Identification of sex chromosome, sex-biased gene expression and dosage compensation in the pygmy mole cricket Xya riparia (Orthoptera: Tridactyloidea)

Sex-biased gene expression and sex chromosome dosage compensation are crucial for the growth and development of sexually reproducing organisms. Sex-biased genes are regarded as pivotal drivers of sexual dimorphism in regard to phenotypic traits. In species that possess an XX/XO sex determination system, males are characterized by the absence of a homologous Y chromosome and the possession of a hemizygous X chromosome. It is noteworthy that X-linked genes in males are present as a single copy, while females possess two copies of these genes. This imbalance in gene copy number can lead to gene expression disparities that may be disadvantageous. Consequently, a dosage compensation mechanism evolves with the objective of equalizing the expression levels of X-linked genes between sexes. Xya riparia, a species of cricket with an XX/XO sex determination system, provides a valuable opportunity to study the expression dynamics of sex-biased genes and the mechanism of dosage compensation in Orthoptera. In this study, we employed Illumina sequencing data to identify the X chromosome of X. riparia, thereby demonstrating that the second of its six chromosomes is indeed the X chromosome. We further performed orthologous comparisons with Locusta migratoria to investigate the “faster-X effect” in X. riparia, and the distribution of sex-biased genes across the genome. We revealed a significant chromosomal bias, with male-biased genes predominantly located on the autosomes whereas female-biased genes were enriched on the X-chromosome. Furthermore, the sex-biased genes exhibited relatively higher Ka/Ks ratios than unbiased genes, suggesting a potential faster evolutionary rate. The ratio of female to male expression on the X chromosome indicates that the X chromosome of X. riparia exhibits incomplete dosage compensation (where XX: AA in female is 0.9342–0.9619 and X: AA in male is 0.6884–0.7201). Our findings provide evidence that the X chromosome of X. riparia is “feminized”, with the majority of X-linked genes showing higher expression in females than males. We further show that the dosage compensation is incomplete in X. riparia, as X-linked genes in males exhibit lower expression than in females but remain above one-half of the female expression level. In conclusion, this study establishes X. riparia as a valuable model for investigating the dynamics of sex chromosomes and sex-biased genes in Orthopteran insects.