Pleiotropy is associated with the parallel gene expression evolution during adaptation to a novel environment
Authors: Wei-Yun Lai 1,2; Sheng-Kai Hsu 1,2; Andreas Futschik 3; Christian Schlötterer 1
Affiliations: 1) Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.; 2) Vienna Graduate School of Population Genetics, Vienna, Austria.; 3) Department of Applied Statistics, Johannes Kepler University Linz, Linz, Austria.
Keywords: Molecular Evolution
Repeatable genomic/phenotypic changes across replicated population pairs provide evolutionary biologists with strong evidence for adaptive evolution. Nevertheless, adaptation to a similar environment often yields inconsistent outcomes, particularly at the genic level. The evolutionary response can range from a subset of adaptive genes evolving in a highly repeatable manner to highly heterogeneous evolutionary responses in replicate experiments. Understanding the potential factors affecting the extent of parallelism in gene evolution is an important research question as this provides an important step towards the prediction of evolution. The degree of pleiotropy has been proposed as a potential factor affecting the degree of evolutionary parallelism/repeatability of a gene. Although several theoretical predictions have been made, their empirical validation is still limited. To fill this gap, we studied the evolution of gene expression in 10 replicated Drosophila simulans populations adapting to the same new temperature regime. Comparing the parallelism of expression evolution among putatively selected genes, we observed a positive relationship between the degree of evolutionary parallelism and the pleiotropic effects. In addition, the degree of evolutionary parallelism was negatively associated with the magnitude of natural variation in the expression of the genes. Because gene expression variation was also associated with the extent of the pleiotropic effect, we performed causal analysis to disentangle the causal influence of natural variation and pleiotropic effects on parallel evolution. Our analyses identified pleiotropy as the causal factor for the parallel evolution of gene expression and levels of natural variation. We conclude that pleiotropy is a key factor determining evolutionary predictability.