The Geographic Distribution of Rhagoletis pomonella (Diptera: Tephritidae) in the Western United States: Introduced Species or Native Population?

Transcription

1 The Geographic Distribution of Rhagoletis pomonella (Diptera: Tephritidae) in the Western United States: Introduced Species or Native Population? Author(s): Glen R. Hood, Wee Yee, Robert B. Goughnour, Sheina B. Sim, Scott P. Egan, Tracy Arcella, Gilbert Saint-Jean, Thomas H. Q. Powell, Charles C. Y. Xu, and Jeffrey L. Feder Source: Annals of the Entomological Society of America, 106(1): Published By: Entomological Society of America URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

2 ECOLOGY AND POPULATION BIOLOGY The Geographic Distribution of Rhagoletis pomonella (Diptera: Tephritidae) in the Western United States: Introduced Species or Native Population? GLEN R. HOOD, 1,2 WEE YEE, 3 ROBERT B. GOUGHNOUR, 4 SHEINA B. SIM, 1 SCOTT P. EGAN, 1,5 TRACY ARCELLA, 1 GILBERT SAINT JEAN, 1 THOMAS H. Q. POWELL, 1 CHARLES C. Y. XU, 1 AND JEFFREY L. FEDER 1,5 Ann. Entomol. Soc. Am. 106(1): 59Ð65 (2013); DOI: ABSTRACT The apple maggot ßy, Rhagoletis pomonella Walsh (Diptera: Tephritidae), is a major pest of commercially grown domesticated apple (Malus domestica Borkhausen) in North America. The shift of the ßy from its native host hawthorn (Crataegus mollis) to apple in the eastern United States is often cited as an example of incipient sympatric speciation in action. However, R. pomonella is also present in the PaciÞc Northwest region of the United States where it infests apple, native black hawthorn (Crataegus douglasii), and introduced English ornamental hawthorn (C. monogyna). It is believed that R. pomonella was introduced to the Portland, OR, area via larval-infested apples from the east. The ßy subsequently spread through the region, shifting onto black hawthorn and ornamental hawthorn as additional hosts as it spread. It is also possible, however, that R. pomonella is native to black hawthorn in the PaciÞc Northwest and switched to infest apple and ornamental hawthorn after the introduction of these two alternative hosts to the region. Here, we document the distribution of R. pomonella through the PaciÞc Northwest and Rocky Mountain states of the western United States to help clarify the origin(s) of the ßy outside the eastern United States. We report a distribution pattern consistent with the hypothesis that R. pomonella was introduced to the PaciÞc Northwest via infested apples. In particular, the low levels or lack of C. douglasii-infesting R. pomonella east of the Cascade Mountains in the states of Washington, OR, and Idaho implies that the ßy is not native on black hawthorn and is of recent origin. We discuss the evolutionary and applied implications of the results with respect to our current understanding of host race formation and control for R. pomonella. KEY WORDS apple maggot ßy, black hawthorn, English hawthorn, red hawthorn The apple maggot ßy, Rhagoletis pomonella Walsh (Diptera: Tephritidae) is a major economic pest of apples in North America (Boller and Prokopy 1976, AliNiazee and Penrose 1981, Prokopy et al. 1994). The ßy is also a model for speciation in the absence of geographic isolation via sympatric host plant shifting (Bush 1966, Berlocher and Feder 2002, Coyne and Orr 2004). In particular, the sympatric shift of R. pomonella from its native host hawthorn (Crataegus sp.) to introduced, domesticated apple (Malus domestica Borkhausen) in the northeastern United States, 150 yr ago is often cited as an example of ecological speciation-with-gene-ßow in action (Berlocher and Feder 2002, Coyne and Orr 2004). 1 Department of Biological Sciences, University of Notre Dame, 1052 Woodward Ave., Notre Dame, IN Corresponding author, ghood@nd.edu. 3 USDAÐARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA Washington State University, Research and Extension Unit, 1919 NE 78th Street, Vancouver, WA Advanced Diagnostics and Therapeutics, University of Notre Dame, Notre Dame, IN R. pomonella is endemic to the eastern United States, where the apple host race of the ßy originated (Bush 1966, Foote et al. 1993). However, populations of the ßy are also known from the western United States, including the PaciÞc Northwest where they are also a quarantine pest of apples (Brunner 1987, Tracewski et al. 1987, Dowell 1988, Yee and Goughnour 2008). The origin of R. pomonella in the PaciÞc Northwest has important implications for control, as well as being of basic interest to evolutionary biologists. A critical question in these regards is whether R. pomonella was introduced to the PaciÞc Northwest, as opposed to being endemic and attacking a native hawthorn host in the area. It is commonly thought that R. pomonella was introduced to the PaciÞc Northwest in apples because of: 1) a specimen collected from apples near Rowena, OR, in 1951 along the Columbia River conþrmed by researchers at the Oregon Department of Agriculture though to be R. pomonella based on ovipositor length (Dowell 1988); 2) the Þrst report of R. pomonella in residential apple trees in the Portland, OR, area in the late 1970s (AliNiazee and Penrose 1981); and 3) a lack of R. pomonella in agricultural or /13/0059Ð0065$04.00/ Entomological Society of America

3 60 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 1 Fig. 1. Distribution of Rhagoletis pomonella infesting apple (diamond), black hawthorn (square), English ornamental hawthorn (circle), and red hawthorn (triangle) in the PaciÞc Northwestern and Mountain west regions of the United States. Red symbols represent infested locations and white symbols represent uninfested locations (numbers correspond to site designations in Supp. Table 1 [online only]). Species of red hawthorns infested at each location are designated in Supp. Table 1 [online only]. Regions outlined in dashed blue lines (1Ð5) are the areas where R. pomonella were found in the current study and correspond to the sites listed in Table 1. Dashed green outlines shows areas in which black hawthorn and red hawthorn are native to the western United States according to the USDA plant database (United States Department of Agriculture 2012). (Map image 2012 Google). (Online Þgure in color.) museum records before this time (W. Yee, personal communication). After its introduction, the ßy subsequently spread primarily along the western side of the Cascade Mountain range northward from Portland up through Washington into Canada and southward down through Oregon into northern California (Yee 2008, Yee and Goughnour 2008). In addition to apple, R. pomonella also infests hawthorns in the PaciÞc Northwest, principally the native black hawthorn, C. douglasii, and the introduced English ornamental hawthorn, C. monogyna Jacq. (Yee 2008). If R. pomonella was introduced via apple, then the current populations infesting black and ornamental hawthorns would represent recent shifts of the ßy onto these trees and possibly new host-associated races of R. pomonella (Cha et al. 2012, Linn et al. 2012, Sim et al. 2012). However, the presence of ßies on ornamental and black hawthorn also raises several alternative hypotheses about the origin of R. pomonella in the PaciÞc Northwest, including that the ßy: 1) was introduced along with ornamental hawthorn sometime between the Þrst and second world wars (AliNiazee and Penrose 1981, Brunner 1987, Tracewski et al. 1987, Yee 2008); or 2) is native and was previously undetected, possibly because of low population density, on black hawthorn (AliNiazee and Wescott 1986). The issue of introduced versus endemic status for R. pomonella is important for control because if the ßy is native, then any local populations on hawthorns in the central apple growing regions of Washington and Oregon pose potentially serious threats to fruit crops. In contrast, if the ßy was introduced, then the spread of R. pomonella by the transport of larval infested apples should be of greatest concern for growers. Previous studies have implied that C. douglasii is not a prevalent plant east of the Cascade Mountains in central apple growing areas of the PaciÞc Northwest, such as the Yakima Valley region of Washington (Yee 2008, Yee and Goughnour 2008). Moreover, R. pomonella populations, although present, appear to be nominal and conþned mainly to streams and rivers draining from the eastern slopes of the Cascade Mountains (W.Y., unpublished data). It has been proposed that the more arid and hot conditions in central Washington and Oregon have impeded the wide-spread advance of both black hawthorn and R. pomonella into the region (Dowell 1988, Yee 2008, Yee and Goughnour 2008). However, black hawthorn is common further to the north in Washington and Canada, forming an arc stretching along the Rocky Mountains down into far eastern areas of Washington and Oregon, as well as parts of Idaho, Wyoming, Utah, and Colorado (Fig. 1) (Bush 1966, Dowell 1988, McPheron 1990, Messina and Jones 1990, Alldred and Jorgensen 1993). These areas have not been well surveyed, and it is conceivable that endemic populations of R. pomonella exist

4 January 2013 HOOD ET AL.: DISTRIBUTION OF R. pomonella IN THE WESTERN U.S. 61 there and have gone undetected in the past. If true, then these endemic populations of R. pomonella to the north and the east of the currently documented range of the ßy in the PaciÞc Northwest would represent a previously unrecognized threat encroaching on the apple industry. Resolving the question of R. pomonellaõs origin in the PaciÞc Northwest also has ramiþcations for evolutionary biology because it would help clarify the directionality of the host shifts that have transpired between apple and hawthorn in the area. If the apple introduction hypothesis is correct, then after its introduction, R. pomonella ßies shifted back to hawthorn from apple in the last 30 yr (Cha et al. 2012, Linn et al. 2012, Sim et al. 2012). In contrast, if the ßy is endemic, then it likely shifted from black hawthorn to ornamental hawthorn and apple after the introduction of these latter two plants to the PaciÞc Northwest. In this case, the shift to apple would potentially represent an independent origin of an apple-infesting host race of the ßy from the classic example in the eastern United States. Recent studies of ßy responses to synthetic host fruit volatile blends in the laboratory (Cha et al. 2012, Linn et al. 2012) and Þeld (Sim et al. 2012) have provided behavioral evidence for partially reproductively isolated apple, ornamental hawthorn, and black hawthorn host races of R. pomonella in the PaciÞc Northwest. Thus, resolving the history of R. pomonella in the region could help clarify the sequence and nature of host shifts for the ßy. Here, we report the results from an extensive geographic survey of R. pomonella to establish the ßyÕs current distribution in the PaciÞc Northwest and Mountain West regions of the United States to investigate whether R. pomonella is likely native to the far West or was introduced to the area from its native range in the East. If R. pomonella is endemic to the western United States, then we predict that we will Þnd populations of the ßy throughout the West infesting native hawthorn species, including surrounding the central apple growing regions of Washington and Oregon. Populations of R. pomonella have been previously recorded from parts of the states of Utah and Colorado (Bush 1966, McPheron 1990, Messina and Jones 1990, Alldred and Jorgensen 1993, Foote et al. 1993). The origin and status of these two other western ßy populations are also not completely known. However, if R. pomonella is native to the western United States, then we anticipate Þnding that these populations would show a degree of spatial continuity, or at least a plausible historical connection, to ßies further west in Washington and Oregon. In contrast, if R. pomonella was introduced to the PaciÞc Northwest, then we would expect all western ßy populations to be geographically isolated from one another and show little evidence for interconnection now or in the past. Moreover, western R. pomonella should display this disjunct pattern despite the presence of native hawthorns in several intervening areas where the ßy is absent that should likely be infested if it was endemic to the region. Table 1. The five major areas of R. pomonella infestation in the western U.S. along with the host plants attacked in each region Region a General area where R. pomonella is found b 1 Cascade Mountains in Washington and Oregon 2 Northeastern Oregon near Hells Canyon 3 Northern Utah, Southeastern Idaho, and Southwestern Wyoming 4 Eastern foothills of the Rocky Mountains near Boulder, CO 5 Western Colorado in the Rocky Mountains Host plants infected Apple, black, and ornamental hawthorn Black hawthorn Black and red hawthorn Black and red hawthorn Black and red hawthorn a Locations 1Ð5 correspond to the areas designated by dashed lines in Fig. 1. b For detailed information on all 214 individual sites see Table S1. Materials and Methods Fruit from apple, black hawthorn, English ornamental hawthorn, and red hawthorn (native C. macracantha and C. erythropoda, and in one instance a transplanted C. mollis) were collected from both the ground beneath host trees and from the canopies of trees at sites from July to October in 2006, 2009, 2010, and 2011 in eight western states (Table 1; Supp. Table 1, Supp. Fig. 1 [online only]). Collections were aided by the use of U.S. Department of Agriculture (USDA) host plant records to assist in Þnding locations where native hawthorn host plants were documented to occur. Our collections were augmented by previous locality data of known ßy infestation in the PaciÞc Northwest from Yee (2008) and Yee and Goughnour (2008). We also included data from R. pomonella surveys conducted from 2003 to 2008 compiled by the Center of Environmental and Regulatory Information Systems (CERIS) at Purdue University (National Agricultural Pest Information System 2012) based primarily on information of ßy capture on pheromone or sticky traps. Upon collection in the Þeld, fruits were stored either in large plastic containers with lids or in 1-gallon, sealed plastic freezer bags for transport back to the laboratory. Fruit were housed at the USDA Þeld station in Wapato, WA, the Washington State University Research and Extension Unit in Vancouver, WA (now the Clark County Washington 78th street Heritage Farm) or the University of Notre Dame, South Bend, IN. In the laboratory, fruit in plastic bags were transferred to plastic containers similar to those used for the other collections. Two methods were used to monitor fruit collections for ßies. In the Þrst method, the plastic containers with fruit were inspected every other day for R. pomonella larvae that upon Þnishing feeding, had left fruit and formed puparia in the bottom of the containers. The number of pupae from each collection site was recorded on each survey day and ßy pupae immediately frozen at 20 C. In the second method, fruit were placed on top of a layer of moist

5 62 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 1 vermiculite that was used to line the bottom of the plastic containers. The vermiculite was sifted each week for pupae using a ßour sifter. The number of pupae from each collection site was recorded on each survey day and pupae either: 1) immediately frozen at 20 C, or 2) placed in petri-dishes with moist vermiculite and ßies overwintered to adulthood using standard Rhagoletis husbandry methods (Filchak and Feder 1999). To estimate infestation rates at sites as an approximation of population density, the total number of pupae reared from a site was divided by the number of fruits collected the site. At sites with modest numbers of fruit ( 1,000), we individually hand counted fruit to determine sample size. For sites with higher numbers of fruit ( 1,000), we estimated fruit number using a weighting procedure in which the total mass of fruit collected from a site was divided by the mass of 100 randomly chosen fruit weighted from the site using an analytical balance to approximate sample size. In addition to making Þeld collections, we also dissected apple fruit at numerous sites in the vicinity ( 1 km distance) of each infested hawthorn collecting location in the states of Utah, ID, and Wyoming. We conducted these surveys because contrary to other regions of the country, previous studies had reported no R. pomonella infestation of apple in the state of Utah (Alldred and Jorgensen 1993). Dissection involved cutting open a total of 50 apples collected off the ground beneath an apple tree with a paring knife and inspecting the fruit for ßy larvae or the feeding trails left by larvae that are visually apparent within fruit. We surveyed from three to Þve different apple trees in the vicinity of each hawthorn site. Results Overall Geographic Distribution. The distribution of R. pomonella was widespread, yet discontinuous, across the western United States (Fig. 1, Table 1; Supp. Table 1 [online only]). The ßy was primarily found in Þve different areas: 1) in and to the west of the Cascade Mountains in Washington and Oregon; 2) in northeastern Oregon in the vicinity of Hells Canyon; 3) in northern Utah, southeastern Idaho, and southwestern Wyoming; 4) in the eastern foothills of the Rocky Mountains around Boulder, CO; and (5) in western Colorado in the Rocky Mountains (Fig. 1). However, R. pomonella was basically absent from all intervening regions between these Þve areas, including far eastern Washington, northern and central Idaho, and western Montana. We also failed to detect ßies from the Black Hills region of western South Dakota and northeastern Wyoming. The lack of ßies was not because of a shortage of host fruit or from reduced sampling effort in these areas; we found numerous native hawthorn host species suitable for infestation and collected extensive fruit samples across far eastern Washington, northern Idaho, western Montana, and the Black Hills (Table 1; Supp. Table 1 [online only]). There were, however, still gaps in the distribution of native hawthorns in central Washington and Oregon, in much of Montana and Wyoming that extended down into central and southern Idaho, and in Utah, Colorado, and Nevada that could isolate ßies in different regions of the West. The overall patchy distribution of R. pomonella is consistent with the ßy having been introduced, perhaps independently several different times, to the western United States. Distribution in the Pacific Northwest. As previously reported, large populations of R. pomonella were present on the western side of the Cascade Mountain Range through the state of Washington infesting black hawthorn, ornamental hawthorn, and apples (Table 1; Supp. Table 1, Supp. Fig. 1 [online only]). The ßy was also abundant in the Columbia River gorge heading east from Portland, OR, to the town of Klickitat, WA (Table 1; Supp. Table 1, Supp. Fig. 1 [online only]). Although R. pomonella was detected south of Portland in the Wilmette Valley as far down as Cottage Grove, OR, populations of both black hawthorn, C. douglasii (the preferred host in the region), and ßies were spotty and less dense than elsewhere. R. pomonella was also present infesting black hawthorn and apples on the eastern slopes of the Cascade Mountains leading into the central apple growing regions of Washington. However, as has been previously found (Oregon Department of Agriculture Plant Division 2010), the distribution of the ßy was patchy and population densities were relatively low. Infestation was higher on average west of the Cascade Mountains (mean ßy puparia per fruit SE; n 64; range 0Ð3.23) compared with the east side of the mountain range (mean ; n 54; range 0Ð0.0073) and areas of the Mountain West (mean ; n 61; range 0Ð0.3866) (Supp. Table 1 [online only]). We failed to detect R. pomonella from extensive black hawthorn samples collected in more northern areas of central and eastern Washington, as well as in northern Idaho (Fig. 1; Supp. Table 1 [online only]). These samples included sites in the Spokane, WA, area where previous outbreaks of R. pomonella on apple have been reported (AliNiazee and Penrose 1981, Brunner 1987, Tracewski et al. 1987, Yee 2008). Indeed, except for sites west of and on the eastern slopes of the Cascade Mountains, and in the Columbia River Gorge, R. pomonella was absent from much of the remainder of the PaciÞc Northwest. The exception was a series of sites in the Hells Canyon region of northeastern Oregon (Supp. Table 1, Supp. Fig. 1 [online only]), which may be related to an outbreak of the ßy in Pendleton, OR, 2 yr ago (Oregon Department of Agriculture Plant Division Annual Report 2010). The distribution of ßies in the PaciÞc Northwest is therefore disjunct from other western R. pomonella populations. Moreover, we found several areas in the region that contained suitable black hawthorn hosts for attack where R. pomonella was not detected. Taken together, the results imply that R. pomonella is not native and was introduced into the PaciÞc Northwest.

6 January 2013 HOOD ET AL.: DISTRIBUTION OF R. pomonella IN THE WESTERN U.S. 63 Distribution of Flies in Utah, Idaho, and Wyoming. Populations of R. pomonella were found infesting black hawthorn stretching from southeastern Idaho and northwestern Wyoming south through central Utah (Fig. 1). Our records indicate that the southeastern population in Idaho and the northwestern population in Wyoming represent previously undocumented localities for R. pomonella (National Agricultural Pest Information System 2012). Fly densities were generally fairly high for this Utah centered-ßy population (Supp. Table 1 [online only]), with almost 0.3 ßies reared per fruit from a site outside of the city of Springville, UT. In contrast to this Utah centric population that spilled over into parts of southeastern Idaho and northwestern Wyoming, we failed to detect R. pomonella through the remainder of these two states. In Idaho, this included the central Snake River Plain, along the Payette River, and in the Sawtooth and Boise National Forests. Black hawthorn appeared relatively sparse in the central portion of Idaho around the Snake River from Boise to Pocatello. The lack of hawthorn in this area could present a barrier to westward ßy migration from the Utah-centered population to the PaciÞc Northwest. R. pomonella was also absent east of the Washington border moving through the pan handle of northern Idaho, into western Montana (Fig. 1; Supp. Table 1 [online only]). Our surveys also failed to detect ßies infesting red hawthorns in the Black Hills regions of northeastern Wyoming and South Dakota. Similarly, we were unable to locate an apple-infesting population of ßies at any of these areas, including Utah, despite extensive sampling of feral and residential apple, even in the proximity of sites with fairly heavy hawthorn infestations (Supp. Table 1 [online only]). Distribution of Flies in Colorado. We located two populations of R. pomonella in Colorado. One population was found infesting both black hawthorn and red hawthorn (C. macracantha) on the western side of the Rocky Mountain in Collbran 100 km from the ColoradoÐUtah border. Another population was found on the east side of the Rocky Mountains, near Boulder, CO, infesting the red hawthorns C. macracantha, C. erythropoda, and C. mollis (Fig. 1, Table 1). We failed to locate suitable host plants in the central Rocky Mountains areas of Colorado despite records suggesting that red hawthorns may be occasionally present (United States Department of Agriculture 2012). R. pomonella may therefore have a disjunct distribution in Colorado; however, further sampling of hawthorns and apples in the state is needed to conþrm this possibility. Discussion Our results describing the distribution of R. pomonella in the western United States imply that the ßy has a complex history. Although R. pomonella is widespread through much of the northern portion of the western United States, the ßy is nevertheless not continuous in its distribution. Apparent gaps exist between Þve different population pockets of the ßy in the West in: 1) the PaciÞc Northwest; 2) Hells Canyon and vicinity in eastern Oregon; 3) Utah, southeastern Idaho, and southwestern Wyoming; 4) north central Colorado around the city of Boulder; and 5) west central Colorado. In addition, host use patterns for R. pomonella differ across the western United States. In the PaciÞc Northwest primarily in and west of the Cascade Mountains, sympatric populations of ßies occurs that attack black hawthorn, ornamental hawthorn, and apple host plants. However, east of the Cascades and in central Washington, ornamental hawthorns are rare and not infested and black hawthorn infestations are patchy. Further east, in the Mountain West states, we located several discontinuous black hawthorn-infesting populations of R. pomonella, as well as populations infesting red hawthorn. Overall, the spatial and host use patterns in the West are consistent with the hypothesis that R. pomonella was introduced into the PaciÞc Northwest via larvalinfested apples. Densities of the ßy are greatest and populations geographically radiate out from the Portland, OR, area, the hypothesized point of initial introduction (AliNiazee and Penrose 1981). Moreover, the ßy was not detected in our survey from other areas of Washington and Oregon, with the exception of the HellÕs Canyon region, despite suitable native black hawthorn hosts being present. Finally, feral and residential apples are heavily infested in the PaciÞc Northwest, which is not the case elsewhere in the West, as would be predicted if apples from the eastern United States were the source of the original introduction. Thus, commercial fruit growers should probably be most concerned with the movement of infested apples from west of the Cascade Mountains into central apple growing regions of Washington and Oregon. Black and ornamental hawthorn-infesting populations of R. pomonella from an evolutionary standpoint would therefore appear most likely to be newly derived forms (races) of the ßy that shifted from introduced apple populations. These hawthorn hosts can threaten the apple industry. However, the relatively low numbers of these hawthorns and low densities of R. pomonella populations attacking these hosts in central Washington imply that they may be less of a risk than introductions of ßies transported via apple from high density infestations to the west establishing on local feral apples. The underlying cause(s) for R. pomonellaõs presence in other areas of the West besides the PaciÞc Northwest and, in particular, the population in Utah/ Idaho/Wyoming is less clear. Either an independent introduction of the ßy or historical endemism could account for R. pomonellaõs occurrence in Utah/Idaho/ Wyoming. Of important note in this regard is the ßyÕs absence from apple in this region. Previous studies had reported that ßies from Utah do not attack apples (Alldred and Jorgensen 1993). It was hypothesized that this could be because of commercially grown and feral apples in Utah generally being later fruiting, less sweet fall varieties not conducive for larval survivorship. In the current study, we surveyed feral and res-

7 64 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 106, no. 1 idential apples extensively through Utah, dissecting over 50 apple fruit collected at each of over 100 trees in close proximity to (sometimes only a few meters away from) infested black hawthorn trees. Several of these apples were earlier fruiting and sweeter varieties that appeared to be ideal for ßy infestation. Nevertheless, consistent with previous Þndings, we failed to detected R. pomonella infesting apples through Utah/ Idaho/Wyoming. As discussed above, this is not the case elsewhere in the western United States, especially in the PaciÞc Northwest. Although we did not sample infested apples in Colorado in the current study, unlike Utah, there are records of R. pomonella attacking apples in the state (Bush 1966, Foote et al. 1993). Consequently, the apparent inability and/or lack of interest of R. pomonella to attack apples in Utah/Idaho/Wyoming stands in stark contrast to the general situation for the ßy. Therefore, it is conceivable that R. pomonella was not introduced and is endemic to native hawthorns in Utah/Idaho/Wyoming and has not yet evolved to recognize and adapt to using apple as an alternative host. Further studies including behavioral analyses of ßies from Utah/ Idaho/Wyoming assessing their capacity to accept and survive in apples as a host fruit are needed to help resolve this issue. Molecular genetic studies are also warranted to test whether Utah/Idaho/Wyoming ßies are distinct from other R. pomonella populations, as might be predicted if they were endemic to the region. Previous allozyme studies have found that ßies from Utah do differ markedly in allele frequencies for a few loci from other ßies in the western and eastern United States (McPheron 1990). However, the majority of allozymes displayed minimal differences for Utah ßies. These data could be interpreted to represent either the result of a population bottleneck associated with a founder event during introduction or as evidence for endemism. If the latter is true, however, then the Utah population has likely not been isolated for a long period of time from the main body of ßies in the eastern United States after its introduction, given that the majority of allozymes do not show extensive divergence. Clearly, more information is needed to determine the history of the ßy population in Utah/ Idaho/Wyoming. In two areas of Colorado, R. pomonella densities can also be high. The ßy populations in northðcentral and western Colorado appear to be disjunct from each other and from all other R. pomonella populations in the eastern and western United States. In contrast to elsewhere in the western United States, the native red hawthorns C. macracantha and C. erythropoda were the principle hosts for the ßy in the Boulder, CO, area. In addition, we discovered a population of ßies on a transplanted and introduced residential stand of eastern downy hawthorn, C. mollis, in Boulder. Downy hawthorn is the primary host for R. pomonella in the ßyÕs native range in the Midwestern United States (Bush 1966). Thus, it is possible that transplanted downy hawthorn was the source of ßies in the Boulder area, although the stand of C. mollis trees in question were believed by residents to have been planted from seed. Black hawthorn was also attacked extensively in western Colorado along with the native red hawthorn, C. macracantha. Previous R. pomonella outbreaks in apple have also been reported in the literature from Colorado (Bush 1966). The history of the ßy in the region could therefore be explained by past introductions of larval infested apples during the last century, as well. Consistent with this view, the allozyme study of McPheron (1990) found little differentiation between ßies from Collbran, CO, and the eastern United States. In conclusion, the geographic distribution of R. pomonella is consistent with the hypothesis that the ßy was introduced to the PaciÞc Northwest via infested apples. In particular, the general lack of C. douglasiiinfesting R. pomonella east of the Cascade Mountains in the states of Washington, OR, and Idaho implies that the ßy is not native on black hawthorn and is of recent origin. Broader surveying is needed to complete our understanding of the biogeography and evolutionary histories of ßies in the western United States. For example, records of R. pomonella exist from Southern Utah and New Mexico (National Agricultural Pest Information System 2012). We also know that R. pomonella is more or less continuous in the eastern United States (Foote et al. 1993) as far southwest as the Hill Country of Texas (Berlocher and Enquist 1993). In addition, populations of the ßy exist through the Sierra Madre Oriental Mountains and the Altiplano central highland of Mexico (Rull et al. 2006). Resolving how widespread R. pomonella is in the Southwest will complete our understanding of western ßies and help determine the relationship of these populations to those in the northern Rocky Mountain and PaciÞc Northwest regions of the United States, as well as Texas and Mexico. For example, it is conceivable that ßies in New Mexico could represent a corridor through which ßies in Colorado, and possibly Utah/Idaho/Wyoming, spread and/or were introduced from the native range of R. pomonella. Regardless, the current results imply that the ßy does not have a simple history in the western United States. Introductions likely contribute to part of the story (i.e., populations in the PaciÞc Northwest and Colorado), while it is still conceivable that an enclave of R. pomonella centered in northern Utah are endemic or the result of an older more dramatically bottlenecked introduction. Acknowledgments The authors would like to thank Blair Wolßey, Doug Stienbarger, Terry Porter, and Kathleen Rogers and the Clark County Washington 78th street Heritage Farm, the Washington State University Research and Extension Unit, Vancouver, for their support and assistance on the project. G.R.H. would also like to thank Patricia Morton for continuous support and encouragement. This study was funded by grants awarded to G.R.H. from the Entomological Society of America, Sigma Xi, the Indiana Academy of Science, and the National Science Foundation IGERT sponsored GLOBES program at the University of Notre Dame, as well as grants to J.L.F. from the NSF and the U.S. Department of Agricul-

8 January 2013 HOOD ET AL.: DISTRIBUTION OF R. pomonella IN THE WESTERN U.S. 65 ture, and to W.L.Y. by the Washington Tree Fruit Research Commission and Washington State Commission on Pesticide Registration. References Cited AliNiazee, M. T., and R. L. Penrose Apple maggot in Oregon: a possible threat to the Northwest apple industry. Bull. Ecol. Soc. Am. 27: 245Ð246. AliNiazee, M. T., and R. L. Wescott Distribution of the apple maggot Rhagoletis pomonella (Diptera, Tephritidae) in Oregon USA. J. Entomol. Soc. B. C. 83: 54Ð56. Alldred, D. B., and C. D. Jorgensen Hosts, adult emergence, and distribution of the apple maggot (Diptera: Tephritidae) in Utah. Pan-Pac. Entomol. 69: 236Ð246. Berlocher, S. H., and M. Enquist Distribution and host plants of the apple maggot ßy, Rhagoletis pomonella (Diptera: Tephritidae) in Texas. J. Kans. Entomol. 66: 51Ð59. Berlocher, S. H., and J. L. Feder Sympatric speciation in phytophagous insects: moving beyond controversy? Annu. Rev. Entomol. 47: 773Ð815. Boller, E. F., and R. J. Prokopy Bionomics and management of Rhagoletis. Annu. Rev. Entomol. 21: 223Ð246. Brunner, J. F Apple maggot in Washington state: a review with special reference to its status in western states. Melanderia 45: 33Ð51. Bush, G. L The taxonomy, cytology, and evolution of the genus Rhagoletis in North America (Diptera, Tephritidae). Bull. Mus. Comp. Zool. 134: 431Ð562. Cha, D. H., W. L. Yee, R. B. Goughnour, S. B. Sim, T.H.Q. Powell, J. L. Feder, and C. E. Linn IdentiÞcation of host fruit volatiles from domestic apples (Malus domestica), native black hawthorn (Crataegus douglasii) and introduced ornamental hawthorn (C. monogyna) attractive to Rhagoletis pomonella ßies from the western United States. J. Chem. Ecol. 38: 219Ð329. Coyne, J. A., and H. A. Orr Speciation. Sinauer, Sunderland, MA. Dowell, R. V History of apple maggot in the western United States, vol. 3341, p. 95. In R. V. Dowell, L. T. Wilson, and V. P. Jones (eds.), Apple maggot in the West. University of California Division of Agriculture and Natural Resources, Oakland, CA. Filchak, K. E., J. B. Roethele, and J. L. Feder Natural selection and sympatric divergence in the apple maggot, Rhagoletis pomonella. Nature 407: 739Ð742. Foote, R. H., F. L. Blanc, and A. L. Norrbom Handbook of the fruit ßies (Diptera: Tephritidae) of America North of Mexico. Comstock Publishing Associates, Ithaca, NY. Linn, C. E., W. Yee, S. Sim, D. Cha, R. Goughnour, and J. L. Feder Behavioral evidence for fruit odor discrimination and sympatric host races of Rhagoleis pomonella ßies in the western United States. J. Evol. Biol. 25: 961Ð 971. McPheron, B. A Genetic structure of apple maggot ßy (Diptera: Tephritidae) populations. Ann. Entomol. Soc. Am. 83: 568Ð577. Messina, F. J., and V. P. Jones Relationship between fruit phenology and infestation by the apple maggot (Diptera: Tephritidae) in Utah. Ann. Entomol. Soc. Am. 83: 742Ð752. National Agricultural Pest Information System Pest tracker. ( Oregon Department of Agriculture Plant Division Apple maggot program. Oregon Department of Agriculture Plant Division Annual Report, Salem, OR. Prokopy, R. J., D. R. Cooley, W. R. Autio, and W. M. Coli Second-level integrated pest management in commercial apple orchards. Am. J. Altern. Agric. 9: 148Ð156. Rull, J., M. Aluja, J. L. Feder, and S. Berlocher Distribution and host range of hawthorn-infesting Rhagoletis (Diptera: Tephritidae) in Mexico. Ann. Entomol. Soc. Am. 99: 662Ð672. Sim, S., M. Mattsson, J. L. Feder, C. E. Linn, D. Cha, W. Yee, R. Goughour, and J. L. Feder Host fruit odor discrimination behavior of western black hawthorn (Crataegus douglasii)-origin Rhagoletis pomonella ßies in the Þeld: implications for sympatric race formation. Evolution (in press). Tracewski, K. T., J. F. Brunner, S. C. Hoyt, and S. R. Dewey Occurrence of Rhagoletis pomonella (Walsh) in hawthorns, Crataegus, of the PaciÞc Northwest. Melanderia 45: 19Ð25. (USDA) U.S. Department of Agriculture Natural resources conservation services. USDA Plant Database, Urbandale, IA. Yee, W. L Host plant use by apple maggot, western cherry fruit ßy and other Rhagoletis species (Diptera: Tephritidae) in central Washington state. Pan-Pac. Entomol. 84: 163Ð178. Yee, W. L., and R. B. Goughnour Host plant use by the new host records of apple maggot, western cherry fruit ßy and other Rhagoletis species (Diptera: Tephritidae) in western Washington state. Pan-Pac. Entomol. 84: 179Ð193. Received 13 June 2012; accepted 12 October 2012.