Classic multi-locus cline theory 16 and genomic simulations 17, 18 support the hypothesis that the synergistic effects of many weakly selected alleles can promote a rapid buildup of pronounced genomic differentiation 5, 13. Apart from the proposed pivotal role of major effect loci for speciation, theoretical work has also suggested that many small-effect loci can jointly constitute effective genome-wide barriers to gene flow 15. The discovery of such ‘barrier loci’, which resist the homogenizing effects of gene flow, fits theoretical expectations 4, 6, 7, 8. Genomic studies on the early stages of speciation with gene flow 10 have found that differentiation between incipient species is commonly restricted to a few genomic regions 2, 11, 12, 13, 14. In addition, with fewer loci, recombination is less likely to break up co-adapted alleles 4, 9. Moreover, if divergently selected traits are based on few instead of many loci, speciation with gene flow is generally thought to occur more readily, assuming that per-locus effects are larger and that selection acting on these loci will be stronger. Theoretical models predict that speciation with gene flow is strongly facilitated if traits under divergent selection also contribute to assortative mating 4, 6, 7, 8.
Sympatric speciation is the most extreme form of speciation with gene flow. Recently, the recognition that speciation can also occur in the absence of geographic barriers (under sympatric conditions) has increased, although only a few empirical examples are widely accepted 1. Speciation has long been assumed to require geographic barriers that limit the homogenizing effects of gene flow (allopatric speciation but see ref. Thus, we conclude that simple trait architectures are not always as conducive to speciation with gene flow as previously suggested, whereas polygenic architectures can promote rapid and stable speciation in sympatry. By contrast, differentiation among species that have diverged in polygenic traits is genomically widespread and much higher overall, consistent with the evolution of effective and stable genome-wide barriers to gene flow. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. By generating a new genome assembly and re-sequencing 453 genomes, we uncovered the genetic architecture of traits that have been suggested to be important for divergence. Here, within a young species complex of neotropical cichlid fishes ( Amphilophus spp.), we analysed genomic divergence among populations and species. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs 4, but empirical tests of this theory are scant because comprehensive data are difficult to collect and synthesize across species, owing to their unique biologies and evolutionary histories 5. Gene flow counteracts the buildup of genome-wide differentiation, which is a hallmark of speciation and increases the likelihood of the evolution of irreversible reproductive barriers (incompatibilities) that complete the speciation process 3. The transition from ‘well-marked varieties’ of a single species into ‘well-defined species’-especially in the absence of geographic barriers to gene flow (sympatric speciation)-has puzzled evolutionary biologists ever since Darwin 1, 2.