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Adaptive phenotypes often arise by rewiring existing developmental networks. Co-option of transcription factors in novel contexts has facilitated the evolution of ecologically important adaptations.  doublesex  ( dsx ) governs fundamental sex differentiation during embryonic stages and has been co-opted to regulate diverse secondary sexual dimorphisms during pupal development of holometabolous insects. In  Papilio polytes ,  dsx  regulates female-limited mimetic polymorphism, resulting in mimetic and non-mimetic forms. To understand how a critical gene such as  dsx  regulates novel wing patterns while maintaining its basic function in sex differentiation, we traced its expression through metamorphosis in  P. polytes  using developmental transcriptome data. We found three key  dsx  expression peaks: (i) eggs in pre- and post-ovisposition stages; (ii) developing wing discs and body in final larval instar; and (iii) 3-day pupae. We identified potential  dsx  targets using co-expression and differential expression analysis, and found distinct, non-overlapping sets of genes—containing putative  dsx- binding sites—in developing wings versus abdominal tissue and in mimetic versus non-mimetic individuals. This suggests that  dsx  regulates distinct downstream targets in different tissues and wing colour morphs and has perhaps acquired new, previously unknown targets, for regulating mimetic polymorphism. Additionally, we observed that the three female isoforms of  dsx  were differentially expressed across stages (from eggs to adults) and tissues and differed in their protein structure. This may promote differential protein–protein interactions for each isoform and facilitate sub-functionalization of  dsx  activity across its isoforms. Our findings suggest that  dsx  employs tissue-specific downstream effectors and partitions its functions across multiple isoforms to regulate primary and secondary sexual dimorphism through insect development.

royal society open science

Tissue-specific developmental regulation and isoform usage underlie the role of<i>doublesex</i>in sex differentiation and mimicry in<i>Papilio</i>swallowtails

Tissue-specific developmental regulation and isoform usage underlie the role ofdoublesexin sex differentiation and mimicry inPapilioswallowtails