Expression of defense genes in Drosophila evolves under a different selective regime from expression of other genes

Genes involved in host-pathogen interactions are expected to be evolving under complex coevolutionary dynamics, including positive directional and/or frequency-dependent selection. Empirical work has largely focused on the evolution of immune genes at the level of the protein sequence. We examine components of genetic variance for transcript abundance of defense genes in Drosophila melanogaster and D. simulans using a diallel and a round robin breeding design, respectively, and infer modes of evolution from patterns of segregating genetic variation. Defense genes in D. melanogaster are overrepresented relative to nondefense genes among genes with evidence of significant additive variance for expression. Directional selection is expected to deplete additive genetic variance, whereas frequency-dependent selection is expected to maintain additive variance. However, relaxed selection (reduced or no purifying selection) is an alternative interpretation of significant additive variation. Of the three classes of defense genes, the recognition and effector classes show an excess of genes with significant additive variance; whereas signaling genes, in contrast, are overrepresented for dominance variance. Analysis of protein-coding sequences revealed no evidence for an association between additive or dominance variation in expression and directional selection. Both balancing selection driven by host-pathogen coevolution and relaxed selection for expression of uninduced defense genes are viable interpretations of these data.