Natural Variation Reveals Functional and Genetic Integration of a Polyphenism

Integration and modularity can have a profound impact on the function and evolution of environmentally responsive traits, especially when they result in discrete, alternative forms-that is, developmental polyphenism. An unresolved issue for understanding this impact is the degree to which the genetic architectures of the individual components of a plastic trait permit independent versus coordinated evolution. The association of trait variation with genomic variation can provide a test of whether the same loci influence different components of the same integrated phenotype. An example of a coordinated, plastic trait is in the shark-tooth nematode Pristionchus pacificus, which develops into either a bacterial-feeding or a predatory adult morph, depending on its perception of local food availability. Moreover, this polyphenism, when measured as morph induction in response to a common set of cues, differs across natural isolates of the species. By creating recombinant inbred lines (RILs) from natural isolates that have diverged in their morph-induction bias, followed by quantitative trait locus analysis, we tested whether and the extent to which component traits of this resource polyphenism are linked. We found that RILs with more frequent induction of the predatory morph also produced Eu individuals that were more effective predators. We also found that these two traits are associated with the same major-effect locus, suggesting that their causal genes are physically linked, if not the same, and are therefore likely to experience coordinated selection. In contrast, we found that morphological variation was not linked to these two traits and that such variation within each morph was even independent of variation in the other. Our findings show that the same coordinated plastic trait exhibits a blend of genetic correlation and independence, whose balance shapes the trait's evolutionary potential.