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 in Papilio 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.