Genetic Variation in a Cellular Adhesin Suggests Self-Discrimination Driven by Ecological Competition in Yeast

Abstract

Kin selection can explain most examples of altruism, with kin recognition common in many animal systems. In microbes, cooperative behaviors involving cell-cell adherence generally rely on “kind” recognition, in which a greenbeard locus signals cooperation regardless of overall relatedness. However, in motile microbes that must locate one another and avoid cheaters, rare examples of kin- and self-recognition have been reported; variable membrane-associated proteins confer discrimination. In contrast, clonal growth of non-motile microbes generates patches of highly-related individuals, thus obviating the need for discriminatory systems. Instead, kind-recognition adhesion can serve as an adaptive strategy for a lineage in ecological competition. Here we use population genetic data to investigate Flo11, a membrane-anchored adhesion protein required for social phenotypes in the budding yeast, and find evidence that it functions in both ways. Surprisingly, the regions implicated in cell-cell interaction exhibit a signature of positive selection, suggesting the possibility of a recognition system in which cells preferentially interact with like kinds. At an upstream activation site, there is evidence for balancing selection, thus suggesting selection on variegated gene expression, which has been proposed as an adaptive strategy in clonal yeast populations. Phenotypic assays support these inferences and demonstrate that different alleles confer a competitive advantage. Unlike in motile microbes where cheater avoidance is driving the evolution of recognition, competition among clones may be the evolution of homophilic binding in S. cerevisiae. Thus, the interplay between inter-clone competition and intra-clone cooperation in spatially structured microbial communities may lead to complex recognition systems.