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Abstract Parasitoids comprise a speciose insect group, displaying a wide array of life history strategies. In the Pacific Northwest of the United States, the tephritid fruit flies Rhagoletis tabellaria (Fitch) and Rhagoletis indifferens Curran infest red osier dogwood, Cornus sericea L. (Cornaceae), and bitter cherry, Prunus emarginata (Douglas ex Hooker) Eaton (Rosaceae), respectively. The flies are parasitized by different braconid wasps at different life stages; Utetes tabellariae (Fischer) oviposits into R. tabellaria eggs, whereas Diachasma muliebre (Muesebeck) oviposits into R. indifferens larvae feeding in cherries. Because Rhagoletis only have one major generation a year and the wasps attack temporally distinct fly life stages, we predicted that eclosion times of U. tabellariae should more closely follow that of its host than the larval-attacking D. muliebre. As predicted, U. tabellariae eclosed on average 6.0–12.5 d later than R. tabellaria, whereas D. muliebre eclosed on average 32.1 d after R. indifferens. Unexpectedly, however, longer chill duration differentially affected the systems; longer overwinters minimally influenced eclosion times of R. tabellaria and U. tabellariae but caused earlier eclosion of both R. indifferens and D. muliebre. Results imply that in temperate regions, diapause timing in braconid wasps evolves in response to both host life stage attacked and fly eclosion characteristics, possibly reflecting differential effects of winter on host plant fruiting phenology. Differences in phenological sensitivity of the lower host plant trophic level to variation in environmental conditions may have cascading effects, sequentially and differentially affecting eclosion times in higher frugivore (fly) and parasitoid (wasp) trophic levels. 

Abstract Closely related phytophagous insects that specialize on different host plants may have divergent responses to environmental factors. Rhagoletis pomonella (Walsh) and Rhagoletis zephyria Snow (Diptera: Tephritidae) are sibling, sympatric fly species found in western North America that attack and mate on plants of Rosaceae (~60 taxa) and Caprifoliaceae (three taxa), respectively, likely contributing to partial reproductive isolation. Rhagoletis zephyria evolved from R. pomonella and is native to western North America, whereas R. pomonella was introduced there. Given that key features of the flies’ ecology, breeding compatibility, and evolution differ, we predicted that adult eclosion patterns of the two flies from Washington State, USA are also distinct. When puparia were chilled, eclosion of apple- and black hawthorn-origin R. pomonella was significantly more dispersed, with less pronounced peaks, than of snowberry-origin R. zephyria within sympatric and nonsympatric site comparisons. Percentages of chilled puparia that produced adults were ≥67% for both species. However, when puparia were not chilled, from 13.5 to 21.9% of apple-origin R. pomonella versus only 1.2% to 1.9% of R. zephyria eclosed. The distinct differences in eclosion traits of R. pomonella and R. zephyria could be due to greater genetic variation in R. pomonella, associated with its use of a wider range of host plants than R. zephyria. 

Abstract Insect pests destroy ~15% of all U.S. crops, resulting in losses of $15 billion annually. Thus, developing cheap, quick, and reliable methods for detecting harmful species is critical to curtail insect damage and lessen economic impact. The apple maggot fly, Rhagoletis pomonella, is a major invasive pest threatening the multibillion-dollar apple industry in the Pacific Northwest United States. The fly is also sympatric with a benign but morphologically similar and genetically closely related species, R. zephyria, which attacks noncommercial snowberry. Unambiguous species identification is essential due to a zero-infestation policy of apple maggot for fruit export. Mistaking R. zephyria for R. pomonella triggers unnecessary and costly quarantines, diverting valuable control resources. Here we develop and apply a relatively simple and cost-effective diagnostic approach using Illumina sequencing of double-digest restriction site-associated DNA markers. We identified five informative single-nucleotide polymorphisms (SNPs) and designed a diagnostic test based on agarose gel electrophoresis of restriction enzyme-digested polymerase chain reaction amplification products (RFLPs) to distinguish fly species. We demonstrated the utility of this approach for immediate, 1-d species identification by scoring apple- and snowberry-infesting flies from known hosts, reared from fruit collected at 11 sites throughout Washington. However, if immediate diagnosis is not required, or hundreds to thousands of specimens must be assessed, then a direct Illumina-based sequencing strategy, similar to that used here for diagnostic SNP identification, can be powerful and cost-effective. The genomic strategy we present is effective for R. pomonella and also transferable to many cryptic pests. 

Abstract 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 domesticaBorkh.) 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 douglasiiLindl.) and an introduced species (Crataegus monogynaJacq.) – 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 thatR. pomonellacan 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. 

Abstract An important criterion for understanding speciation is the geographic context of population divergence. Three major modes of allopatric, parapatric, and sympatric speciation define the extent of spatial overlap and gene flow between diverging populations. However, mixed modes of speciation are also possible, whereby populations experience periods of allopatry, parapatry, and/or sympatry at different times as they diverge. Here, we report clinal patterns of variation for 21 nuclear‐encoded microsatellites and a wing spot phenotype for cherry‐infestingRhagoletis(Diptera: Tephritidae) across North America consistent with these flies having initially diverged in parapatry followed by a period of allopatric differentiation in the early Holocene. However, mitochondrial DNA (mtDNA) displays a different pattern; cherry flies at the ends of the clines in the eastern USA and Pacific Northwest share identical haplotypes, while centrally located populations in the southwestern USA and Mexico possess a different haplotype. We hypothesize that the mitochondrial difference could be due to lineage sorting but more likely reflects a selective sweep of a favorable mtDNA variant or the spread of an endosymbiont. The estimated divergence time for mtDNA suggests possible past allopatry, secondary contact, and subsequent isolation between USA and Mexican fly populations initiated before the Wisconsin glaciation. Thus, the current genetics of cherry flies may involve different mixed modes of divergence occurring in different portions of the fly's range. We discuss the need for additional DNA sequencing and quantification of prezygotic and postzygotic reproductive isolation to verify the multiple mixed‐mode hypothesis for cherry flies and draw parallels from other systems to assess the generality that speciation may commonly involve complex biogeographies of varying combinations of allopatric, parapatric, and sympatric divergence.