Invasion Genetics of American Cherry Fruit Fly in Europe and Signals of Hybridization with the European Cherry Fruit

DOI: 10.1111/eea.12041 Invasion genetics of American cherry fruit flyinEurope and signals of hybridization with the European cherry fruit fly Jes Johannesen1*, Nusha Keyghobadi2, Hannes Schuler3, Christian Stauffer3 & Heidrun Vogt4 1Institute of Zoology, Ecological Department, University of Mainz, Johann-Joachim-Becherweg 13, Mainz 55128, Germany, 2Department of Biology, Western University, London, Ontario, ON N6A 5B7, Canada, 3Department of Forest & Soil Sciences, Institute of Forest Entomology, Forest Pathology & Forest Protection, BOKU, University of Natural Resources & Applied Life Sciences, Hasenauerstrasse 38, Vienna 1190, Austria, and 4Julius Kuhn-Institute,€ Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Fruit Crops and Viticulture, Schwabenheimer Strasse 101, Dossenheim 69221, Germany Accepted: 2 January 2013 Key words: Rhagoletis cingulata, Rhagoletis indifferens, Rhagoletis cerasi, microsatellites, COI, cross- species amplification, hybridization, invasion biology, pest species, Diptera, Tephritidae, wing pattern Abstract The American cherry fruit fly is an invasive pest species in Europe, of serious concern in tart cherry production as well as for the potential to hybridize with the European cherry fruit fly, Rhagoletis cerasi L. (Diptera: Tephritidae), which might induce new pest dynamics. In the first European reports, the question arose whether only the eastern American cherry fruit fly, Rhagoletis cingulata (Loew) (Di- ptera: Tephritidae), is present, or also the closely related western American cherry fruit fly, Rhagoletis indifferens Curran. In this study, we investigate the species status of European populations by comparing these with populations of both American species from their native ranges, the invasion dynamics in German (first report in 1993) and Hungarian (first report in 2006) populations, and we test for signals of hybridization with the European cherry fruit fly. Although mtDNA sequence gene- alogy could not separate the two American species, cross-species amplification of 14 microsatellite loci separated them with high probabilities (0.99–1.0) and provided evidence for R. cingulata in Europe. German and Hungarian R. cingulata populations differed significantly in microsatellite allele frequencies, mtDNA haplotype and wing pattern distributions, and both were genetically depauper- ate relative to North American populations. The diversity suggests independent founding events in Germany and Hungary. Within each country, R. cingulata displayed little or no structure in any trait, which agrees with rapid local range expansions. In cross-species amplifications, signals of hybridization between R. cerasi and R. cingulata were found in 2% of R. cingulata individuals and in 3% of R. cerasi. All putative hybrids had R. cerasi mtDNA indicating that the original between-species mating involved R. cerasi females and R. cingulata males. Doody et al., 2009; Luan et al., 2012), whereas indirect Introduction effects between native and invasive species can arise via the Invasive species have serious impacts on agricultural crops transmission of new pathogens (Kozubikova et al., 2009). and biodiversity worldwide (Shine, 2007; Vie et al., 2009). A third potentially serious impact of invasive species Deleterious effects may take place by direct interaction involves altering the genetic constitution of native species between species for resources, such as predation, herbiv- through hybridization and introgression. This may for ory, or competitive exclusion (Reitz & Trumble, 2002; example lead to species erosion (Elledge et al., 2008) or new disease syndromes (Brasier, 2001; Nunney et al., *Correspondence: Jes Johannesen, Institute of Zoology, Ecological 2010). Department, University of Mainz, Johann-Joachim-Becherweg 13, The eastern American cherry fruit fly, Rhagoletis cingu- Mainz 55128, Germany. E-mail: [email protected] lata (Loew) (Diptera, Tephritidae), is an invasive species © 2013 The Netherlands Entomological Society Entomologia Experimentalis et Applicata 1–12, 2013 Entomologia Experimentalis et Applicata © 2013 The Netherlands Entomological Society 1 2 Johannesen et al. in Europe that causes direct negative effects in agricultural 1997), of which the two most widespread are R. cingulata cherry production and potentially poses the threat of and Rhagoletis indifferens Curran. In the first reports from hybridizing with the native European cherry fruit fly, Europe, it was debated whether one or both of these two Rhagoletis cerasi L. Direct negative effects are caused by lar- species were present (Merz, 1991). The two species are val infestation of cherries, particularly in Prunus cerasus L. genetically closely related (Berlocher & Bush, 1982; Smith (tart cherry; Rosaceae) (Lampe et al., 2005). The infesta- & Bush, 1997) and morphologically very similar (Bush, tion of tart cherries poses a new pest syndrome because 1966). In the native range, the main identification trait of important economic varieties like ‘Schattenmorelle’ and these very similar species is the geographical distribution. ‘Gerema’ mature roughly 3–4 weeks later than the main The eastern cherry fruit fly R. cingulata occurs in eastern sweet cherry varieties, Prunus avium L., and, in doing so, and midwestern USA, Canada, and Mexico, whereas the they have avoided high infestation rates by R. cerasi, whose western cherry fruit fly R. indifferens is found in western peak flight period is mainly timed to the phenology of North America. Morphologically, R. cingulata has a yellow middle- to late-ripening sweet cherry. By contrast, the fore coxa and the anterior apical crossband on the wing is flight period of R. cingulata coincides with the above- often reduced to an isolated spot, whereas R. indifferens mentioned tart cherry varieties causing infestation rates up has posteriorly black shaded fore coxa and the anterior to 30% (Vogt, 2007; Vogt et al., 2010). Reported for the apical crossband is rarely reduced to an isolated spot first time in Europe in 1983 in Switzerland and in 1993 in (Foote et al., 1993). Although the morphological determi- Germany, R. cingulata is now established in Germany nation is most easily based on the frequency of the (Lampe et al., 2005; this study) and The Netherlands crossband’s spot-line pattern, it remains a frequency based (Smit & Dijkstra, 2008), whereas recent reports from Hun- and not a decisive trait and this has perhaps led to confu- gary (Szeoke,€ 2006) and Slovenia (OEPP/EPPO, 2007) sion in species determinations outside the core distribu- indicate new pest status in these countries. tion ranges in USA (CABI, 2012) and in the invasive range The potential threat of hybridization posed by Ameri- in Europe (Merz, 1991; van Aartsen, 2001). can cherry fruit flies is the possibility for introgression into In this study, we asked the following four questions to R. cerasi populations and the evolution of novel pest explore the species status and population dynamics of dynamics. In the Tephritidae, plants for oviposition also American cherry fruit flies in Europe. (1) Which species is/ act as mating locations (Zwolfer,€ 1974). Both the Ameri- are present in Europe? (2) How genetically structured can and the European cherry fruit fly use cherry trees as are European populations of American cherry fruit flies? mating location, and this creates the possibility for contact (3) Are there signs of multiple introductions in the Euro- and hybridization between them. In North America, inde- pean populations? (4) Are there signals of hybridisation pendent host plant shifts of two native Rhagoletis species, with the European cherry fruit fly? The second question Rhagoletis mendax Curran and Rhagoletis zephyria Snow, addresses the relative rate of dispersal in the introduced to the same introduced plant, Lonicera spec., has led to the range. We answer these questions by comparing allele fre- evolution of a hybrid Rhagoletis species (Schwarz et al., quency distributions at 14 microsatellite loci, mtDNA 2005). Although American and European cherry fruit flies haplotypes, and wing patterns of North American cherry have different peak flight and mating periods, they show fruit flies sampled in Germany and Hungary and compare considerable overlap (Lampe et al., 2005; Vogt et al., them with reference populations of R. cingulata and R. in- 2010). The phenological overlap, and with it the potential differens from eastern and western North America, respec- for increasing mating interactions between the species, can tively, and R. cerasi collected in Germany and Austria. The be extended by prolonging the sweet cherry season with European populations of American fruit fly in this study late varieties or by different management practices (Teix- represent a succession of population establishments: ‘old’ eira et al., 2007). The observation that some R. cerasi do populations in western Germany, ‘middle-aged’ popula- not diapause (Koppler,€ 2008) could also lead to a second tions in eastern Germany, and ‘young’ populations in generation in the late flight period of R. cingulata. Finally, Hungary. contact between the species may be facilitated by the wide distribution in Europe of the native host plant Prunus serotina Ehrh. (black cherry). Thus, both the possibility Materials and methods of bridging flight seasons and the introduction of a new Sampling host plant to R. cerasi (i.e., P. serotina) may facilitate Flies were collected in North America and Europe in 2009 hybridization. and 2010 in P. avium (sweet cherry) and P. cerasus (tart

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