Evidence for adaptation of Rhagoletis pomonella (Diptera: Tephritidae) on large-thorn hawthorn, Crataegus macracantha, in Okanogan County, Washington State, USA

Abstract

The apple maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), was introduced from eastern North America into western North America via infested apples (Malus domestica Borkhausen) about 44 yr ago, where it subsequently adapted to 2 hawthorn species, Crataegus douglasii Lindley and C. monogyna Jacquin. Here, we test whether R. pomonella has also adapted to large-thorn hawthorn, Crataegus macracantha Loddiges ex Loudon, in Okanogan County, Washington State, USA. In 2020, 2021, and 2022, fruit of C. macracantha were shown to ripen in late September and were infested at rates from 0.7% to 3.0%. In laboratory rearing studies, large-thorn hawthorn flies from C. macracantha eclosed on average 9–19 days later than apple flies from earlier ripening apple (August–early September), consistent with large-thorn hawthorn flies having adapted to the later fruiting phenology of its host. In a laboratory no-choice test, significantly fewer (64.8%) large-thorn hawthorn than apple flies visited apples. In choice tests, greater percentages of large-thorn hawthorn than apple flies resided on and oviposited into C. macracantha versus apple fruit. Large-thorn hawthorn flies were also smaller in size than apple flies. Our results provide further support for the recursive adaptation hypothesis that R. pomonella has rapidly and independently specialized phenologically and behaviorally to different novel hawthorn hosts since its introduction into the Pacific Northwest of the USA, potentially leading to host race formation.

Abundances, ecologies, and distributions of Rhagoletis Loew, 1862 (Diptera: Tephritidae) flies in central Washington State, U.S.A. inferred from fly trapping surveys

“…We did not separate between/among species of native hawthorns in the survey, but we found C. douglasii in Yakima, Chelan, and Okanogan Counties, whereas among the three counties we found C. macracantha only in Okanogan County. There, C. macracantha was more heavily infested than C. douglasii (Yee et al 2023), disproportionately contributing to the overall greater relative abundance of R. pomonella caught in native hawthorns (4.1%) than other host trees (≤ 1.3%). The preponderance of R. pomonella catches on native hawthorns in Okanogan County occurred in September, indicating surveyed trees there were mostly C. macracantha, which has late-ripening fruit that support late-eclosing flies (Yee et al 2023).…”

“…macracantha only in Okanogan County. There, C. macracantha was more heavily infested than C. douglasii (Yee et al 2023), disproportionately contributing to the overall greater relative abundance of R . pomonella caught in native hawthorns (4.1%) than other host trees (≤ 1.3%).…”

“…The preponderance of R . pomonella catches on native hawthorns in Okanogan County occurred in September, indicating surveyed trees there were mostly C. macracantha , which has late-ripening fruit that support late-eclosing flies (Yee et al 2023).…”

Conserved cold tolerance of Rhagoletis species from different host fruits and elevations in Colorado, USA

“…This relationship is maintained even when apple and hawthorn populations are overwintered under common conditions in the laboratory (Feder et al, 1993;Smith, 1988) and is driving speciation between sympatric populations of apple-and hawthorn-infesting R. pomonella (Dowle et al, 2020;Filchak et al, 2000;Ragland et al, 2017). The duration of cold exposure also impacts developmental timing, with longer chilling of pupae resulting in faster completion of post-chill eclosion and apple flies eclosing faster than hawthorn flies (Dambroski & Feder, 2007;Feder et al, 1997;Toxopeus et al, 2024;Yee et al, 2023). We have recently observed Rhagoletis flies infesting introduced (non-native) crabapple with fruiting phenology that overlaps with sympatric hawthorn trees (see Section 2), providing an opportunity to examine the impact of a rare host fruit on R. pomonella life history timing and cold tolerance.…”

Conserved cold tolerance ofRhagoletisspecies from different host fruits, elevations in Colorado, USA

“…This relationship is maintained even when apple and hawthorn populations are overwintered under common conditions in the laboratory (Feder et al, 1993; Smith, 1988) and is driving speciation between sympatric populations of apple- and hawthorn-infesting R. pomonella (Dowle et al, 2020; Filchak et al, 2000; Ragland et al, 2017). The duration of cold exposure also impacts developmental timing, with longer chilling of pupae resulting in faster completion of post-chill eclosion, with apple flies eclosing faster than hawthorn flies (Dambroski and Feder, 2007; Feder et al, 1997; Toxopeus et al, 2023; Yee et al, 2023). We have recently observed Rhagoletis flies infesting introduced (non-native) crabapple with fruiting phenology that overlaps with sympatric hawthorn trees (see Methods), providing an opportunity to examine the impact of a rare host fruit on R. pomonella life history timing and cold tolerance.…”