Hybridization Reveals the Evolving Genomic Architecture of Speciation

• Speciation with gene flow in Heliconius generates genomic heterogeneity in divergence
• Initial divergence is highly restricted, largely clustered on wing-patterning genes
• Divergence evolves rapidly due to newly differentiated regions of the genome
• Process influenced by divergent and purifying selection as well as introgression

SummaryThe rate at which genomes diverge during speciation is unknown, as are the physical dynamics of the process. Here, we compare full genome sequences of 32 butterflies, representing five species from a hybridizing Heliconius butterfly community, to examine genome-wide patterns of introgression and infer how divergence evolves during the speciation process. Our analyses reveal that initial divergence is restricted to a small fraction of the genome, largely clustered around known wing-patterning genes. Over time, divergence evolves rapidly, due primarily to the origin of new divergent regions. Furthermore, divergent genomic regions display signatures of both selection and adaptive introgression, demonstrating the link between microevolutionary processes acting within species and the origin of species across macroevolutionary timescales. Our results provide a uniquely comprehensive portrait of the evolving species boundary due to the role that hybridization plays in reducing the background accumulation of divergence at neutral sites.

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