Recursive Adaptation in Action: Allochronic Isolation and Divergence of Host-Associated Populations of the Apple Maggot Fly, Rhagoletis Pomonella, Following Its Recent Introduction to the Western USA
We thank the Clark County Washington 78th Street Heritage Farm, the Washington State University Research and Extension Unit (Vancouver, WA, USA), Blair Wolfley, Doug Stienbarger, Terry Porter, and Kathleen Rogers, and especially Patricia Morton for their support and assistance. This work was supported by grants to JLF, SPE, and GRH from the NSF, USDA, and the University of Notre Dame Environmental Change Initiative and Advanced Diagnostics and Therapeutics Initiative, to MM from the American Museum of Natural History’s Theodore Roosevelt Memorial Grant and Portland State University’s Forbes Lea Fund for Student Research, and to WLY by the Washington Tree Fruit Research Commission and Washington State Commission on Pesticide Registration.
Entomologia Experimentalis Et Applicata
An outstanding issue in the study of insect host races concerns the idea of ‘recursive adaptive divergence’, whereby adaptation can occur repeatedly across space and/or time, and the most recent adaptive episode is defined by one or more previously similar cases. The host plant shift of the apple maggot fly, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae, Carpomyini), from ancestral downy hawthorn [Crataegus mollis (Torr. & A. Gray) Scheele] to introduced, domesticated apple (Malus domestica Borkh.) in the eastern USA has long served as a model system for investigating ecologically driven host race formation in phytophagous insect specialists. Here, we report results from an annual geography survey of eclosion time demonstrating a similar ecological pattern among nascent host-associated populations of the fly recently introduced ca. 40 years ago from its native range in the east into the Pacific Northwest (PNW) region of the USA. Specifically, using data collected from 25 locations across 5 years, we show that apple-infesting fly populations in the PNW have rapidly and repeatedly shifted (and maintained differences in) their adult eclosion life-history timing to infest two novel hawthorn hosts with different fruiting phenologies – a native species (Crataegus douglasii Lindl.) and an introduced species (Crataegus monogyna Jacq.) – generating partial allochronic reproductive isolation in the process. The shifts in the PNW parallel the classic case of host race formation in the eastern USA, but have occurred bi-directionally to two hawthorn species with phenologies slightly earlier (black hawthorn) and significantly later (ornamental hawthorn) than apple. Our results imply that R. pomonella can both possess and retain extensive-standing variation (i.e., ‘adaptive memory’) in diapause traits, even following introductions, to rapidly and temporally track novel phenological host opportunities when they arise. Thus, ‘specialized’ host races may not constitute evolutionary dead ends. Rather, adaptive phenotypic and genetic memory may carry over from one host shift to the next, recursively facilitating host race formation in phytophagous insects.
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Mattsson, M., Hood, G. R., Yee, W. L., Doellman, M. M., Bruzzese, D. J., Goughnour, R. B., Driscoe, A. L., Van Dexter, S., Tait, C., Glover, M. M., Meyers, P., Ruedas, L. A., & Feder, J. L. (2021). Recursive adaptation in action: allochronic isolation and divergence of host‐associated populations of the apple maggot fly, Rhagoletis pomonella , following its recent introduction to the western USA. Entomologia Experimentalis Et Applicata, eea.13098. https://doi.org/10.1111/eea.13098