Gene expression changes during female reproductive development in a colour polymorphic insect

Pleiotropy (multiple phenotypic effects of single genes) and epistasis (gene interaction) play key roles in the development of complex phenotypes and might be especially important in polymorphic taxa. The development of discrete and heritable sympatric phenotypic polymorphisms often emerges from major-effect genes that interact with other loci and have pleiotropic effects on multiple traits and physiological functions. We quantified gene expression changes during ontogenetic colour development in an insect (damselfly: Ischnura elegans ) with three heritable female colour morphs, one which is a male mimic. Using transcriptome sequencing and de novo assembly, we demonstrate that all morphs show extensive downregulation of gene expression during early colour development. Morphs then become increasingly differentiated during sexual maturation and when developing adult colouration. These different ontogenetic trajectories arise because of the heterochronic development of the male-mimicking females, compared to other two female morphs. Many loci with regulatory functions in reproductive development are uniquely regulated in male-mimicking females, including upstream and downstream regulators of ecdysone signalling and transcription factors that influence insect sexual differentiation. Our study reveals extensive epistasis in the genomic architecture of I. elegans and suggest a central role for pleiotropy in shaping the developmental trajectories of the different morphs.