A test of the Baldwin Effect: Differences in both constitutive expression and inducible responses to parasites underlie variation in host response to a parasite

ABSTRACT

Despite the significant effect of host-parasite interactions on both ecological systems and organism health, there is still limited understanding of the mechanisms driving evolution of host resistance to parasites. One model of rapid evolution, the Baldwin Effect, describes the role of plasticity in adaptation to novel conditions, and subsequent canalization of associated traits. While mostly applied in the context of environmental conditions, this theory may be relevant to the evolution of host resistance to novel parasites. Here we test the applicability of the Baldwin Effect to the evolution of resistance in a natural system using threespine stickleback fish (Gasterosteus aculeatus) and their cestode parasite Schistochephalus solidus. We leverage a large transcriptomic data set to describe the response to S. solidus infection by three different genetic crosses of stickleback, from a resistant and a tolerant population. Hosts mount a multigenic response to the parasite that is similar among host genotypes. In addition, we document extensive constitutive variation in gene expression among host genotypes. However, although many genes are both infection-induced and differentially expressed between genotypes, this overlap is not more extensive than expected by chance. We also see little evidence of canalization of infection-induced gene expression in the derived resistant population. These patterns do not support the Baldwin Effect, though they illustrate the importance of variation in both constitutive expression and induced responses to parasites. Finally, our results improve understanding of the cellular mechanisms underlying a putative resistance phenotype (fibrosis). Combined, our results highlight the importance of both constitutive and inducible variation in the evolution of resistance to parasites, and identify new target genes contributing to fibrosis. These findings advance understanding of host-parasite interactions and co-evolutionary relationships in natural systems.