Pleiotropy increases parallel selection signatures during adaptation from standing genetic variation

Abstract

The phenomenon of parallel evolution, whereby similar genomic and phenotypic changes occur across replicated pairs of population or species, is widely studied. Nevertheless, the determining factors of parallel evolution remain poorly understood. Theoretical studies have proposed that pleiotropy, the influence of a single gene on multiple traits, is an important factor. In order to gain a deeper insight into the role of pleiotropy for parallel evolution from standing genetic variation, we characterized the interplay between parallelism, polymorphism and pleiotropy. The present study examined the parallel gene expression evolution in 10 replicated populations of Drosophila simulans, which were adapted from standing variation to the same new temperature regime. The data demonstrate that parallel evolution of gene expression from standing genetic variation is positively correlated with the strength of pleiotropic effects. The ancestral variation in gene expression is, however, negatively correlated with parallelism. Given that pleiotropy is also negatively correlated with gene expression variation, we conducted a causal analysis to distinguish cause and correlation and evaluate the role of pleiotropy. The causal analysis indicated that both direct (causative) and indirect (correlational) effects of pleiotropy contribute to parallel evolution. The indirect effect is mediated by historic selective constraint in response to pleiotropy. This results in parallel selection responses due to the reduced standing variation of pleiotropic genes. The direct effect of pleiotropy is likely to reflect a genetic correlation among adaptive traits, which in turn gives rise to synergistic effects and higher parallelism.