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

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 (Coregonus clupeaformis)
and its sister lineage, the European Whitefish (Coregonus lavaretus), 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.