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.

诸多昆虫体内都携带一条古老的X染色体——果蝇穆勒F元件（Drosophila Muller element F），其起源甚至早于昆虫类群本身的出现。值得注意的是，该X染色体在保守存续超过4.5亿年后，在多个双翅目（Diptera）昆虫类群中发生了染色体更替。双翅目与其他已测序昆虫演化支之间存在漫长的演化距离，这使得学界难以推断究竟是何种因素导致了其染色体更替速率的突然提升。本研究首次获取了蝎蛉属（Panorpa）昆虫的基因组与转录组数据。蝎蛉所在的长翅目（Mecoptera）是一个长期被学界忽视的类群，与双翅目互为姊妹目。本研究将基因组组装结果与基因组短读长测序数据相结合，得到了基因组覆盖度信息，并成功鉴定出X染色体连锁的超级支架（super-scaffolds）。我们进一步开展了蝎蛉X染色体与近缘双翅目物种的基因同源性分析，并评估了蝎蛉X连锁基因集与更远缘昆虫类群的基因保守性。我们通过测定其重复序列含量、GC含量与核苷酸多样性，解析了蝎蛉X染色体的结构特征。最后，我们借助RNA测序（RNAseq）数据，检测了体细胞组织中的剂量补偿（dosage compensation）现象，并探究了基因表达的组织特异性与性别偏倚性。本研究发现，长翅目X染色体与双翅目穆勒F元件的基因集具有高度保守性，二者还共享多项生物学特征：例如均存在剂量补偿现象，遗传多样性水平较低，这与低重组率的特征相符。但二者的同源X染色体在染色体大小与携带基因数量上却存在显著差异。因此，本研究结果支持长翅目与祖先双翅目X染色体具有共同起源的假说，并表明穆勒F元件在双翅目与长翅目分化后发生了大小与基因含量的缩减，这一事件或促成了双翅目中X染色体的更替现象。