Locusta migratoria Genome sequencing. Locusta migratoria isolate:cfst_grasshopper1

We present the first chromosome-level genome assembly of the grasshopper, Locusta migratoria, 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 L. migratoria 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.

本研究报道了全球最大昆虫基因组之一的飞蝗（Locusta migratoria）首个染色体级全基因组组装结果。本研究利用雌性（XX）与雄性（X0）个体间的测序覆盖度差异，鉴定了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（dosage compensation）效应，且精巢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）与双翅目（Diptera）四个昆虫目中高度保守；尽管经历了4亿年的演化分化，该800 Mb的飞蝗X染色体仍与果蝇的祖先X染色体同源，这提示要么性染色体经历了多次起源且基因组成高度相似，要么X染色体经历了长期的演化保守。本研究依托X染色体的这一广泛保守性，针对快速X染色体演化（Fast-X evolution）的时间动态展开验证，结果发现：与X保守基因的缓慢演化相比，新出现的X连锁基因呈现出近期爆发式演化的特征。此外，本研究结果显示，X染色体是与迁徙以及飞蝗群聚表型相关的适应性蛋白演化的热点区域。综上，本研究结果揭示了X染色体上一个兼具演化保守性与适应性的典型案例。