Ecological and Genomic Evidence of Cryptic Speciation in the Potato Psyllid (Bactericera cockerelli)

The potato psyllid (Bactericera cockerelli) is a crop pest that serves as a vector for the bacterial pathogen Candidatus Liberibacter solanacearum (CLso), which causes disease in solanaceous and apiaceous crops. This psyllid species carries substantial haplotypic diversity based on mitochondrial cytochrome oxidase 1 (mtCOI) sequences, associated with strong geographic and temporal separation. Using mtCOI sequencing and genomic ddRADseq analysis of 111,587 SNPs across 590 individuals collected from native Solanaceae and cultivated crops at 50 geographically paired sites in California, we show that the previously described haplotype diversity in B. cockerelli may represent at least three genetically distinct cryptic species. These three lineages exhibited extremely high genomic F _ST values across all 13 chromosomes and are strongly partitioned by the host plant. The Northwestern lineage is strictly associated with the native perennial Solanum umbelliferum, while the Western lineage is associated with solanaceous crops, and the Southwestern lineage moves between native and cultivated hosts in desert regions. Hybridization is also rare, suggesting reproductive isolation. SNP and divergence analyses for the obligate bacterial symbiont support conclusions of the host nuclear and mtCOI sequence analyses. We also detected five CLso variants in psyllid samples. The Northwestern lineage housed G, Sumb2, F and B variants, while the Western lineage housed only B and A variants. The largest diversity of CLso variants occurred in coastal regions where psyllid lineages overlap. Exploring the ecology and CLso associations of this potential cryptic species complex provides a foundation for improving biosecurity and management of potato psyllids and CLso pathogens.