The Genetic Basis for Fruit Odor Discrimination in Rhagoletis Flies and Its Significance for Sympatric Host Shifts

Abstract

Rhagoletis pomonella (Diptera: Tephritidae) use volatile compounds emitted from the surface of ripening fruit as important chemosensory cues for recognizing and distinguishing among alternative host plants. Host choice is of evolutionary significance in Rhagoletis because these flies mate on or near the fruit of their respective host plants. Differences in host choice based on fruit odor discrimination therefore result in differential mate choice and prezygotic reproductive isolation, facilitating sympatric speciation in the absence of geographic isolation. We test for a genetic basis for host fruit odor discrimination through an analysis of F2 and backcross hybrids constructed between apple-, hawthorn-, and flowering dogwood-infesting Rhagoletis flies. We recovered a significant proportion (30-65%) of parental apple, hawthorn, and dogwood fly response phenotypes in F2 hybrids, despite the general failure of F1 hybrids to reach odor source spheres. Segregation patterns in F2 and backcross hybrids suggest that only a modest number of allelic differences at a few loci may underlie host fruit odor discrimination. In addition, a strong bias was observed for F2 and backcross flies to orient to the natal fruit blend of their maternal grandmother, implying the existence of cytonuclear gene interactions. We explore the implications of our findings for the evolutionary dynamics of sympatric host race formation and speciation.

Identification of Host Fruit Volatiles from Domestic Apple (Malus domestica), Native Black Hawthorn (Crataegus douglasii) and Introduced Ornamental Hawthorn (C. monogyna) Attractive to Rhagoletis pomonella Flies from the Western United States

“…Hence, differences in host plant choice translate directly to mate choice, generating premating reproductive isolation between the apple and downy hawthorn host races (Feder et al, 1994;Linn et al, 2003;Forbes et al, 2005;Forbes and Feder, 2006). In flight tunnel assays and field trapping studies, we found that the eastern apple and downy hawthorn host races of R. pomonella preferentially orient to the fruit volatile blends of their respective native host fruit relative to non-natal volatiles (i.e., apple flies positively respond and fly to a synthetic volatile blend developed for apple fruit and are not overly attracted to downy hawthorn fruit volatiles, and the reverse for downy hawthorn flies) (Linn et al, 2003(Linn et al, , 2004(Linn et al, , 2005aForbes et al, 2005;Dambroski et al, 2005;Forbes and Feder, 2006;Feder andForbes, 2007, 2008).…”

“…For the experiments with apple and black hawthorn-origin flies, each treatment involved a separate group of flies, but for ornamental hawthorn flies, the same group of 25 individuals was tested to all of the treatments. In previous studies, we showed that R. pomonella flies can be repeatedly tested without affecting odor preference as displayed in the flight tunnel (Dambroski et al, 2005). Differences in the frequency of upwind flight were compared using Fisher's Exact Test in R (R development core team, Vienna, Austria).…”

“…In the eastern USA, apple and downy hawthorn-infesting flies use volatile compounds released from the surface of ripening fruit as key olfactory cues to find and discriminate among host plants (Linn et al, 2003(Linn et al, , 2004(Linn et al, , 2005aDambroski et al, 2005;Forbes et al, 2005). Host fruit odor discrimination is important because the eastern apple and downy hawthornorigin flies mate exclusively on or near the fruit of their respective host plants (Prokopy et al, 1971(Prokopy et al, , 1972Feder et al, 1994).…”

Identification of Host Fruit Volatiles from Three Mayhaw Species (Crataegus Series Aestivales) Attractive to Mayhaw-Origin Rhagoletis pomonella Flies in the Southern United States

“…For each set of experiments, almost all of the flies were tested to all of the treatments, usually over a continuous period of 2-4 d, with no more than 3 treatments being tested on a given day. In previous studies, we have shown that R. pomonella flies can be repeatedly tested without affecting odor preference as displayed in the flight tunnel (Dambroski et al, 2005). Differences in the frequency of upwind flight were compared using Fisher's Exact Test in R (R development core team, Vienna, Austria).…”

“…In addition, mark-release-recapture studies in the field have shown that host fidelity while strong, is not absolute, and currently inter-host migration between apples and hawthorns occurs at a rate of~4-6% per generation (Feder et al, 1994). Apple and hawthorn flies readily mate with each other in the lab and produce viable and fertile offspring (Dambroski et al, 2005). Consequently, there appears to be no obvious intrinsic post-zygotic reproductive isolation between the host races, and apple and hawthorn flies are primarily, if not exclusively, isolated by ecological barriers to gene flow.…”