Prey-associated genetic differentiation in two species of silver fly (Diptera: Chamaemyiidae), Leucotaraxis argenticollis and L. piniperda

Abstract

Sympatric host-associated genetic differentiation is a prominent pattern that could lead to speciation. In insects, there are numerous examples of host-associated differentiation among herbivores that prefer different plants, and parasitoids that prefer different hosts, but few examples for specialist predators. We developed new microsatellite loci for two species of silver fly, Leucotaraxis argenticollis (Zetterstedt) and L. piniperda (Malloch) (Diptera: Chamaemyiidae), being evaluated as biological control agents for the hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), in eastern North America where it is a nonnative pest. We obtained DNA from specimens of both fly species feeding on native A. tsugae in western North America, as well as on other western and eastern adelgid species. We performed population genetic analyses using the new loci and DNA barcode sequences. Our results confirmed east–west allopatric divergence and uncovered nested genetic differentiation associated with different adelgid prey species and their host plants in western North America for both species of silver flies. For both species, there is also evidence for a longer history of diversification in the west, with ancestral specialization of feeding on pine adelgids, which was retained after range expansion to the east. More recently, divergence to feeding on new adelgid prey species occurred in the west. Our findings are consistent with the hypothesis that host-alternating life cycles in Adelgidae may provide temporary escape from specialist predators. We discuss the implications for biological control efficacy and potential for lineage hybridization as western flies are released in the east to control A. tsugae.