Implementing an evolutionary framework for understanding genetic relationships of phenotypically defined insect biotypes in the invasive soybean aphid (Aphis glycines)

Jacob A Wenger,Andy P Michel

doi:10.1111/eva.12084

Abstract

Adaptive evolution of pest insects in response to the introduction of resistant cultivars is well documented and commonly results in virulent (i.e., capable of feeding upon resistant cultivars) insect populations being labeled as distinct biotypes. Phenotypically defined, biotypes frequently remain evolutionarily indistinct, resulting in ineffective application of virulence control measures and shorter durability of resistant cultivars. Here, we utilize an evolutionary framework to discern the genetic relationship between biotypes of the soybean aphid (Aphis glycines, Matsumura). The soybean aphid is invasive in North America and is among the most destructive pests of commercial soybean on the continent. Attempts to breed host-plant-resistant soybean have been hampered by the emergence of virulent aphid biotypes that are unaffected by the plant's resistance mechanism(s). Comparative population genetic analysis of virulent and avirulent (i.e., unable to feed on resistant cultivars) biotypes found populations to be genetically indistinguishable across biotype and geographic distance, with high rates of interpopulation immigration and admixture. The lack of genetic distinction between biotypes coupled with elevated genotypic diversity within all populations suggested virulence has a nongenetic-based or includes a gene complex that is widely distributed throughout soybean aphid populations, which undergo regular dispersal and unimpeded sexual recombination.

Highlights

The interactions between phytophagous insects and their respective host plants have long served as a model system for coevolution (Tilmon 2008)
Collection and biotype differentiation Biotype 1 and 2 soybean aphids were sampled in pairwise, concurrent collections at seven sites across northern Ohio, with sites grouped into two geographic clusters (Fig. 1, Table 2)
The eastern cluster was composed of four sites at the Ohio Agricultural Research and Development Center (OARDC) in Wooster, Wayne County, Ohio; all Wayne county field sites were established within a 2 km radius to allow sampling on a microgeographic scale

Summary

Introduction

The interactions between phytophagous insects and their respective host plants have long served as a model system for coevolution (Tilmon 2008). Many naturally occurring examples exist, though the development of crop cultivars exhibiting natural pest resistance (Painter 1968; Panda and Khush 1995; Smith 2005) provides a widespread anthropogenic microcosm of this interaction. The increased selection pressure associated with the extensive implementation across landscapes accelerates insect and host coevolutionary interactions within agroecosystems as compared to natural environments. The genetic and environmental mechanisms of pest virulence to resistant cultivars are often ill defined. Virulent pests are most commonly organized within the pseudo-taxonomic category of biotype, an intraspecies taxon defined by a shared differentiating phenotype (Claridge and den Hollander 1983; Diehl and Bush 1984). Most biotypes fail to be reclassified and languish within these ambiguous

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