Transcriptome profiling in the damselfly Ischnura elegans identifies genes with sex-biased expression

Sexual dimorphism occurs widely across the animal kingdom and has profound effects on evolutionary trajectories. Here, we investigate sex-specific gene expression in Ischnura elegans (Odonata: dragonflies and damselflies), a species with pronounced sexual differences including a female-limited colour polymorphism with two female-like gynochrome morphs and one male-mimicking, androchrome morph. Whole-organism transcriptome profiling and sex-biased gene expression analysis was conducted on adults of both sexes (pooling all females as well as separating the three morphs) to gain insights into genes and pathways potentially associated with sexual development and sexual conflict.

The de novo transcriptome assembly was of high quality and completeness (54 k transcripts; 99.6% CEGMA score; 55% annotated). We identified transcripts of several relevant pathways, including transcripts involved in sex determination, hormone biosynthesis, pigmentation and innate immune signalling. A total of 1,683 genes were differentially expressed (DE) between males and all females (1,173 were female-biased; 510 male-biased). The DE genes were associated with sex-specific physiological and reproductive processes, olfaction, pigmentation (ommochrome and melanin), hormone (ecdysone) biosynthesis and innate immunity signalling pathways. Comparisons between males and each female morph category showed that the gynochromes differed more from males than the androchrome morph.

This is the first study to characterize sex-biased gene expression in odonates, one of the most ancient extant insect orders. Comparison between I. elegans sexes revealed expression differences in several genes related to sexual differences in behaviour and development as well as morphology. The differential expression of several olfactory genes suggests interesting sexual components in the detection of odours, pheromones and environmental volatiles. Up-regulation of pigmentation pathways in females indicates a prominent role of ommochrome pigments in the formation of the genetically controlled female colour polymorphism. Finally, the female-biased expression of several immunity genes suggests a stronger immune response in females, possibly related to the high levels of male mating harassment and recurrent matings in this species, both of which have been shown to injure females and expose them to sexually transmitted diseases and toxins contained in seminal fluids.