Ecological speciation in the holly leaf-miner, Phytomyza glabricola (Diptera: Agromyzidae)

Phytophagous insects are often specialized to particular host plants. If a host range expansion occurs, divergent selection between the ancestral and novel hosts can potentially lead to reproductive isolation, especially if insects reproduce on the host, in the process known as ecological speciation. We tested for evidence of ecological speciation in a leaf-mining fly associated with two species of holly, all of which are native to the eastern United States. Nuclear sequence data indicated the flies have expanded from Ilex glabra to I. coriacea, documenting one of very few examples of an endemic host range expansion. No-choice mating trials revealed that flies from both host plants could mate and produce viable offspring on either host. However, flies from different host plants did not produce leaf-mines, implying some form of reproductive isolation. Despite the reproductive isolation, there is evidence of ongoing gene flow between host-associated populations of flies. Yet, the flies showed significant host-associated genetic differences in all collection locations despite sympatry, indicating the maintenance of genetic divergence despite gene flow. Finally, AFLP genome scans revealed several loci under divergent selection across hosts. We conclude that Phytomyza glabricola is in the process of ecological speciation fueled by adaptation to different host plant species.