing, siderophore production, and biofilms. Here we use molecular signatures of population genetics and molecular evolution to address controversies over the existence of altruism and cheating in social amoebas. First, we find signatures of rapid adaptive molecular evolution that are consistent with social conflict being a significant force in nature. Second, we find population-genetic signatures of purifying selection to support the hypothesis that the cells that form the sterile stalk evolve primarily through altruistic kin selection rather than through selfish direct reproduction. Our results show how molecular signatures can provide insight into social adaptations that cannot be observed in their natural context, and they support the hypotheses that social amoebas in the wild are both altruists and cheaters.

Keywords: Dictyostelium discoideum; altruism; cheating; kin selection; social amoeba.

Fig. 1.

Genes that change expression in chimeric mixtures show elevated rates of adaptive evolution α. Each violin plot shows a Gaussian kernel-density plot of 1,000 bootstrap replicates of α, the median, the interquartile range, and the 95% range or confidence interval (Table S1) (A) Bootstrap distributions for the 78 chimera-biased genes and for samples of 78 from genomic background genes. The chimera-biased genes show significantly higher α (P < 0.002 permutation test). (B) Bootstrap distributions for the chimera-biased genes separated into the 19 up-regulated genes and 59 down-regulated genes, both of which are significantly different from background genes (up-regulated P = 0.006, down-regulated P = 0.034, permutation tests).

Fig. 2.

Nonsynonymous diversity π_Ν supports kin selection, not direct selection, in prestalk cells. Violin plots (Fig. 1) for distributions from 10,000 resamples of the prestalk π_N: prespore π_N, the ratio of nonsynonymous nucleotide diversity π_N for genes expressed significantly more in prestalk to π_N for genes expressed significantly more in prespore. (A) All prestalk-biased genes (n = 992) and prespore-biased genes (n = 879). (B) Prestalk-biased genes (n = 145) and prespore-biased genes (n = 113) that are not expressed in the vegetative stage (Table S3).