Abstract
The African Mocker Swallowtail, Papilio dardanus, is a textbook example in evolutionary genetics. Classical breeding experiments have shown that wing pattern variation in this polymorphic Batesian mimic is determined by the polyallelic H locus that controls a set of distinct mimetic phenotypes. Using bacterial artificial chromosome (BAC) sequencing, recombination analyses and comparative genomics, we show that H co-segregates with an interval of less than 500 kb that is collinear with two other Lepidoptera genomes and contains 24 genes, including the transcription factor genes engrailed (en) and invected (inv). H is located in a region of conserved gene order, which argues against any role for genomic translocations in the evolution of a hypothesized multi-gene mimicry locus. Natural populations of P. dardanus show significant associations of specific morphs with single nucleotide polymorphisms (SNPs), centred on en. In addition, SNP variation in the H region reveals evidence of non-neutral molecular evolution in the en gene alone. We find evidence for a duplication potentially driving physical constraints on recombination in the lamborni morph. Absence of perfect linkage disequilibrium between different genes in the other morphs suggests that H is limited to nucleotide positions in the regulatory and coding regions of en. Our results therefore support the hypothesis that a single gene underlies wing pattern variation in P. dardanus.
Highlights
Batesian mimics are palatable species that avoid predation by evolving resemblance to toxic or harmful models [1]
Because these species were only distantly related to P. dardanus, tests of molecular rates may be affected by multiple hits at variable sites, which was corrected by applying a Jukes – Cantor model of sequence variation [36]
We found all of these genes, except for carotenoid-binding protein (CBP), to be present in a transcriptome library prepared from normalized cDNA of last larval instar and pre-pupal wing discs, in addition to inv and en transcripts
Summary
Batesian mimics are palatable species that avoid predation by evolving resemblance to toxic or harmful models [1]. As Batesian mimics increase in frequency in the local prey community, predators may begin to associate the phenotype with palatability and the benefit of mimicry becomes reduced [3]. This leads to negative frequency-dependent selection on mimetic phenotypes, which may favour the evolution of multiple morphs in a population that mimic different models [4].
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