The transition from “well-marked varieties” into “well-defined species” has puzzled evolutionary biologists ever since Darwin — especially when extensive gene flow between incipient species is possible due to the lack of physical barriers (sympatric speciation). Gene flow counteracts the build-up of genome-wide differentiation, which is both a hallmark of speciation and forms the underlying basis 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. However, empirical data to test this prediction remain rare and are often difficult to synthesize across animal taxa due to idiosyncrasies in their biology and evolutionary histories. Here, within a young species complex of Neotropical cichlid fish (Amphilophus spp.), we analyzed genomic divergence among populations and species, and the genetic architecture of traits that have been suggested to be important for this 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 between 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.

This work is based on a new, high-quality reference genome of Amphilophus citrinellus and 453 re-sequenced genomes that were sampled between 2003 and 2015. Sample sizes for the resequenced genomes (in []) are GL Nicaragua A. citrinellus [24], GL Nicaragua A. labiatus [24], GL Managua A. citrinellus [25], GL Managua A. labiatus [25], CL Apoyeque A. cf. citrinellus [40], CL Apoyo A. astorquii [23], CL Apoyo A. chancho [16], CL Apoyo A. flaveolus [16], CL Apoyo A. globosus [25], CL Apoyo A. supercilius [10], CL Apoyo A. zaliosus [21], CL Apoyo admixed individuals [9], CL As. León A. cf. citrinellus [20], CL As. Managua A. tolteca [20], CL Xiloá A. amarillo [21], CL Xiloá A. sagittae [27], CL Xiloá A. viridis [24], CL Xiloá A. xiloaensis [16], CL Xiloá admixed individuals [14], CL Masaya A. cf. citrinellus [40], CL Tiscapa A. cf. citrinellus [20]. Fish were caught with gill nets or by harpooning in crater lakes Asososca León, Asososca Managua, Apoyeque, Apoyo, Masaya Tiscapa, and Xiloá. Fish or tissue samples from the great lakes Nicaragua and Managua were obtained  from local fishermen, mostly the big fish market in Granada (Lake Nicaragua fish) and Mateares (Lake Managua fish). Adult fish were collected in field expeditions of the Meyer lab to Nicaragua between 2003 and 2015. Photographs were taken in the field. Next-generation sequencing data generation was performed at the University of Konstanz, the Max Planck Institute of Molecular Cell Biology and Genetics in Dresden, and BGI Hongkong.