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  1. Genome re-arrangements such as chromosomal inversions are often involved in adaptation. As such, they experience natural selection, which can erode genetic variation. Thus, whether and how inversions can remain polymorphic for extended periods of time remains debated. Here we combine genomics, experiments, and evolutionary modeling to elucidate the processes maintaining an inversion polymorphism associated with the use of a challenging host plant (Redwood trees) inTimemastick insects. We show that the inversion is maintained by a combination of processes, finding roles for life-history trade-offs, heterozygote advantage, local adaptation to different hosts, and gene flow. We use models to show how such multi-layered regimes of balancing selection and gene flow provide resilience to help buffer populations against the loss of genetic variation, maintaining the potential for future evolution. We further show that the inversion polymorphism has persisted for millions of years and is not a result of recent introgression. We thus find that rather than being a nuisance, the complex interplay of evolutionary processes provides a mechanism for the long-term maintenance of genetic variation.

     
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    Free, publicly-accessible full text available June 20, 2024
  2. Host shifts are considered a key generator of insect biodiversity. For insects, adaptation to new host plants often requires changes in larval/pupal development and adult behavioural preference toward new hosts. Neurochemicals play key roles in both development and behaviour and therefore provide a potential source for such synchronization. Here, we correlated life-history timing, brain development and corresponding levels of 14 neurochemicals in Rhagoletis pomonella (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. These races exhibit differences in pupal diapause timing as well as adult behavioural preference with respect to their hosts. This difference in behavioural preference is coupled with differences in neurophysiological response to host volatiles. We found that apple race pupae exhibited adult brain morphogenesis three weeks faster after an identical simulated winter than the hawthorn race, which correlated with significantly lower titres of several neurochemicals. In some cases, particularly biogenic amines, differences in titres were reflected in the mature adult stage, when host preference is exhibited. In summary, life-history timing, neurochemical titre and brain development can be coupled in this speciating system, providing new hypotheses for the origins of new species through host shifts. 
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  3. Identifying the genetic basis of adaptation is a central goal of evolutionary biology. However, identifying genes and mutations affecting fitness remains challenging because a large number of traits and variants can influence fitness. Selected phenotypes can also be difficult to know a priori , complicating top–down genetic approaches for trait mapping that involve crosses or genome-wide association studies. In such cases, experimental genetic approaches, where one maps fitness directly and attempts to infer the traits involved afterwards, can be valuable. Here, we re-analyse data from a transplant experiment involving Timema stick insects, where five physically clustered single-nucleotide polymorphisms associated with cryptic body coloration were shown to interact to affect survival. Our analysis covers a larger genomic region than past work and revealed a locus previously not identified as associated with survival. This locus resides near a gene, Punch ( Pu ) , involved in pteridine pigments production, implying that it could be associated with an unmeasured coloration trait. However, by combining previous and newly obtained phenotypic data, we show that this trait is not eye or body coloration. We discuss the implications of our results for the discovery of traits, genes and mutations associated with fitness in other systems, as well as for supergene evolution. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’. 
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  4. Our ability to predict natural phenomena can be limited by incomplete information. This issue is exemplified by `Laplace's demon', an imaginary creature proposed in the 18th century, who knew everything about everything, and thus could predict the full nature of the universe forward or backward in time. Quantum mechanics, among other things, has cast doubt on the possibility of Laplace's demon in the full sense, but the idea still serves as a useful metaphor for thinking about the extent to which prediction is limited by incomplete information on deterministic processes versus random factors. Here we use simple analytical models and computer simulations to illustrate how data limits can be captured in a Bayesian framework, and how they influence our ability to predict evolution. We show how uncertainty in measurements of natural selection, or low predictability of external environmental factors affecting selection, can greatly reduce predictive power, often swamping the influence of intrinsic randomness caused by genetic drift. Thus, more accurate knowledge concerning the causes and action of natural selection is key to improving prediction. Fortunately, our analyses and simulations show quantitatively that reasonable improvements in data quantity and quality can meaningfully increase predictability. 
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  5. Schilder, Rudolf (Ed.)
    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. 
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  6. Abstract

    Climate change may alter phenology within populations with cascading consequences for community interactions and on‐going evolutionary processes. Here, we measured the response to climate warming in two sympatric, recently diverged (~170 years) populations ofRhagoletis pomonellaflies specialized on different host fruits (hawthorn and apple) and their parasitoid wasp communities. We tested whether warmer temperatures affect dormancy regulation and its consequences for synchrony across trophic levels and temporal isolation between divergent populations. Under warmer temperatures, both fly populations developed earlier. However, warming significantly increased the proportion of maladaptive pre‐winter development in apple, but not hawthorn, flies. Parasitoid phenology was less affected, potentially generating ecological asynchrony. Observed shifts in fly phenology under warming may decrease temporal isolation, potentially limiting on‐going divergence. Our findings of complex sensitivity of life‐history timing to changing temperatures predict that coming decades may see multifaceted ecological and evolutionary changes in temporal specialist communities.

     
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  7. null (Ed.)