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Abstract Leafhoppers comprise over 20,000 plant‐sap feeding species, many of which are important agricultural pests. Most species rely on two ancestral bacterial symbionts,SulciaandNasuia, for essential nutrition lacking in their phloem and xylem plant sap diets. To understand how pest leafhopper genomes evolve and are shaped by microbial symbioses, we completed a chromosomal‐level assembly of the aster leafhopper's genome (ALF;Macrosteles quadrilineatus). We compared ALF's genome to three other pest leafhoppers,Nephotettix cincticeps,Homalodisca vitripennis, andEmpoasca onukii, which have distinct ecologies and symbiotic relationships. Despite diverging ~155 million years ago, leafhoppers have high levels of chromosomal synteny and gene family conservation. Conserved genes include those involved in plant chemical detoxification, resistance to various insecticides, and defence against environmental stress. Positive selection acting upon these genes further points to ongoing adaptive evolution in response to agricultural environments. In relation to leafhoppers' general dependence on symbionts, species that retain the ancestral symbiont,Sulcia, displayed gene enrichment of metabolic processes in their genomes. Leafhoppers with bothSulciaand its ancient partner,Nasuia, showed genomic enrichment in genes related to microbial population regulation and immune responses. Finally, horizontally transferred genes (HTGs) associated with symbiont support ofSulciaandNasuiaare only observed in leafhoppers that maintain symbionts. In contrast, HTGs involved in non‐symbiotic functions are conserved across all species. The high‐quality ALF genome provides deep insights into how host ecology and symbioses shape genome evolution and a wealth of genetic resources for pest control targets. 

Abstract Planthoppers in the family Cixiidae (Hemiptera: Auchenorrhyncha: Fulgoromorpha) harbor a diverse set of obligate bacterial endosymbionts that provision essential amino acids and vitamins that are missing from their plant-sap diet. “Candidatus Sulcia muelleri” and “Ca. Vidania fulgoroidea” have been associated with cixiid planthoppers since their origin within the Auchenorrhyncha, whereas “Ca. Purcelliella pentastirinorum” is a more recent endosymbiotic acquisition. Hawaiian cixiid planthoppers occupy diverse habitats including lava tube caves and shrubby surface landscapes, which offer different nutritional resources and environmental constraints. Genomic studies have focused on understanding the nutritional provisioning roles of cixiid endosymbionts more broadly, yet it is still unclear how selection pressures on endosymbiont genes might differ between cixiid host species inhabiting such diverse landscapes, or how variation in selection might impact symbiont evolution. In this study, we sequenced the genomes of Sulcia, Vidania, and Purcelliella isolated from both surface and cave-adapted planthopper hosts from the genus Oliarus. We found that nutritional biosynthesis genes were conserved in Sulcia and Vidania genomes in inter- and intra-host species comparisons. In contrast, Purcelliella genomes retain different essential nutritional biosynthesis genes between surface- and cave-adapted planthopper species. Finally, we see the variation in selection pressures on symbiont genes both within and between host species, suggesting that strong coevolution between host and endosymbiont is associated with different patterns of molecular evolution on a fine scale that may be associated with the host diet.