Abstract
Supergene mimicry is a striking phenomenon but we know little about the evolution of this trait in any species. Here, by studying genomes of butterflies from a recent radiation in which supergene mimicry has been isolated to the gene doublesex, we show that sexually dimorphic mimicry and female-limited polymorphism are evolutionarily related as a result of ancient balancing selection combined with independent origins of similar morphs in different lineages and secondary loss of polymorphism in other lineages. Evolutionary loss of polymorphism appears to have resulted from an interaction between natural selection and genetic drift. Furthermore, molecular evolution of the supergene is dominated not by adaptive protein evolution or balancing selection, but by extensive hitchhiking of linked variants on the mimetic dsx haplotype that occurred at the origin of mimicry. Our results suggest that chance events have played important and possibly opposing roles throughout the history of this classic example of adaptation.
Highlights
Supergene mimicry is a striking phenomenon but we know little about the evolution of this trait in any species
Alfred Russel Wallace, most famous for his co-discovery with Charles Darwin of evolution by natural selection[1], made many other fundamental insights, one of which was his discovery of female-limited mimetic polymorphism in butterflies[2], a phenomenon he described in Papilio polytes
The mimicry supergene in Papilio polytes was recently characterized at a molecular genetic level and shown to be controlled by a single gene, doublesex, but with this single gene contained in an inversion polymorphism[14,15]
Summary
Supergene mimicry is a striking phenomenon but we know little about the evolution of this trait in any species. By studying genomes of butterflies from a recent radiation in which supergene mimicry has been isolated to the gene doublesex, we show that sexually dimorphic mimicry and female-limited polymorphism are evolutionarily related as a result of ancient balancing selection combined with independent origins of similar morphs in different lineages and secondary loss of polymorphism in other lineages. The mimicry supergene in Papilio polytes was recently characterized at a molecular genetic level and shown to be controlled by a single gene, doublesex (dsx), but with this single gene contained in an inversion polymorphism[14,15] This discovery opens the door to addressing long-standing questions about the evolution of supergenes and mimicry more generally[16,17,18]. Our results suggest important roles for both selection and drift in shaping genetic and phenotypic variation across this historically significant clade of mimetic butterflies
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