Tephritid fruit flies belonging to the Rhagoletis pomonella sibling species complex are controversial because they have been proposed to diverge in sympatry (in the absence of geographic isolation) by shifting and adapting to new host plants. Here, we report evidence suggesting a surprising source of genetic variation contributing to sympatric host shifts for these flies. From DNA sequence data for three nuclear loci and mtDNA, we infer that an ancestral, hawthorn-infesting R. pomonella population became geographically subdivided into Mexican and North American isolates Ϸ1.57 million years ago. Episodes of gene flow from Mexico subsequently infused the North American population with inversion polymorphism affecting key diapause traits, forming adaptive clines. Sometime later (perhaps ؎1 million years), diapause variation in the latitudinal clines appears to have aided North American flies in adapting to a variety of plants with differing fruiting times, helping to spawn several new taxa. Thus, important raw genetic material facilitating the adaptive radiation of R. pomonella originated in a different time and place than the proximate ecological host shifts triggering sympatric divergence.

In On the Origin of Species, Darwin proposed that natural selection had a fundamental role in speciation. But this view receded during the Modern Synthesis when allopatric (geographic) models of speciation were integrated with genetic studies of hybrid sterility and inviability. The sympatric hypothesis posits that ecological specialization after a host shift can result in speciation in the absence of complete geographic isolation. The apple maggot, Rhagoletis pomonella, is a model for sympatric speciation in progress. Hawthorn (Crataegus spp.) is the native host for R. pomonella in N. Americas. But in the mid-1800s, a new population formed on introduced, domesticated apple (Malus pumila). Recent studies have conferred 'host race' status on apple flies as a potentially incipient species, partially isolated from haw flies owing to host-related adaptation. However, the source of selection that differentiates apple and haw flies is unresolved. Here we document a gene-environment interaction (fitness trade-off) that is related to host phenology and that genetically differentiates the races.