Field cricket genome reveals the footprint of recent, abrupt adaptation in the wild: Letter

Sonia Pascoal, Judith E. Risse, Xiao Zhang, Mark Blaxter, Timothee Cezard, Richard J. Challis, Karim Gharbi, John Hunt, Sujai Kumar, Emma Langan, Xuan Liu, Jack G. Rayner, Michael G. Ritchie, Basten L. Snoek, Urmi Trivedi, Nathan W. Bailey (Corresponding author)

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Abstract

Abstract Evolutionary adaptation is generally thought to occur through incremental mutational steps, but large mutational leaps can occur during its early stages. These are challenging to study in nature due to the difficulty of observing new genetic variants as they arise and spread, but characterizing their genomic dynamics is important for understanding factors favoring rapid adaptation. Here, we report genomic consequences of recent, adaptive song loss in a Hawaiian population of field crickets (Teleogryllus oceanicus). A discrete genetic variant, flatwing, appeared and spread approximately 15 years ago. Flatwing erases sound-producing veins on male wings. These silent flatwing males are protected from a lethal, eavesdropping parasitoid fly. We sequenced, assembled and annotated the cricket genome, produced a linkage map, and identified a flatwing quantitative trait locus covering a large region of the X chromosome. Gene expression profiling showed that flatwing is associated with extensive genome-wide effects on embryonic gene expression. We found that flatwing male crickets express feminized chemical pheromones. This male feminizing effect, on a different sexual signaling modality, is genetically associated with the flatwing genotype. Our findings suggest that the early stages of evolutionary adaptation to extreme pressures can be accompanied by greater genomic and phenotypic disruption than previously appreciated, and highlight how abrupt adaptation might involve suites of traits that arise through pleiotropy or genomic hitchhiking.
Original languageEnglish
Pages (from-to)19-33
JournalEvolution Letters
VolumeOnline
Early online date19 Dec 2019
DOIs
Publication statusPublished - 2020

Keywords

  • international
  • feminization
  • genomics
  • rapid evolution
  • sexual signaling
  • trait loss
  • Adaptation
  • Plan_S-Compliant_OA

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    Pascoal, S., Risse, J. E., Zhang, X., Blaxter, M., Cezard, T., Challis, R. J., Gharbi, K., Hunt, J., Kumar, S., Langan, E., Liu, X., Rayner, J. G., Ritchie, M. G., Snoek, B. L., Trivedi, U., & Bailey, N. W. (2020). Field cricket genome reveals the footprint of recent, abrupt adaptation in the wild: Letter. Evolution Letters, Online, 19-33. https://doi.org/10.1002/evl3.148