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Silent Crickets Reveal the Genomic Footprint of Recent Adaptive Trait Loss

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
doi: https://doi.org/10.1101/489526
Sonia Pascoal
1Department of Zoology, University of Cambridge, CB2 3EJ, United Kingdom
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Judith E. Risse
2Bioinformatics, Department of Plant Sciences, Wageningen University & Research, 6708 PB Wageningen, The Netherlands
3Animal Ecology, Netherlands Institute of Ecology, PO Box 50, 6700 AB Wageningen, The Netherlands
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Xiao Zhang
4School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, United Kingdom
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Mark Blaxter
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
6Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
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Timothee Cezard
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
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Richard J. Challis
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
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Karim Gharbi
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
7Earlham Institute, Norwich Research Park, Norwich NR4 7UZ, United Kingdom
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John Hunt
8School of Science and Health and the Hawkesbury Institute for the Environment, Western Sydney University, Penrith, NSW 2751, Australia
9Centre for Ecology and Conservation, University of Exeter, Cornwall Campus, Penryn TR10 9FE, United Kingom
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Sujai Kumar
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
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Emma Langan
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
10School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7UZ, United Kingdom
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Xuan Liu
11Centre for Genomic Research, University of Liverpool, Liverpool L69 7ZB, United Kingdom
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Jack G. Rayner
4School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, United Kingdom
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Michael G. Ritchie
4School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, United Kingdom
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Basten L. Snoek
12Theoretical Biology and Bioinformatics, Utrecht University, Padualaan 8, 3584 CH Utrecht, The Netherlands
13Terrestrial Ecology, Netherlands Institute of Ecology, PO Box 50, 6700 AB Wageningen, The Netherlands
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Urmi Trivedi
5Edinburgh Genomics, University of Edinburgh, Edinburgh EH9 3JT, United Kingdom
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Nathan W. Bailey
4School of Biology, University of St Andrews, St Andrews, Fife KY16 9TH, United Kingdom
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  • For correspondence: nwb3@st-andrews.ac.uk
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Abstract

Secondary trait loss is widespread and has profound consequences, from generating diversity to driving adaptation. Sexual trait loss is particularly common1. Its genomic impact is challenging to reconstruct because most reversals occurred in the distant evolutionary past and must be inferred indirectly2, and questions remain about the extent of disruption caused by pleiotropy, altered gene expression and loss of homeostasis3. We tested the genomic signature of recent sexual signal loss in Hawaiian field crickets, Teleogryllus oceanicus. Song loss is controlled by a sex-linked Mendelian locus, flatwing, which feminises male wings by erasing sound-producing veins. This variant spread rapidly under pressure from an eavesdropping parasitoid fly. We sequenced, assembled and annotated the T. oceanicus genome, produced a high-density linkage map, and localised flatwing on the X chromosome. We characterised pleiotropic effects of flatwing, including changes in embryonic gene expression and alteration of another sexual signal, chemical pheromones. Song loss is associated with pleiotropy, hitchhiking and genome-wide regulatory disruption which feminises flatwing male pheromones. The footprint of recent adaptive trait loss illustrates R. A. Fisher’s influential prediction that variants with large mutational effect sizes can invade genomes during the earliest stages of adaptation to extreme pressures, despite having severely disruptive genomic consequences.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted December 09, 2018.
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Silent Crickets Reveal the Genomic Footprint of Recent Adaptive Trait Loss
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
bioRxiv 489526; doi: https://doi.org/10.1101/489526
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Silent Crickets Reveal the Genomic Footprint of Recent Adaptive Trait Loss
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
bioRxiv 489526; doi: https://doi.org/10.1101/489526

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