One species, two lives: cryptic population structure and life-history divergence in a vineyard spittlebug (Aphrophora sp.), a candidate vector for Pierce's disease

Whole genome analysis of spittlebug populations, an Aphrophora species (Hemiptera: Aphrophoridae) known to spread Pierce's disease, from various vineyards in Napa and Sonoma Counties demonstrates that these insects are conspecific with Aphrophora permutata found in quasi-natural populations. The genomes analyzed fall in three autosomal clusters with two sympatric populations (based on admixture) that diverged around 40,000-90,000 years before present according to demographic models. We also recover three related but distinct mitochondrial clusters. There is no genetic differentiation between Napa and Sonoma County vineyard populations and very modest differentiation among vineyards and quasi-natural Berkeley/Oakland Hills population. These vineyard and quasi-natural populations have distinct life histories, including divergent oviposition hosts (understory herbs versus pines) and different patterns of adult seasonal migration (out-migration and return versus simple movement from the understory to the pine canopy). Analysis of the mitochondrial gene COI indicates that A. permutata, Aphrophora fulva and Aphrophora maculosa are intermingled in the same mitochondrial clade, along with the more distantly related species Aphrophora gelida. Further, all three autosomal genetic clusters show evidence of selection for insecticide resistance. We also find that endosymbionts Wolbachia and Rickettsia were both present in a substantial fraction of specimens analyzed, but neither appears to influence population structure. Overall, our findings elucidate an intriguing degree of life history divergence between geographically proximate, conspecific populations linked by gene flow and may have implications for the continued management of vineyard populations.