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

Abstract

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.