shift of the species R. pomonella from its ancestral host hawthorn (Crataegus spp.) to introduced, domesticated apple (Malus pumila) within the last 150 years in the eastern United States is often cited as an example of host race formation in action, the hypothesized initial stage of sympatric speciation (Bush, 1966, 1969). However, we have discovered a surprising geographic source of genetic variation contributing to sympatric host shifts (Feder et al., 2003a). Based on gene trees constructed for three anonymous nuclear loci mapping to separate rearrangements on chromosomes 1–3 of the R. pomonella genome, as well as mtDNA, we inferred that an ancestral, hawthorn-infesting fly population became geographically subdivided into Mexican and “Northern” (United States) isolates ≈1.57 million years ago (Mya). Episodes of gene flow from the Altiplano highland fly population in Mexico subsequently infused the Northern population with inversion polymorphism affecting key diapause traits, forming adaptive clines. Later, diapause variation in the latitudinal inversion clines appears to have aided flies in the United States in shifting and adapting to various new plants with different fruiting times. These shifts were mediated by population-level changes in allele (inversion) frequencies, generating premating and postmating reproductive isolation in the process and helping to spawn several new host-specific taxa, including the recently formed apple race. We stress that we are not contending that the R. pomonella complex in the United States evolved in allopatry. Rather, certain raw genetic material contributing to the adaptive radiation of R. pomonella in the United States originated in a different time and place than the proximate ecological host shifts triggering sympatric divergence.
The evidence for past introgression and its contribution to sympatric host shifts could be interpreted as indicating that inversions preferentially flowed from the Mexican Altiplano into the Northern fly population after secondary contact. However, the persistence of latitudinal clines in the United States suggests that environmental factors may have constrained the spread (prevented the fixation) of the inversions relative to other genes. Hawthorns tend to fruit later in southern latitudes (H.D. and J.L.F., unpublished data). Hawthorn-fly populations in the United States track this geographic variation in host phenology, possessing inversion genotypes for chromosomes 1–3 in the “South” that cause them to eclose later in the season (Feder and Filchak, 1999; Feder et al., 2003a; Filchak et al., 2000). The pattern continues into Mexico. In the Altiplano, flies infest their primary hawthorn hosts, Crataegus mexicana and Crataegus rosei var. rosei, from mid-October to late December (J.R., J.L.F., S. Berlocher, and M.A., unpublished data). However, in the United States, R. pomonella infests various different hawthorn species, mainly from mid-August to late October. Mexican flies take significantly longer to eclose than U.S. flies, even those from Texas (H.D., J.L.F., J.R., S. Berlocher, and M.A., unpub-