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The evolutionary success of sap-feeding hemipteran insects in the suborder Auchenorrhyncha was enabled by nutritional contributions from their heritable endosymbiotic bacteria. However, the symbiont diversity, functions, and evolutionary origins in this large insect group have not been broadly characterized using genomic tools. In particular, the origins and relationships among ancient betaproteobacterial symbionts Vidania (in Fulgoromorpha) and Nasuia/Zinderia (in Cicadomorpha) are uncertain. Here, we characterized the genomes of Vidania and Sulcia from three Pyrops planthoppers (family Fulgoridae) to understand their metabolic functions and evolutionary histories. We find that, like in previously characterized planthoppers, these symbionts share nutritional responsibilities, with Vidania providing seven out of ten essential amino acids. Sulcia lineages across the Auchenorrhyncha have a highly conserved genome but with multiple independent rearrangements occurring in an early ancestor of Cicadomorpha or Fulgoromorpha and in a few succeeding lineages. Genomic synteny was also observed within each of the betaproteobacterial symbiont genera Nasuia, Zinderia, and Vidania, but not across them, which challenges the expectation of a shared ancestry for these symbionts. The further comparison of other biological traits strongly suggests an independent origin of Vidania early in the planthopper evolution and possibly of Nasuia and Zinderia in their respective host lineages. This hypothesis further links the potential acquisition of novel nutritional endosymbiont lineages with the emergence of auchenorrhynchan superfamilies.

Planthoppers (Hemiptera: Fulgoromorpha) are a species‐rich and globally distributed insect clade with high economic, ecological and evolutionary importance. However, the relationships among planthopper lineages and families remain unclear. Previous efforts based on inconsistent morphological traits, a few genes or limited sampling often resulted in conflicting tree topologies. Here, we used genome‐level data to assemble 1164 nuclear single‐copy genes and 13 mitochondrial protein‐coding genes for 149 planthopper species representing 19 out of 21 extant families. Additional markers were added from published mitogenomes, expanding our sampling to 285 species. These markers were used for maximum likelihood–based tree inference and dating analyses. The newly inferred phylogenies validated well‐accepted relationships and recovered novel placements for several taxa, including the family Achilixiidae and species from the tribe Lyncidini and genus Madagascaritia in Dictyopharidae and Fulgoridae. Based on molecular and morphological evidence, we proposed taxonomic changes including the establishment of a new family Borysthenidae stat. rev. within Delphacoidea and a new superfamily Meenoploidea superfam. nov. with redefined Kinnaridae stat. rev. and Meenoplidae stat. rev. The time analyses based on 57 nuclear markers and 30 fossils dated the origin of extant Fulgoromorpha back to Guadalupian, Permian (~263 Ma), close to the maximum constraint at 267.3 Ma, while applying an older root constraint resulted in an origin in Mississippian, Carboniferous (~332 Ma). While future sampling of unstudied fauna in unexplored regions or habitats may change the topology, the current phylogenomic analysis will serve as a solid foundation for research into planthopper ecology, evolution and significance. [ABSTRACT FROM AUTHOR]