Limited genetic evidence for host plant‐related differentiation in the Western cherry fruit fly, Rhagoletis indifferens

Abstract

The shift of the fruit fly Rhagoletis pomonella (Walsh) in the mid-1800s from downy hawthorn, Crataegus mollis (Torrey & Asa Gray) Scheele, to introduced domesticated apple, Malus domestica (Borkhausen), in the eastern USA is a model for ecological divergence with gene flow. A similar system may exist in the northwestern USA and British Columbia, Canada, where Rhagoletis indifferens Curran (Diptera: Tephritidae) attacks the native bitter cherry Prunus emarginata (Douglas ex Hooker) Eaton (Rosaceae). Populations of R. indifferens have shifted and became economic pests on domesticated sweet cherry, Prunus avium (L.) L., shortly after sweet cherries were introduced to the region in the mid-1800s. The fruiting phenologies of the two cherries differ in a similar manner as apples and hawthorns, with domesticated sweet cherries typically ripening in June and July, and bitter cherries in July and August. Here we report, however, little evidence for genetic differentiation between bitter vs. sweet cherry populations of R. indifferens or for pronounced genetic associations between allele frequencies and adult eclosion time, as has been documented for apple and downy hawthorn flies. The current findings support a previous more geographically limited survey of R. indifferens in the province of British Columbia, Canada, and an analysis of its sister species, R. cingulata, in the state of Michigan, USA, implying a lack of host-related differentiation for flies infesting different cherry host plants. Possible causes for why host races are readily genetically detected for R. pomonella but not for R. indifferens are discussed.

Geographic and Ecological Dimensions of Host Plant-Associated Genetic Differentiation and Speciation in the Rhagoletis cingulata (Diptera: Tephritidae) Sibling Species Group

“…In this regard, the nuclear-encoded microsatellites imply that host association significantly affects patterns of genetic divergence and, by inference, generates ecologically based RI and induces speciation in R. cingulata group flies (Figure 2 and Figure 3; Table 2). In previous studies, Maxwell et al [25], Smith et al [24] and Saint Jean et al [26] found little evidence for genetic differentiation between native and domesticated cherry-infesting populations of R. cingulata or R. indifferens . However, here we have shown that genetically distinct forms of R. cingulata group flies exist on non-cherry host plants, including native olives and muttonwood, in areas of geographic overlap (sympatry) with the cherry-infesting species R. cingulata .…”

“…Fruits infested with larvae of R. cingulata species group flies were collected from 2004–2012 at sites across North America (Figure 1, Table 1). Microsatellite and mtDNA data for R. indifferens and R. cingulata were taken from Saint Jean et al [26] and Doellman et al [36]. New microsatellite and mtDNA sequencing data in the current study were generated from three non-cherry-infesting populations of R. cingulata group flies: R. chionanthi (site 18, collected from fringe-tree at Perry, Georgia), R. osmanthi (site 19, collected from tea-olive at Lake Lizzie, Florida), and R. turpiniae (site 20, collected from muttonwood at Xalapa, Veracruz, Mexico).…”

“…The 21 microsatellites were chosen because they displayed no systematic evidence for heterozygote deficiency from Hardy–Weinberg equilibrium due to null alleles, as determined using MICRO-CHECKER [47]. Genotyping was performed on a Beckman–Coulter CEQ8000, as described in Saint Jean et al [26]. Microsatellite alleles were sized using the Fragment Analysis software provided by Beckman–Coulter (Brea, CA, USA).…”

“…Thus, cherry host affiliation may not be a strong barrier to gene flow between R. cingulata and R. indifferens if the two taxa come in contact. Microsatellite studies of R. cingulata [24] and R. indifferens [25,26] have also found little evidence for host-related differentiation between populations of these species attacking sweet or tart cherries versus their respective native cherry trees. Additionally, studies of non-host related RI reported only modest levels of premating isolation between R. cingulata and R. indifferens (isolation index = 0.27; [27]).…”

Evidence for spatial clines and mixed geographic modes of speciation for North American cherry‐infesting Rhagoletis (Diptera: Tephritidae) flies

“…Genotyping was performed as described in Saint Jean et al. (2018), with size standards included in each genotyper run, as well as representative eastern R. cingulata and western R. indifferens , to ensure that alleles were properly aligned and comparably scored. Details of the methods used for microsatellite data analysis are given in the .…”