Gene flow begets gene flow? Testing the hybrid bridge hypothesis and its role in ecological speciation

Plants and phytophagous insects have a very tight-knit relationship. Hence, divergence in plants can either limit or promote gene flow between populations of the phytophagous insects that feed on them. Plants often hybridize in nature and hybrids can be intermediate in parental traits. If hybrid host plants are intermediate in traits important to the insects that feed on them, they could potentially serve as a bridge between parental host plant species. We tested this ‘hybrid-bridge hypothesis’ using a native leafmining fly, Phytomyza glabricola, that is undergoing ecological speciation between its two native host plants, Ilex coriacea and I. glabra. Using random genomic markers, we found low rates of hybridization between host plants that varied across geographic locations. Levels of gene flow between host-associated populations of insects also geographically varied, with higher rates of gene flow in locations with greater rates of hybridization. In addition, comparisons of individual flies to the plant from which they were collected revealed primarily unidirectional gene flow toward I. coriacea with backcrossed flies feeding on backcrossed plants. The results suggest hybrid host plants may be serving as a bridge for flies to move between parental host plants, potentially allowing for the initial host range expansion from I. glabra to I. coriacea. More broadly, hybridization between hosts in host-race systems could allow for continuing gene flow, preventing speciation from reaching completion.