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

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Pascoal_2019_EL_Fieldcricket_CC.pdf (1.183Mb)
Date
07/02/2020
Author
Pascoal, Sonia
Risse, Judith E.
Zhang, Xiao
Blaxter, Mark
Cezard, Timothee
Challis, Richard J.
Gharbi, Karim
Hunt, John
Kumar, Sujai
Langan, Emma
Liu, Xuan
Rayner, Jack G.
Ritchie, Michael G.
Snoek, Basten L.
Trivedi, Urmi
Bailey, Nathan William
Keywords
Adaptation
Feminization
Genomics
Rapid evolution
Sexual signaling
Trait loss
QH301 Biology
3rd-DAS
BDC
R2C
Metadata
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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.
Citation
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 ' , Evolution Letters , vol. 4 , no. 1 , pp. 19-33 . https://doi.org/10.1002/evl3.148
Publication
Evolution Letters
Status
Peer reviewed
DOI
https://doi.org/10.1002/evl3.148
ISSN
2056-3744
Type
Journal article
Rights
Copyright © 2019 The Author(s). Evolution Letters published by Wiley Periodicals, Inc. on behalf of Society for the Study of Evolution (SSE) and European Society for Evolutionary Biology (ESEB). This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
Description
The Natural Environment Research Council provided funding to N.W.B. (NE/G014906/1, NE/L011255/1) and to N.W.B. and M.G.R. (NE/1027800/1). Sequencing was provided by Edinburgh Genomics and the Centre for Genomic Research (University of Liverpool). Bioinformatics resources at St Andrews were funded by the Wellcome Trust (105621/Z/14/Z). Support from the China Scholarship Council (201703780018) to X.Z. is gratefully acknowledged. The Biotechnology and Biological Sciences Research Council provided support to M.B. for development of ChirpBase (BB/K020161/1).
Collections
  • University of St Andrews Research
URI
http://hdl.handle.net/10023/19174

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