Reduced parallel gene expression evolution with increasing genetic divergence – a hallmark of polygenic adaptation

Parallel evolution, the repeated evolution of similar traits in independent lineages, is a topic of considerable interest in evolutionary biology. While previous studies have focused on the parallelism of phenotypic traits and their underlying genetic basis, the extent of parallelism at the level of gene expression across different levels of genetic divergence remains largely unexplored. This study investigates the evolution of gene expression in replicate Drosophila populations exposed to the same novel environment at three divergence levels: within a population, between populations, and between species. We show that adaptive gene expression changes are more heterogeneous with increasing genetic divergence between the compared groups. This finding suggests that the adaptive architecture, which encompasses factors such as allele frequencies and the effect size of contributing loci, becomes more distinct with increasing divergence, leading to less parallel gene expression evolution. This result implies that redundancy is a crucial factor in both genetic selection responses and gene expression evolution. Hence, our findings are consistent with the omnigenic model, which posits that selection acts on higher-order phenotypes. This work contributes to our understanding of phenotypic evolution and the complex interplay between genomic and molecular responses.