Origins of virulence: A molecular investigation of the genetic relationship among avirulent and virulent soybean aphid biotypes

The soybean aphid (Aphis glycines) was introduced to North America in 2000 and quickly established itself as the continent’s premier insect pest of soybean.  Host plant-resistant (HPR) soybean was bred shortly after the invasion, providing natural plant-based resistance against the aphid. Breeders achieved early success with the Rag1 (Resistance to Aphis glycines) gene, but an aphid biotype virulent to the Rag1 expressing soybean was discovered prior to Rag1’s commercialization. Designated biotype 2, this aphid lineage is capable of feeding and parthenogenesis on Rag1 soybean where the HPR susceptible biotype 1 cannot. Biotypic virulence is commonly treated as an issue of Mendellian inheritance, with growers decreasing selection pressure on biotypes by mixing HPR and susceptible plants. However, theoretical and applied research suggests biotype virulence is a product of numerous evolutionary processes including: speciation, race formation, coadaptive gene complexes, and non-genetic factors. The diversity of biotype virulence sources calls into question the efficacy of selection based solutions, and illustrates the importance of understanding the molecular basis of biotype dispersal and inheritance. We investigated the mechanism of biotypic virulence in soybean aphid biotypes through population genetic analysis of eighteen single nucleotide polymorphisms from concurrently collected and geographically identical populations of biotype 1 and 2 across northern Ohio. Genetic differentiation between populations was small and did not correlate with biotypic designation or geographic location.  This lack of correlation, coupled with high diversity in genotypes of both biotypes, suggests that coadaptive gene complexes or a non-genetic mechanism is the source of virulent soybean aphid biotypes.