Contrasting signatures of genomic divergence during sympatric speciation

Andreas F. Kautt, Claudius F. Kratochwil, Alexander Nater, Gonzalo Machado-Schiaffino, Melisa Olave, Frederico Henning, Julián Torres-Dowdall, Andreas Härer, C. Darrin Hulsey, Paolo Franchini, Martin Pippel, Eugene W. Myers and Axel Meyer ()
Additional contact information
Andreas F. Kautt: University of Konstanz
Claudius F. Kratochwil: University of Konstanz
Alexander Nater: University of Konstanz
Gonzalo Machado-Schiaffino: University of Konstanz
Melisa Olave: University of Konstanz
Frederico Henning: University of Konstanz
Julián Torres-Dowdall: University of Konstanz
Andreas Härer: University of Konstanz
C. Darrin Hulsey: University of Konstanz
Paolo Franchini: University of Konstanz
Martin Pippel: Max Planck Institute of Molecular Cell Biology and Genetics
Eugene W. Myers: Max Planck Institute of Molecular Cell Biology and Genetics
Axel Meyer: University of Konstanz

Nature, 2020, vol. 588, issue 7836, 106-111

Abstract: Abstract 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 Darwin1,2. 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 process3. Theory predicts that the genetic architecture of divergently selected traits can influence whether sympatric speciation occurs4, 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 histories5. Here, within a young species complex of neotropical cichlid fishes (Amphilophus spp.), we analysed genomic divergence among populations and species. 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. Species that differ in monogenic or oligogenic traits that affect ecological performance and/or mate choice show remarkably localized genomic differentiation. 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. 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.

Date: 2020
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DOI: 10.1038/s41586-020-2845-0

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