Evolutionary Dynamics of Dosage Compensation and Sex-biased Gene Expression in Morabine Grasshopper Vandiemenella...

Sex chromosome evolution and gene regulation are closely linked but remain understudied in many taxa. Young neo-sex chromosomes offer unique insights into these processes. We examine dosage compensation and sex-biased gene expression in Vandiemenella viatica grasshoppers by comparing the ancestral X chromosome in the P24X0 race with derived neo-sex chromosomes in the P24XY race. The P24XY neo-XY arose via X-autosome fusion: the XL arm represents the ancestral X and the XR arm a former autosome (chromosome 1 in P24X0) now part of the neo-X and homologous to the neo-Y. We first assess dosage compensation via male and female gene expression. In somatic tissues, male P24X0 X-linked and P24XY XL-linked genes are upregulated to match both female expression and autosomal levels, indicating near-complete dosage compensation. In testes, expression of X-linked and the XL-linked genes is reduced nearly 4-fold reflecting absent dosage compensation and the presence of meiotic X chromosome inactivation. We then analyze sex-biased gene expression across tissues and chromosomes. Gonads show stronger sex-biased gene expression than somatic tissues. Female-biased genes are concentrated on the P24X0 X and P24XY XL, whereas male-biased genes are enriched on autosomes and the XR arm of the neo-X. Overall, the ancestral X in P24X0 and the XL arm of the P24XY neo-X are hypertranscribed, while the XR arm retains autosomal expression, male-biased enrichment, and lacks dosage compensation. These patterns show that dosage compensation is regulated at levels of chromosome arms and illustrate how chromosome structure, gene regulation, and reproduction interact, shedding light on sex chromosome evolution in V. viatica.