The role of gene expression in the recent evolution of resistance in a model host parasite system

Abstract

Damage by parasites is a perpetual challenge for hosts, often leading to the evolution of elaborate mechanisms of avoidance, immunity, or tolerance. Host resistance can evolve via changes in immune protein coding and/or expression. Heritable population differences in gene expression following infection can reveal mechanisms of immune evolution. We compared gene expression in infected and uninfected threespine stickleback (Gasterosteus aculeatus) from two natural populations that differ in their resistance to a native cestode parasite, Schistocephalus solidus. Genes in both the innate and adaptive immune system were differentially expressed as a function of host population, infection status, and their interaction. These genes were enriched for loci controlling immune functions that we independently verified differ between host populations, or in response to infection. For instance, populations differ strongly in reactive oxygen (ROS) production, and we observed corresponding differences in expression of ROS-affecting loci. Differentially expressed genes also were involved in fibroblast activation, B-cell activation, and leukocyte trafficking. Coexpression network analysis identified two distinct immune processes contributing to stickleback resistance; several modules of genes are correlated with parasite survival while a different set of modules are correlated with suppression of cestode growth. Comparison of networks between populations showed resistant fish have a dynamic expression profile while susceptible fish are static. In summary, recent evolutionary divergence between two vertebrate populations has generated population-specific gene expression responses to parasite infection, which reveal a few immune modules likely to separately affect cestode establishment, and growth.