Evolution of novel mimicry polymorphisms through Haldane’s sieve and rare recombination

Origins of phenotypic novelty represent a paradox. Maintenance of distinct, canalized morphs usually requires a complex array of polymorphisms, whose co-retention requires a genetic architecture resistant to recombination, involving inversions and master regulators. Here, we reveal how such a constraining architecture can still accommodate novel morphs in evolving polymorphisms using the classic polymorphic Batesian mimicry inPapilio polytes, whose supergene-like genetic architecture is maintained in a large inversion. We show that rapidly evolving alleles of the conserved gene,doublesex, within this inversion underlie the genetic basis of this polymorphism. Using precisely dated phylogeny and breeding experiments, we show that novel adaptive mimetic morphs and underlying alleles evolved in a sequentially dominant manner, undergoing selective sweeps in the mimetic species as predicted under Haldane’s sieve. Furthermore, we discovered that mimetic forms share precise inversion breakpoints, allowing rare exon swaps between the universally dominant and a recessive allele to produce a novel, persistent intermediate phenotype, ultimately facilitating the acquisition of phenotypic novelty. Thus, genetic dominance, selective sweeps, rapid molecular divergence, and rare recombination promote novel forms in this iconic evolving polymorphism, resolving the paradox of phenotypic novelty arising even in highly constrained genetic architectures.