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Title: On the scent of standing variation for speciation: behavioral evidence for native sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae) in the southern United States

Author
item POWELL, THOMAS - University Of Notre Dame
item Cha, Dong
item LINN, JR, CHARLES - University Of Notre Dame
item FEDER, JEFFREY - University Of Notre Dame

Submitted to: Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/29/2012
Publication Date: 9/3/2012
Citation: Powell, T.H., Cha, D.H., Linn, Jr, C.E., Feder, J.L. 2012. On the scent of standing variation for speciation: behavioral evidence for native sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae) in the southern United States. Evolution. doi:10.1111/j.1558-5646.2012.01625.x.

Interpretive Summary: The apple maggot fly is a major pest of apples and is a major quarantine concern for apple growers in the western U.S. In the northeastern U.S., some apple maggot fly populations shifted their host plant preference from the native host plant, hawthorn, to specialize on apple, so that now there are two “host races” that feed within the fruits of apples or hawthorns. This shift has been shown to be mediated by the differences in preference and avoidance of odor (blend of volatile chemicals) emitted from the apple and hawthorn fruits. However, apples emit volatiles that appear to be largely missing from hawthorn volatiles that are used by the flies, raising the question of how apple maggot fly evolved a preference for apple in the first place. To understand this, Electrophysiological and behavioral tests were done, using apple maggot flies from different species of native hawthorns in the southern U.S. Blends of fruit chemicals attractive to apple maggot flies infesting these southern hawthorns included the apple chemicals missing from northern hawthorn fruits, potentially explaining why northern hawthorn flies could prefer a blend of apple volatiles. Northern hawthorn flies may have an evolutionary history of responding to these chemicals, if they originated from southern hawthorn fly populations. This information better explains how insects can become crop pests with minor genetic modifications.

Technical Abstract: Standing variation can be critical for speciation. Here, we investigate the origins of fruit odor discrimination for Rhagoletis pomonella underlying the fly’s sympatric shift in the northeastern United States from downy hawthorn (Crataegus mollis) to apple (Malus domestica). Because R. pomonella mate on host fruit, preferences for natal fruit volatiles generate prezygotic isolation. Apples emit volatiles that appear to be missing from gas chromatography/electroantennographic detection profiles for flies infesting downy hawthorns, raising the question of how R. pomonella evolved a preference for apple. In the southern United States, R. pomonella attacks several native hawthorns. Behaviorally active volatile blends for R. pomonella infesting southern hawthorns contain the missing apple volatiles, potentially explaining why downy hawthorn flies could have evolved to be sensitive to a blend of apple volatiles. Flight tunnel assays imply that southern hawthorn populations were not the antecedent of a preassembled apple race, as southern flies were not attracted to the apple volatile blend. Instead, behavioral evidence was found for southern host races on native hawthorns, complementing the story of the historical sympatric shift to introduced apple in the North and illustrating how R. pomonella may evolve novel combinations of agonist and antagonist responses to volatiles to use new fruit resources.