Polygenic selection drives the evolution of convergent transcriptomic landscapes across continents within a Nearctic sister species complex

Abstract

In contrast to the plethora of studies focusing on the genomic basis of adaptive phenotypic divergence, the role of gene expression during speciation has been much less investigated and consequently less understood. Yet, the convergence of differential gene expression patterns between closely related species‐pairs might reflect the role of natural selection during the process of ecological speciation. Here, we test for intercontinental convergence in differential transcriptional signatures between limnetic and benthic sympatric species‐pairs of Lake Whitefish (<i>Coregonus clupeaformis</i>) and its sister lineage, the European Whitefish (<i>Coregonus lavaretus</i>), using six replicated sympatric species‐pairs (two in North America, two in Norway and two in Switzerland). We characterized both sequence variation in transcribed regions and differential gene expression between sympatric limnetic and benthic species across regions and continents. Our first finding was that differentially expressed genes (DEG) between limnetic and benthic whitefish tend to be enriched in shared polymorphism among sister lineages. We then used both genotypes and covariation in expression in order to infer polygenic selection at the gene level. We identified parallel outliers and DEG involving genes primarily overexpressed in limnetic species relative to the benthic species. Our analysis finally revealed the existence of shared genomic bases underlying parallel differential expression across replicated species‐pairs from both continents, such as a cis‐eQTL affecting the pyruvate kinase expression level involved in glycolysis. Our results are consistent with a long‐standing role of natural selection in maintaining trans‐continental diversity at phenotypic traits involved in ecological speciation between limnetic and benthic whitefishes.