Genomic Comparisons Reveal Selection Pressure and Functional Variation Between Nutritional Endosymbionts of Cave-Adapted and Epigean Hawaiian Planthoppers

Abstract

AbstractPlanthoppers 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.