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Title: Geographic variation in fruit volatiles emitted by the hawthorn Crataegus mollis and its consequences for host race formation in the apple maggot fly, Rhagoletis pomonella

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

Submitted to: Entomologia Experimentalis et Applicata
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/23/2012
Publication Date: 6/2/2012
Citation: Cha, D.H., Powell, T.H., Feder, J.L., Linn, Jr., C.E. 2012. Geographic variation in fruit volatiles emitted by the hawthorn Crataegus mollis and its consequences for host race formation in the apple maggot fly, Rhagoletis pomonella. Entomologia Experimentalis et Applicata. 143:254-268.

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 ancestral flies shifted their host plant preference from the native host plant, hawthorn, to specialize on apples, so that now there are two “host races” that feed within the fruits of apples or hawthorns. This shift was mediated by the differences in preference and avoidance of odor (blend of volatile chemicals) emitted from the respective host fruits—apple and hawthorn. However, apples emit volatiles that appear to be missing from hawthorn volatiles that are used by the flies. To answer the question how apple maggot flies could shift from hawthorn to apple. Researchers at the USDA ARS, Wapato, WA laboratory and Cornell University, Geneva, NY, investigated the southern red hawthorn, which is taxonomically similar to the northern red hawthorn, to test whether the southern hawthorn could be the source of variation in fruit chemistry. Behavioral assays show that no fly reared from southern hawthorn were attracted to apple fruit volatiles, although southern hawthorn fruit contain all five of the volatile compounds that elicit strong attraction from apple infesting flies and that appear to be largely missing from volatile profiles for northern hawthorn fruit. Our results suggest that the ancestral northern hawthorn race that shifted to apple in the northeastern U.S. had the ability to respond behaviorally to apple fruit volatiles, potentially enabling the shift from hawthorn to apple.

Technical Abstract: The shift of the apple (AP) maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), from its ancestral host downy hawthorn, Crataegus mollis (DH) (Torr. & A. Gray) Scheele, to introduced domesticated AP, Malus domestica Borkh. (both Rosaceae), is a model for ecological divergence and incipient sympatric speciation with gene flow. However, a portion of the variation contributing to the sympatric host shift from DH to AP appears to have a different biogeographic history, pre-dating the shift. One potential source of standing variation may trace to a number of different native hawthorn species infested by R. pomonella in the southern USA, where the AP-attacking race is absent. Herein, we investigate this possibility for the southern red hawthorn (SR) endemic to Texas, Crataegus mollis var. texana (Buckl.), which has been described as a member of the Molles series that includes the more northern distributed DH. We report results from chemical analyses of host fruit volatiles, fly behavioural responses to synthetic fruit blends, and microsatellite surveys of fly populations, implying that R. pomonella infesting SR may behaviourally and genetically represent a native host race differing from the DH-infesting fly. No fly reared from SR responded to AP fruit volatiles in flight tunnel assays. However, coupled gas chromatographic-electroantennographic detection (GC-EAD) profiles for SR fruit contain all five of the component esters that comprise the standard AP volatile blend inducing behavioural orientation for AP-infesting flies, compounds that appear to be largely missing from volatile profiles for DH fruit. Thus, SR-infesting flies do not represent a source for a preassembled AP-accepting phenotype. However, they may help explain why the ancestral DH race that shifted to AP in the northeastern USA had the ability to recognize AP fruit esters, potentially enabling the shift to AP. Our results highlight how categorizing speciation into different geographic modes may not adequately describe the evolutionary origins of important genetic variation fuelling adaptive radiation and the genesis of new biodiversity.