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

Abstract

BackgroundSexual 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.ResultsThe 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.ConclusionsThis 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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3334-6) contains supplementary material, which is available to authorized users.

Signatures of local adaptation along environmental gradients in a range‐expanding damselfly (Ischnura elegans)

“…Second, (ii) generalized dissimilarity modelling (GDM) is applied to these identified candidate SNPs, to determine relationships of SNP allelic turnover magnitude in relation to environmental gradients and geographic distance (Fitzpatrick & Keller, ). Finally, (iii) signatures of local adaptation are identified via SNP mapping to an annotated I. elegans transcriptome (Chauhan, Wellenreuther, & Hansson, ; Chauhan et al., ), and interpretations about adaptive variation are then based on gene function, experimental gene expression data (e.g., Lancaster et al., ), SNP x environment associations and the pattern of allelic turnover observed (Figure ). Our analysis provides fine‐scale characterization of SNP‐specific genetic gradients of genomewide selection signatures.…”

“…To identify functional genes, RAD tags containing one or more of the 1,758 candidate SNPs were mapped against the annotated transcriptome for I. elegans (Chauhan et al., , ) using blastn with an e ‐value cut‐off of 1 × 10 −5 . All blastn results were imported into the blast2go Web version for further annotation (Conesa et al., ).…”

“…Gene functions were identified from those previously annotated in Chauhan et al. (, ), those with expression levels associated with thermal challenge treatments in I. elegans performed by Lancaster et al. (), or were identified directly from the NCBI database (Table ).…”

“…To examine how adaptive variation changes in I. elegans along its current Swedish distribution, we mapped allelic turnover functions for selected candidate SNPs that (i) were annotated to genes associated with thermal tolerance or other phenotypic traits previously identified (e.g., Chauhan et al., , ; Lancaster et al., ) and (ii) had a higher explanatory power in the GDM than the reference “random” SNP group. In addition to the above, we focused on SNPs that (iii) had the highest allelic turnover in relation to Max Temp in the GDM or (iv) showed a large change in F ST along the sampled gradient (Figure ).…”

Molecular Mechanisms Underlying Color Vision and Color Formation in Dragonflies

“…Recent progress on molecular mechanisms of color vision and color formation unveiled the outstanding diversity of visual opsin genes and the unique mechanisms of body color changes in dragonflies. Meanwhile, only limited information is available on genes potentially involved in color formation (Chauhan et al 2014(Chauhan et al , 2016. Rapid spread of next-generation sequencing technology makes it easier than ever to analyze non-model organisms, although careful evaluation for de novo assembly is still important as described above, especially without genomic information.…”