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1. History, geography and host use shape genomewide patterns of genetic variation in the redheaded pine sawfly ( Neodiprion lecontei )

   https://doi.org/10.1111/mec.13972  

   Bagley, Robin K. ; Sousa, Vitor C. ; Niemiller, Matthew L. ; Linnen, Catherine R. ( January 2017 , Molecular Ecology)

   Divergent host use has long been suspected to drive population differentiation and speciation in plant‐feeding insects. Evaluating the contribution of divergent host use to genetic differentiation can be difficult, however, as dispersal limitation and population structure may also influence patterns of genetic variation. In this study, we use double‐digest restriction‐associatedDNA(ddRAD) sequencing to test the hypothesis that divergent host use contributes to genetic differentiation among populations of the redheaded pine sawfly (Neodiprion lecontei), a widespread pest that uses multiplePinushosts throughout its range in eastern North America. Because this species has a broad range and specializes on host plants known to have migrated extensively during the Pleistocene, we first assess overall genetic structure using model‐based and model‐free clustering methods and identify three geographically distinct genetic clusters. Next, using a composite‐likelihood approach based on the site frequency spectrum and a novel strategy for maximizing the utility of linkedRADmarkers, we infer the population topology and date divergence to the Pleistocene. Based on existing knowledge ofPinusrefugia, estimated demographic parameters and patterns of diversity among sawfly populations, we propose a Pleistocene divergence scenario forN. lecontei. Finally, using Mantel and partial Mantel tests, we identify a significant relationship between genetic distance and geography in all clusters, and between genetic distance and host use in two of three clusters. Overall, our results indicate that Pleistocene isolation, dispersal limitation and ecological divergence all contribute to genomewide differentiation in this species and support the hypothesis that host use is a common driver of population divergence in host‐specialized insects.

    

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2. 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

   https://doi.org/10.1111/eea.13098  

   Mattsson, Monte ; Hood, Glen Ray ; Yee, Wee L. ; Doellman, Meredith M. ; Bruzzese, Daniel J. ; Goughnour, Robert B. ; Driscoe, Amanda L. ; Van Dexter, Seth ; Tait, Cheyenne ; Glover, Mary M. ; et al ( August 2021 , 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 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.

    

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3. Can the genomics of ecological speciation be predicted across the divergence continuum from host races to species? A case study in Rhagoletis

   https://doi.org/10.1098/rstb.2019.0534  

   Meyers, Peter J. ; Doellman, Meredith M. ; Ragland, Gregory J. ; Hood, Glen R. ; Egan, Scott P. ; Powell, Thomas H. ; Nosil, Patrik ; Feder, Jeffrey L. ( August 2020 , Philosophical Transactions of the Royal Society B: Biological Sciences)

   Studies assessing the predictability of evolution typically focus on short-term adaptation within populations or the repeatability of change among lineages. A missing consideration in speciation research is to determine whether natural selection predictably transforms standing genetic variation within populations into differences between species. Here, we test whether and how host-related selection on diapause timing associates with genome-wide differentiation during ecological speciation by comparing ancestral hawthorn and newly formed apple-infesting host races of Rhagoletis pomonella to their sibling species Rhagoletis mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association study (GWAS) on the hawthorn race strongly predicted the direction and magnitude of genomic divergence among the three fly populations at a field site in Fennville, MI, USA. The apple race and R. mendax show parallel changes in the frequencies of putative inversions on three chromosomes associated with the earlier fruiting times of apples and blueberries compared to hawthorns. A diapause GWAS on R. mendax revealed compensatory changes throughout the genome accounting for the earlier eclosion of blueberry, but not apple flies. Thus, a degree of predictability, although not complete, exists in the genomics of diapause across the ecological speciation continuum in Rhagoletis . The generality of this result is placed in the context of other similar systems. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'. 

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4. Body size as a magic trait in two plant-feeding insect species

   Ashleigh N. Glover, Emily E. ( January 2023 , Evolution)

   When gene flow accompanies speciation, recombination can decouple divergently selected loci and loci conferring reproductive isolation. This barrier to sympatric divergence disappears when assortative mating and disruptive selection involve the same “magic” trait. Although magic traits could be widespread, the relative importance of different types of magic traits to speciation remains unclear. Because body size frequently contributes to host adaptation and assortative mating in plant-feeding insects, we evaluated several magic trait predictions for this trait in a pair of sympatric Neodiprion sawfly species adapted to different pine hosts. A large morphological dataset revealed that sawfly adults from populations and species that use thicker-needled pines are consistently larger than those that use thinner-needled pines. Fitness data from recombinant backcross females revealed that egg size is under divergent selection between the preferred pines. Lastly, mating assays revealed strong size-assortative mating within and between species in three different crosses, with the strongest prezygotic isolation between populations that have the greatest interspecific size differences. Together, our data support body size as a magic trait in pine sawflies and possibly many other plant-feeding insects. Our work also demonstrates how intraspecific variation in morphology and ecology can cause geographic variation in the strength of prezygotic isolation. 

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5. Host plant‐related genomic differentiation in the European cherry fruit fly, Rhagoletis cerasi

   https://doi.org/10.1111/mec.15239  

   Bakovic, Vid ; Schuler, Hannes ; Schebeck, Martin ; Feder, Jeffrey L. ; Stauffer, Christian ; Ragland, Gregory J. ( October 2019 , Molecular Ecology)

   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 F_STvalues 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.

    

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