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(Symphoricarpos Albus), Attractive to Rhagoletis Zephyria Flies from the W JChemEcol DOI 10.1007/s10886-016-0814-8 Identification of Host Fruit Volatiles from Snowberry (Symphoricarpos albus), Attractive to Rhagoletis zephyria FliesfromtheWesternUnitedStates Dong H. Cha1,2,3 & Shannon B. Olsson1,4 & Wee L. Yee 2 & Robert B. Goughnour2 & Glen R. Hood5 & Monte Mattsson6 & Dietmar Schwarz7 & Jeffrey L. Feder5 & Charles E. Linn Jr1 Received: 9 September 2016 /Revised: 13 December 2016 /Accepted: 21 December 2016 # Springer Science+Business Media New York 2017 Abstract A mixture of behaviorally active volatiles was iden- apple, black hawthorn (C. douglasii) and ornamental hawthorn tified from the fruit of snowberry, Symphoricarpos albus (C. monogyna) from Washington state. Selected subtraction laevigatus,forRhagoletis zephyria flies reared from snowberry assays showed that whereas removal of DMNT or 1-octen-3- fruit. A nine-component blend containing 3-methylbutan-1-ol ol significantly reduced the level of upwind flight, removal of (3%), dimethyl trisulfide (1%), 1-octen-3-ol (40%), myrcene myrcene and β-caryophyllene, or dimethyl trisulfide alone did (8%), nonanal (9%), linalool (13%), (3E)-4,8-dimethyl-1,3,7- not significantly affect the proportion of upwind flights. Our nonatriene (DMNT, 6%), decanal (15%), and β-caryophyllene findings add to previous studies showing that populations of (5%) was identified that gave consistent electroantennogram Rhagoletis flies infesting different host fruit are attracted to activity and was behaviorally active in flight tunnel tests. In unique mixtures of volatile compounds specific to their respec- other flight tunnel assays, snowberry flies from two sites in tive host plants. Taken together, the results support the hypoth- Washington state, USA, displayed significantly greater levels esis that differences among flies in their behavioral responses to of upwind oriented flight to sources with the snowberry volatile host fruit odors represent key adaptations involved in sympatric blend compared with previously identified volatile blends from host plant shifts, contributing to host specific mating and gen- domestic apple (Malus domestica) and downy hawthorn erating prezygotic reproductive isolation among members of (Crataegus mollis) fruit from the eastern USA, and domestic the R. pomonella sibling species complex. Keywords Gas chromatography . Electroantennogram * Charles E. Linn, Jr detection . Flight tunnel . Sympatric speciation . Habitat [email protected] choice . Reproductive isolation 1 Department of Entomology, NYS Agricultural Experiment Station, Cornell University, Geneva, NY 14456, USA 2 USDA-ARS Yakima Agricultural Research Laboratory, Introduction Wapato, WA 98951, USA 3 Present address: USDA-ARS, 64 Nowelo Street, Hilo, HI 96720, The apple maggot, Rhagoletis pomonella (Walsh) (Diptera: USA Tephritidae), is a model for understanding ecologically based 4 Present address: Naturalist-Inspired Chemical Ecology, National speciation via sympatric host plant shifting (Berlocher and Centre for Biological Sciences, GKVK Campus, Tata Institute of Feder 2002; Dres and Mallet 2002; Feder 1998;Funketal. Fundamental Research, Bellary Road, Bangalore 560 065, India 2002). The shift of the fly from native host downy hawthorn, 5 Department of Biological Sciences, University of Notre Dame, Notre Crataegus mollis Scheele (Rosales: Rosaceae), to introduced Dame, IN 46656, USA Eurasian apple, Malus domestica Borkhausen (Rosales: 6 Department of Botany and Plant Pathology, Oregon State University, Rosaceae) in the mid-1800s is often cited as an example of Cworvallis, OR 97201, USA host race formation in the absence of geographic isolation and 7 Department of Biology, Western Washington University, 510 High in the presence of gene flow (Bush 1966, 1969; Berlocher Street, MS 9160, Washington 98225, USA et al. 1993; Berlocher and Feder 2002; Coyne and Orr 2004; JChemEcol Feder et al. 1988;McPheronetal.1988). The shift of USA (Smith and Bush 2000; Gavrilovic et al. 2007), and R. pomonella to apple also resulted in the fly becoming a S. albus variety albus, which is native to eastern North major pest of commercial apple production in the northeastern America. We report the identification of a behaviorally active and midwestern regions of the USA. blend of volatiles from S. albus variety laevigatus fruit and One of the key ecological adaptations involved in the host flight tunnel assays comparing the responses of R. zephyria shift of R. pomonella to apple involves host choice based on and R. pomonella to snowberry and several other identified fruit odor discrimination (Averill et al. 1988;Linnetal.2003; blends from apple and different hawthorn hosts infested by Nojima et al. 2003a, b; Zhang et al. 1999). Rhagoletis flies. pomonella use volatiles emitted from ripe fruit as the first long to intermediate range cue to find and distinguish between different host plants (Fein et al. 1982; Prokopy et al. 1973, Methods and Materials 1987; Prokopy and Roitberg 1984; Reissig et al. 1982). Fruit odor discrimination is important because Rhagoletis flies mate Insects Snowberry-origin fly larvae were collected in 2009 exclusively on or near the fruit of their respective host plants from fruit at two sites, Burnt Bridge Creek, Vancouver, WA (Feder et al. 1994; Prokopy et al. 1971, 1972). Apple-origin and St. Cloud Park, Stevenson, WA and reared in the labora- flies in the eastern USA have rapidly evolved to prefer the tory using standard R. pomonella husbandry techniques odor of apple fruits and avoid that of hawthorns, while the (Dambroski and Feder 2007;Linnetal.2003; Neilson and opposite is true for the ancestral downy hawthorn race McCallen 1965). Black hawthorn and ornamental hawthorn (Feder and Forbes 2007, 2008; Forbes et al. 2005; Forbes fly larvae were similarly reared from fruit collected from the and Feder 2006;Linnetal.2003, 2004, 2005a, b). Burnt Bridge Creek site from 2008 to 2010, and black haw- Additional studies have shown a similar pattern of host thorn and apple-origin fly larvae from fruit collected at the St. fruit volatile preference for populations of R. pomonella that Cloud Park site from 2008 to 2010. In addition, eastern downy infest different native species of hawthorns in the southern hawthorn larvae collected in 2010 from fruit at Fennville, USA (Berlocher 2000; Berlocher and Enquist 1993;Cha Michigan (MI) were reared to adulthood in the laboratory. et al. 2011a, b, 2012a; Lyons-Sobaski and Berlocher 2009; Eclosing adults from all locations were sent to the Geneva Powell et al. 2012), as well as flies infesting flowering dog- NY lab and kept in an environmental chamber at 23–24 °C, wood, Cornus florida, found throughout the eastern USA, and 16 L: 8D photoperiod, and 65–70% relative humidity, and the immediate sister species to R. pomonella (Berlocher 1999, maintained on an artificial diet containing water, sugar, vita- 2000;Nojimaetal.2003b). mins, casein hydrolysate, and salt (Fein et al. 1982). Adult The geographic range of the apple maggot fly is not limited flies 0–7and10–21 days old were used for GC-EAD analyses to the eastern and southern USA, however. In the late 1970s, and flight-tunnel behavior tests, respectively. Eastern apple- R. pomonella was detected in the Pacific Northwest, believed origin R. pomonella tested in the flight tunnel in 2010 came to be the result of human mediated transport of larval infested from a laboratory colony maintained on Red Delicious apples apples from the eastern USA (AliNiazee and Penrose 1981; at the New York State Agricultural Experiment Station, AliNiazee and Brunner 1986; AliNiazee and Westcott 1986). Barton Laboratory in Geneva, NY (Linn et al. 2003; Neilson Populations of R. pomonella in the western USA also infest and McCallen 1965). native black hawthorn, C. douglasii, and the introduced orna- mental hawthorn, C. monogyna (Hood et al. 2013;Yee2008; Fruit Snowberry fruit were collected at the Geneva Yee and Goughnour 2008; Yee et al. 2012, 2015). As in the Experiment Station from an ornamental planting of the species eastern and southern USA, volatile blends have been identi- Symphoricarpos albus laevigatus,asidentifiedinGavrilovic fied for each of these western fruit types (Cha et al. 2012b; et al. (2007). Collected snowberry fruit were placed in sam- Linn et al. 2012; Sim et al. 2012). pling containers (see below) at room temperature for prepara- Here, we expand our studies on the chemical ecology of tion of headspace volatile collections. Rhagoletis flies in the western USA by investigating a sibling species of R. pomonella, the snowberry fly, R. zephyria.The Headspace Volatile Sampling Adsorbent samples of fruit geographic range of R. zephyria extends from British headspace volatiles were made from whole fruit using 2.4 L Columbia to central California and eastward across the north- closed volatile collection chambers (ARS, Inc., Gainesville, ern USA and southern Canada (Bush 1966; Foote et al. 1993; Florida, USA). Field collected snowberry fruit (500–800 ml in Gavrilovic et al. 2007). The fly infests the fruit of common volume) were gently cleaned with distilled water, dried, and snowberry, Symphoricarpos albus variety laevigatus, aplant then put into a collection chamber. Clean air was pushed into native to the western USA, ranging from San Luis Obispo in the chamber at 0.5 L min−1, and volatiles were pushed out California north to Alaska. The fly also infests western snow- through volatile traps (activated charcoal filters, ORBO32- berry, S. occidentalis, in the northern Great Plains states in the small, Supelco
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