Detecting the Molecular Signature of Social Conflict: Theory and a Test with Bacterial Quorum Sensing Genes

Abstract

Extending social evolution theory to the molecular level opens the door to an unparalleled abundance of data and statistical tools for testing alternative hypotheses about the long-term evolutionary dynamics of cooperation and conflict. To this end, we take a collection of known sociality genes (bacterial quorum sensing [QS] genes), model their evolution in terms of patterns that are detectable using gene sequence data, and then test model predictions using available genetic data sets. Specifically, we test two alternative hypotheses of social conflict: (1) the "adaptive" hypothesis that cheaters are maintained in natural populations by frequency-dependent balancing selection as an evolutionarily stable strategy and (2) the "evolutionary null" hypothesis that cheaters are opposed by purifying kin selection yet exist transiently because of their recurrent introduction into populations by mutation (i.e., kin selection-mutation balance). We find that QS genes have elevated within- and among-species sequence variation, nonsignificant signatures of natural selection, and putatively small effect sizes of mutant alleles, all patterns predicted by our evolutionary null model but not by the stable cheater hypothesis. These empirical findings support our theoretical prediction that QS genes experience relaxed selection due to nonclonality of social groups, conditional expression, and the individual-level advantage enjoyed by cheaters. Furthermore, cheaters are evolutionarily transient, persisting in populations because of their recurrent introduction by mutation and not because they enjoy a frequency-dependent fitness advantage.