Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species.Hereweuse genomic tools to investigate introgression inHeliconius, a rapidly radiating genus of neotropical butterflieswidely used in studies of ecology, behaviour,mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation. The butterfly genus Heliconius (Nymphalidae: Heliconiinae) is associated with a suite of derived life-history and ecological traits, including pollen feeding, extended lifespan, augmented ultraviolet colour vision, ‘trap-lining’ foraging behaviour, gregarious roosting and complexmating behaviours, andprovides outstanding opportunities for genomic studies of adaptive radiation and speciation. Thegenus is best known for the hundreds of races with different colour patterns seen among its 43 species, with repeated examples of both convergent evolution among distantly related species and divergent evolution between closely related taxa. Geographic mosaics of multiple colour-pattern races, such as in Heliconius melpomene (Fig. 1), converge to similar mosaics in other species, and this led to the hypothesis of mimicry. Heliconius are unpalatable to vertebrate predators and Müllerian mimicry of warning colour patterns enables species to share the cost of educating predators. As a result of its dual role inmimicry andmate selection, divergence in wing pattern is also associated with speciation and adaptive radiation. A particularly recent radiation is the melpomene–silvaniform clade, in which mimetic patterns often seem to be polyphyletic (Fig. 1a). Most species in this clade occasionally hybridize in the wild with other clade members. Gene genealogies at