Although fruit fly host status determination/designation lies at the heart of strategic decisions on national and international trade of fruit and vegetables, all attempts thus far to define host plant status have been contentious and as a result long-standing disputes between commercial partners throughout the world have lingered over decades. Part of the problem is that too little effort has been devoted to understanding the underlying mechanisms involved in host plant use by fruit flies and that instead economic and political interests usually prevail. Here we review the most important evolutionary, biological, ecological, physiological, and behavioral aspects that drive host use by fruit flies, and then construct a flow diagram rooted in these fundamentals that outlines a series of steps and definitions to determine if a particular fruit or vegetable (and cultivars thereof) is a natural host, or a conditional (potential, artificial) host, or a nonhost. Along the way, we incorporate risk analysis considerations and propose that the underlying complexity determining host plant utilization by fruit flies requires a flexible systems approach capable of realistically dealing with fly/host/environment/geographic variability on a case-by-case basis.

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 ≈1.57 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.

TheRhagoletis pomonellasibling species complex is a model for sympatric speciation by means of host plant shifting. However, genetic variation aiding the sympatric radiation of the group in the United States may have geographic roots. Inversions on chromosomes 1-3 affecting diapause traits adapting flies to differences in host fruiting phenology appear to exist in the United States because of a series of secondary introgression events from Mexico. Here, we investigate whether these inverted regions of the genome may have subsequently evolved to become more recalcitrant to introgression relative to collinear regions, consistent with new models for chromosomal speciation. As predicted by the models, gene trees for six nuclear loci mapping to chromosomes other than 1-3 tended to have shallower node depths separating Mexican and U.S. haplotypes relative to an outgroup sequence than nine genes residing on chromosomes 1-3. We discuss the implications of secondary contact and differential introgression with respect to sympatric host race formation and speciation inRhagoletis, reconciling some of the seemingly dichotomous views of Mayr, Dobzhansky, and Bush concerning modes of divergence.