The role of host-plant hybridization in host-associated population divergence in Phytomyza glabricola (Diptera: Agromyzidae)

Abstract

<italic>Phytomyza glabricola</italic> (Diptera: Agromyzidae) is a leaf-mining fly native to the eastern United States that mines two sympatric native holly species, <italic>Ilex coriacea</italic> and <italic>I. glabra</italic>. Recent work revealed significant genetic divergence between host-associated populations of flies in North and South Carolina, suggesting the populations are host forms and recent work in <italic>Ilex</italic> phylogenetics hint the two holly hosts may hybridize. In this work, I investigated potential ecological speciation in <italic>P. glabricola</italic>, hybridization in its host plants, and how the hybridization among host plants may affect gene flow between host forms of the flies.

No-choice mating trials in a greenhouse revealed reproductive isolation between host forms of <italic>P. glabricola</italic> and suggested female flies are capable of making oviposition mistakes resulting in adult offspring on the non-natal host. Based on these results, I used sequences of the nuclear gene EF-1&alpha; and AFLPs to genetically confirm host form status of the flies, and identify <italic>I. glabra</italic> as the ancestral host. In addition, genome scans revealed several loci under divergent selection among the hosts, suggesting the flies may be undergoing ecological speciation.

To investigate the role host plants may play in the genetic divergence among flies, I first used AFLPs to confirm hybridization between <italic>I. coriacea</italic> and <italic>I. glabra</italic>. Hybridization rates differed across the geographic range of the species, which was also reflected in the morphology of the leaves. There were no general patterns, however, in the phenotypes of hybrid plants, and no single morphological trait that could reliably identify the hybrids.

Finally, I combined genetic data of the flies and the plants to determine whether hybrid plants serve as bridges or barriers for the flies. Population comparisons revealed a significant positive relationship between hybridization in the plants and gene flow in the flies, and individual comparisons indicated flies are using the hybrid plants, albeit at low levels. The results suggest hybrids could serve as bridges between parental species, helping explain how a species from a typically monophagous lineage could expand its host range.