Contrasting signatures of genomic divergence during sympatric speciation

The transition from “well-marked varieties” into “well-defined species” — especially in the absence of geographic barriers to gene flow (sympatric speciation) — has puzzled evolutionary biologists ever since Darwin — especially in the absence of geographic barriers to gene flow (sympatric speciation). Gene flow counteracts the buildup of genome-wide differentiation, which is both a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that ultimately complete the speciation process. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs, but empirical tests are scant because comprehensive data are difficult to collect and synthesize across taxa due to idiosyncrasies in their biology and evolutionary histories. Here, within an extremely young species complex of Neotropical cichlid fishes (Amphilophus spp.), we analyzed genomic divergence among populations and species and the genetic architecture of traits that have been suggested to be important for divergence by generating a new genome assembly and re-sequencing 453 genomes. We found that species differing in mono/oligogenic traits affecting ecological performance and/or mate choice show remarkably localized genomic differentiation. In contrast, differentiation among species that diverged in polygenic traits is widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Thus, we conclude that simple trait architectures are not always as conducive to speciation-with-gene-flow as previously suggested, whereas, unexpectedly, polygenic architectures can promote rapid and stable speciation in sympatry.