Genome-wide signatures of synergistic epistasis during parallel adaptation in a Baltic Sea copepod

The role of epistasis in adaptive evolution has remained an unresolved
problem dating back to the Evolutionary Synthesis. This role is now being
revisited due to its relevance for polygenic adaptation. In the absence of
epistasis, polygenic adaptation is predicted to result in non-parallel
evolution, because repeated selection could act on subsets of effectively
redundant alleles. However, positive epistatic interactions among adaptive
alleles would make the alleles non-redundant and selection for particular
allelic combinations could drive parallel evolution. The inability to
address this fundamental question might arise from traditional approaches
lacking the power to capture the genomic architecture and dynamics of
polygenic adaptation. To address this problem, we employed a replicated
and controlled evolution experiment using the copepod Eurytemora
affinis to elucidate the evolutionary response architecture to
rapid salinity decline, a predicted consequence of global climate change
in higher latitudes. Based on time-resolved pooled whole-genome
sequencing, we uncovered a remarkably parallel response, despite polygenic
adaptation involving over 1000 loci across ten replicate selection lines.
Interestingly, single-nucleotide polymorphism (SNP) frequencies converged
during the experiment, far beyond expectations, resulting in replicate
lines sharing 93.1% of selected alleles. Using simulations, we found that
this polygenic parallelism was consistent with synergistic epistasis among
alleles responding in concert across replicate lines, a phenomenon that
may be common for selection on complex physiological traits. Furthermore,
we found that the same SNPs with signatures of selection in the laboratory
also exhibited signatures of selection across a natural salinity gradient
in the Baltic Sea. Our study provides the first experimental evidence that
polygenic adaptation can actually be highly repeatable at the genomic
level, given the presence of synergistic epistasis among the loci under
selection.