The scorpionfly (Panorpa cognata) genome highlights conserved and derived features of the peculiar dipteran X chromosome

Many insects carry an ancient X chromosome—the Drosophila Muller element F—that likely predates their origin. Interestingly, the X has undergone turnover in multiple fly species (Diptera) after being conserved for more than 450 My. The long evolutionary distance between Diptera and other sequenced insect clades makes it difficult to infer what could have contributed to this sudden increase in rate of turnover. Here, we produce the first genome and transcriptome of scorpionflies (genus Panorpa), an insect belonging to a long overlooked sister-order to Diptera: Mecoptera. Combining our genome assembly with genomic short-read data, we obtain genome coverage and identify X-linked super-scaffolds. We further perform a gene homology analysis between the Panorpa X and a closely related Diptera species, and we assess the conservation of the Panorpa X-linked gene content with that of more distantly related insect species. We explored the structure of the Panorpa X by determining its repeat content, GC content, and nucleotide diversity. Finally, we used RNAseq data to detect the presence of dosage compensation in somatic tissues, as well as to explore gene expression tissue-specificity, and sex-bias in gene expression. We find high conservation of gene content between the mecopteran X and the dipteran Muller F element, as well as several shared biological features, such as the presence of dosage compensation and a low amount of genetic diversity, consistent with a low recombination rate. However, the 2 homologous X chromosomes differ strikingly in their size and number of genes they carry. Our results therefore support a common ancestry of the mecopteran and ancestral dipteran X chromosomes, and suggest that Muller element F shrank in size and gene content after the split of Diptera and Mecoptera, which may have contributed to its turnover in dipteran insects.