The effect of developmental pleiotropy on the evolution of immune genes in Drosophila melanogaster

Abstract

AbstractThe pressure to survive relentless pathogen exposure explains the frequent observation that immune genes are among the fastest-evolving ones in the genomes of many taxa, but an intriguing proportion of immune genes also appear to be under purifying selection. Though variance in evolutionary signatures of immune genes is often attributed to differences in gene-specific interactions with microbes, this explanation neglects the possibility that immune genes pleiotropically participate in other biological processes that could constrain adaptive selection. In this study, we analyzed available transcriptomic and manual annotation data from Drosophila melanogaster to uncover substantial pleiotropic overlap in the developmental and immunological functions of genes involved in immune signaling. As developmental pleiotropy could constrain both the deployment and evolution of a gene product for immunological purposes, we predicted that pleiotropic immune genes would show stronger signatures of purifying selection than non-pleiotropic immune genes. We further predicted that, within the pleiotropic gene class, genes expressed early in development or more broadly across developmental stages would be under stronger purifying selection than genes with stage-specific functions. Using population genomics data from D. melanogaster and related species, we show that pleiotropic immune genes do undergo slightly slower evolutionary rates than those having no known developmental functions, and that signatures of purifying selection are significantly stronger for broadly-expressed pleiotropic immune genes. This study underscores the need to investigate immune system evolution in the broader context of host life history and development, and raises new questions about the evolution and maintenance of pleiotropic genetic architecture.