An official website of the United States government
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.
more »
« less
Identifying Diagnostic Genetic Markers for a Cryptic Invasive Agricultural Pest: A Test Case Using the Apple Maggot Fly (Diptera: Tephritidae)
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.
more »
« less
- Award ID(s):
- 1638997
- PAR ID:
- 10188260
- Date Published:
- Journal Name:
- Annals of the Entomological Society of America
- Volume:
- 113
- Issue:
- 4
- ISSN:
- 0013-8746
- Page Range / eLocation ID:
- 246 to 256
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Schilder, Rudolf (Ed.)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.more » « less
-
Abstract Elucidating the mechanisms and conditions facilitating the formation of biodiversity are central topics in evolutionary biology. A growing number of studies imply that divergent ecological selection may often play a critical role in speciation by counteracting the homogenising effects of gene flow. Several examples involve phytophagous insects, where divergent selection pressures associated with host plant shifts may generate reproductive isolation, promoting speciation. Here, we use ddRADseq to assess the population structure and to test for host‐related genomic differentiation in the European cherry fruit fly,Rhagoletis cerasi(L., 1758) (Diptera: Tephritidae). This tephritid is distributed throughout Europe and western Asia, and has adapted to two different genera of host plants,Prunusspp. (cherries) andLoniceraspp. (honeysuckle). Our data imply that geographic distance and geomorphic barriers serve as the primary factors shaping genetic population structure across the species range. Locally, however, flies genetically cluster according to host plant, with consistent allele frequency differences displayed by a subset of loci betweenPrunusandLoniceraflies across four sites surveyed in Germany and Norway. These 17 loci display significantly higher FSTvalues between host plants than others. They also showed high levels of linkage disequilibrium within and betweenPrunusandLoniceraflies, supporting host‐related selection and reduced gene flow. Our findings support the existence of sympatric host races inR. cerasiembedded within broader patterns of geographic variation in the fly, similar to the related apple maggot,Rhagoletis pomonella, in North America.more » « less
-
null (Ed.)Changes in behaviour often drive rapid adaptive evolution and speciation. However, the mechanistic basis for behavioural shifts is largely unknown. The tephritid fruit fly Rhagoletis pomonella is an example of ecological specialization and speciation in action via a recent host plant shift from hawthorn to apple. These flies primarily use specific odours to locate fruit, and because they mate only on or near host fruit, changes in odour preference for apples versus hawthorns translate directly to prezygotic reproductive isolation, initiating speciation. Using a variety of techniques, we found a reversal between apple and hawthorn flies in the sensory processing of key odours associated with host fruit preference at the first olfactory synapse, linking changes in the antennal lobe of the brain with ongoing ecological divergence. Indeed, changes to specific neural pathways of any sensory modality may be a broad mechanism for changes in animal behaviour, catalysing the genesis of new biodiversity.more » « less
-
Abstract Parasitoid wasps are among the most speciose animals, yet have relatively few available genomic resources. We report a draft genome assembly of the wasp Diachasma alloeum (Hymenoptera: Braconidae), a host-specific parasitoid of the apple maggot fly Rhagoletis pomonella (Diptera: Tephritidae), and a developing model for understanding how ecological speciation can “cascade” across trophic levels. Identification of gene content confirmed the overall quality of the draft genome, and we manually annotated ∼400 genes as part of this study, including those involved in oxidative phosphorylation, chemosensation, and reproduction. Through comparisons to model hymenopterans such as the European honeybee Apis mellifera and parasitoid wasp Nasonia vitripennis, as well as a more closely related braconid parasitoid Microplitis demolitor, we identified a proliferation of transposable elements in the genome, an expansion of chemosensory genes in parasitoid wasps, and the maintenance of several key genes with known roles in sexual reproduction and sex determination. The D. alloeum genome will provide a valuable resource for comparative genomics studies in Hymenoptera as well as specific investigations into the genomic changes associated with ecological speciation and transitions to asexuality.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/aesa/saz069
