The addition of a novel host plant to a phytophagous insect's diet may result in subsequent host-plant specialisation, and is believed to be a key cause for speciation in this trophic group. In northern Britain, the tephritid fly Tephritis conura has experienced a unique host-plant expansion, from the melancholy thistle Cirsium heterophyllum to the marsh thistle C. palustre. Here, we examine whether the incorporation of C. palustre in the repertoire of British T. conura flies has caused genetic divergence between populations infesting the old host and the novel host, and how British populations differ from populations infesting C. heterophyllum in continental Europe where C. palustre is not infested. No evidence for restricted gene flow among British C. palustre and C. heterophyllum flies was found. Significant differentiation between British and continental T. conura was found at only one allozyme locus, hexokinase, and caused by a new allele, Hex_95. Hexokinase is related to host-race formation in continental European flies infesting C. heterophyllum and C. oleraceum, and might be linked to loci determining host choice. Based on morphological and phenological data from previous studies, we suggest that T. conura in Britain has adapted to the novel host but that host-race formation is impeded by similar plant phenologies.

Whether or not a host plant is incorporated into a phytophagous insect's diet depends on both the insect's ability to colonize the novel host and the host plant's susceptibility to the insect. The latter, again, will be influenced by the genetic structure of the host plant. Cirsium palustre (marsh thistle) is heavily infested by the tephritid fly Tephritis conura in northern Britain, whereas infestation is not only absent in southern England, but also absent on the European continent where T. conura is common on other Cirsium. To understand why regional infestation patterns evolve, we studied how genetic structure and phylogeographic ancestry of C. palustre are related to the probability of infestation in Britain. The probability of infestation in Britain was related neither to phylogeographic lineage (two lineages were observed in Europe), nor to introgressive hybridization with the original host of T. conura, C. heterophyllum. However, infested British C. palustre were strongly genetically deprived. British C. palustre showed continuous loss of genetic variability towards the northern range edge. The loss was explained best by genetic drift during geographic range expansion, rather than by genetic drift in isolated patches or mating system change from predominately outcrossing to selfing. The phylogeographic pattern of C. palustre strongly suggests Scotland as the geographic origin of a recent host-plant expansion of T. conura.