Grasshopper genome reveals long-term conservation of the X chromosome and temporal variation in X chromosome evolution

We present the first chromosome-level genome assembly of the grasshopper, <em>Locusta migratoria</em>, one of the largest insect genomes. We use coverage differences between females (XX) and males (X0) to identify the X chromosome gene content, and find that the X chromosome shows both complete dosage compensation in somatic tissues and an underrepresentation of testes-expressed genes. Remarkably, X-linked gene content from <em>L. migratoria </em>is highly conserved across four insect orders, namely Orthoptera, Hemiptera, Coleoptera and Diptera, and the 800 Mb grasshopper X chromosome is homologous to the fly ancestral X chromosome despite 400 million years of divergence, suggesting either repeated origin of sex chromosomes with highly similar gene content, or long-term conservation of the X chromosome. We use this broad conservation of the X chromosome to test for temporal dynamics to Fast-X evolution, and find evidence of a recent burst evolution for new X-linked genes in contrast to slow evolution of X-conserved genes. Additionally, our results reveal the X chromosome represents a hotspot for adaptive protein evolution related migration and the locust swarming phenotype. Overall, our results reveal a remarkable case of conservation and adaptation on the X chromosome.本研究首次报道了飞蝗（*Locusta migratoria*）的染色体级基因组组装，该物种是基因组规模最大的昆虫类群之一。我们利用雌性（XX）与雄性（X0）间的测序覆盖度差异鉴定X染色体的基因组成，并发现X染色体在体细胞组织中存在完全剂量补偿效应，且睾丸表达基因的占比偏低。值得注意的是，飞蝗的X连锁基因组成在直翅目（Orthoptera）、半翅目（Hemiptera）、鞘翅目（Coleoptera）和双翅目（Diptera）这四个昆虫目中高度保守；尽管经历了4亿年的演化分化，该物种800 Mb的X染色体仍与果蝇的祖先X染色体同源，这提示要么是性染色体经历了多次起源且基因组成高度相似，要么是X染色体经历了长期的演化保守。我们依托这一广泛保守的X染色体特征，针对快速X进化（Fast-X evolution）的时间动态开展检验，结果发现新X连锁基因近期发生了爆发式演化，而X保守基因的演化速率则相对缓慢。此外，我们的研究结果还揭示，X染色体是与迁徙以及飞蝗群聚表型相关的适应性蛋白质进化的热点区域。综上，本研究揭示了X染色体上一种极为罕见的演化保守与适应性进化并存的案例。