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Abstract AimAs species' ranges shift poleward in response to anthropogenic change, they may lose antagonistic interactions if they move into less diverse communities, fail to interact with novel populations or species effectively, or if ancestral interacting populations or species fail to shift synchronously. We leveraged a poleward range expansion in a tractable insect host–enemy community to uncover mechanisms by which altered antagonistic interactions between native and recipient communities contributed to ‘high niche opportunities’ (limited biotic resistance) for a range‐expanding insect. LocationNorth America, Pacific Northwest. MethodsWe created quantitative insect host–enemy interaction networks by sampling oak gall wasps on 400 trees of a dominant oak species in the native and expanded range of a range‐expanding gall wasp species. We compared host–enemy network structure between regions. We measured traits (phenology, morphology) of galls and interacting parasitoids, predicting greater trait divergence in the expanded range. We measured function relating to host control and explored if altered interactions and traits contributed to reduced function, or biotic resistance. ResultsInteraction networks had fewer species in the expanded range and lower complementarity of parasitoid assemblages among host species. While networks were more generalized, interactions with the range‐expanding species were more specialized in the expanded range. Specialist enemies effectively tracked the range‐expanding host, and there was reduced apparent competition with co‐occurring hosts by shared generalist enemies. Phenological divergence of enemy assemblages interacting with the range‐expanding and co‐occurring hosts was greater in the expanded range, potentially contributing to weak apparent competition. Biotic resistance was lower in the expanded range, where fewer parasitoids emerged from galls of the range‐expanding host. Main ConclusionsChanges in interactions with generalist enemies created high niche opportunities, and limited biotic resistance, suggesting weak apparent competition may be a mechanism of enemy release for range‐expanding insects embedded within generalist enemy networks. 

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'. 

Many organisms enter a dormant state in their life cycle to deal with predictable changes in environments over the course of a year. The timing of dormancy is therefore a key seasonal adaptation, and it evolves rapidly with changing environments. We tested the hypothesis that differences in the timing of seasonal activity are driven by differences in the rate of development during diapause in Rhagoletis pomonella , a fly specialized to feed on fruits of seasonally limited host plants. Transcriptomes from the central nervous system across a time series during diapause show consistent and progressive changes in transcripts participating in diverse developmental processes, despite a lack of gross morphological change. Moreover, population genomic analyses suggested that many genes of small effect enriched in developmental functional categories underlie variation in dormancy timing and overlap with gene sets associated with development rate in Drosophila melanogaster . Our transcriptional data also suggested that a recent evolutionary shift from a seasonally late to a seasonally early host plant drove more rapid development during diapause in the early fly population. Moreover, genetic variants that diverged during the evolutionary shift were also enriched in putative cis regulatory regions of genes differentially expressed during diapause development. Overall, our data suggest polygenic variation in the rate of developmental progression during diapause contributes to the evolution of seasonality in R. pomonella . We further discuss patterns that suggest hourglass-like developmental divergence early and late in diapause development and an important role for hub genes in the evolution of transcriptional divergence. 

Abstract For insect species in temperate environments, seasonal timing is often governed by the regulation of diapause, a complex developmental programme that allows insects to weather unfavourable conditions and synchronize their life cycles with available resources. Diapause development consists of a series of distinct phases including initiation, maintenance, termination and post‐diapause development. The evolution of insect seasonal timing depends in part on how these phases of diapause development and post‐diapause development interact to affect variation in phenology. Here, we dissect the physiological basis of a recently evolved phenological shift inRhagoletis pomonella(Diptera: Tephritidae), a model system for ecological divergence. A recently derived population ofR. pomonellashifted from specializing on native hawthorn fruit to earlier fruiting introduced apples, resulting in a 3–4 week shift in adult emergence timing. We tracked metabolic rates of individual flies across post‐winter development to test which phases of development may act either independently or in combination to contribute to this recently evolved divergence in timing. Apple and hawthorn flies differed in a number of facets of their post‐winter developmental trajectories. However, divergent adaptation in adult emergence phenology in these flies was due almost entirely to the end of the pupal diapause maintenance phase, with post‐diapause development having a very small effect. The relatively simple underpinnings of variation in adult emergence phenology suggest that further adaptation to seasonal change in these flies for this trait might be largely due to the timing of diapause termination unhindered by strong covariance among different components of post‐diapause development. 

Abstract Adaptation to novel environments can result in unanticipated genomic responses to selection. Here, we illustrate how multifarious, correlational selection helps explain a counterintuitive pattern of genetic divergence between the recently derived apple‐ and ancestral hawthorn‐infesting host races ofRhagoletis pomonella(Diptera: Tephritidae). The apple host race terminates diapause and emerges as adults earlier in the season than the hawthorn host race, to coincide with the earlier fruiting phenology of their apple hosts. However, alleles at many loci associated with later emergence paradoxically occur at higher frequencies in sympatric populations of the apple compared to the hawthorn race. We present genomic evidence that historical selection over geographically varying environmental gradients across North America generated genetic correlations between two life history traits, diapause intensity and diapause termination, in the hawthorn host race. Moreover, the loci associated with these life history traits are concentrated in genomic regions in high linkage disequilibrium (LD). These genetic correlations are antagonistic to contemporary selection on local apple host race populations that favours increased initial diapause depth and earlier, not later, diapause termination. Thus, the paradox of apple flies appears due, in part, to pleiotropy or linkage of alleles associated with later adult emergence and increased initial diapause intensity, the latter trait strongly selected for by the earlier phenology of apples. Our results demonstrate how understanding of multivariate trait combinations and the correlative nature of selective forces acting on them can improve predictions concerning adaptive evolution and help explain seemingly counterintuitive patterns of genetic diversity in nature.