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Title: Evidence for ecological speciation via a host shift in the holly leafminer, Phytomyza glabricola (Diptera: Agromyzidae)

item HEBERT, J. - University Of Maryland
item Scheffer, Sonja
item HAWTHORNE, D. - University Of Maryland

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/18/2015
Publication Date: 9/18/2016
Citation: Hebert, J.B., Scheffer, S.J., Hawthorne, D.J. 2016. Evidence for ecological speciation via a host shift in the holly leafminer, Phytomyza glabricola (Diptera: Agromyzidae). Molecular Ecology. 6:6565-6577.

Interpretive Summary: Plant-feeding insects cause billions of dollars to US and world agriculture. Leafmining insects are highly damaging to a wide variety of vegetable, cut flower and horticultural crops. This research investigated the genetics of adaptation of a holly leafmining fly to its ornamental holly host plant and to an additional holly species that the insect has more recently begun to feed upon. Results from genome data show that populations of this leafmining fly on the two holly species are genetically distinct, possibly resulting from host-plant adaptation. This research will be of interest to horticulturalists working with holly species as well as ecologists and evolutionary biologists.

Technical Abstract: Evolutionary radiations have been well documented in plants and insects, but we have yet to determine the relative impact of genetic drift and natural selection underlying these radiations. If radiations are adaptive, the diversity of species could be due to ecological speciation in these lineages. Agromyzid flies exhibit patterns of repeated host-associated radiations. We investigated whether the processes of ecological speciation are driving divergence in host-associated populations of the leafminer Phytomyza glabricola feeding on its sympatric host plants, the holly species, Ilex coriacea and I. glabra. Using AFLPs and nuclear sequence data, we found substantial genetic divergence between host-associated populations of these flies throughout their geographic range, and genome scans using the AFLP data identified 13 loci under divergent selection indicating that processes of ecological selection are occurring. EF-1a data strongly suggest that I. glabra is the original host of P. glabricola and that I. coriacea is the novel host, but the AFLP data are ambiguous with regard to directionality of the host shift. Lifecycle differences between host-associated populations of P. glabricola may lead to dramatic differences in both effective population size and in the directionality of gene flow and introgression, all of which will impact microevolutionary processes. These complicate interpretation and prediction in this system, but also offer a novel framework for understanding microevolutionary changes during speciation.