Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution

Xiao Zhang; Mark Blaxter; Jonathan M.D. Wood; Alan Tracey; Shane McCarthy; Peter Thorpe; Jack G. Rayner; Shangzhe Zhang; Kirstin L. Sikkink; Susan L. Balenger; Nathan W. Bailey

doi:10.1038/s41467-024-49344-4

Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution

Xiao Zhang^*, Mark Blaxter, Jonathan M.D. Wood, Alan Tracey, Shane McCarthy, Peter Thorpe, Jack G. Rayner, Shangzhe Zhang, Kirstin L. Sikkink, Susan L. Balenger, Nathan W. Bailey^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

Abstract

Theory predicts that compensatory genetic changes reduce negative indirect effects of selected variants during adaptive evolution, but evidence is scarce. Here, we test this in a wild population of Hawaiian crickets using temporal genomics and a high-quality chromosome-level cricket genome. In this population, a mutation, flatwing, silences males and rapidly spread due to an acoustically-orienting parasitoid. Our sampling spanned a social transition during which flatwing fixed and the population went silent. We find long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to negative flatwing-associated effects. We develop a combinatorial enrichment approach using transcriptome data to test for compensatory, intragenomic coevolution. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population’s transition to silence, particularly behavioural responses to silent environments. Our results demonstrate how ‘adaptation begets adaptation’; changes to the sociogenetic environment accompanying rapid trait evolution can generate selection provoking further, compensatory adaptation.

Original language	English
Article number	5001
Journal	Nature Communications
Volume	15
Issue number	1
DOIs	https://doi.org/10.1038/s41467-024-49344-4
Publication status	Published - 12 Jun 2024

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1 Active
3 Finished

NSF with Lincoln: MULTIDISCIPLINARY APPROACH TO BIOACOUSTICS: Integrating phylogenomics, biophysics, and functional genomics to unravel the evolution of hearing and sin
Bailey, N. W. (PI)
NERC
1/03/20 → 28/02/25
Project: Standard
Nathan Bailey: How repeatable is adaptvie evolution? Testing what promotes rapid adaptation in a replicated natural system
Bailey, N. W. (PI)
NERC
3/12/19 → 2/12/22
Project: Standard
Institutional Strategic Support Fund 2: ISSF 2
Naismith, J. (PI)
The Wellcome Trust
1/11/14 → 31/10/16
Project: Standard

Cite this

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title = "Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution",

abstract = "Theory predicts that compensatory genetic changes reduce negative indirect effects of selected variants during adaptive evolution, but evidence is scarce. Here, we test this in a wild population of Hawaiian crickets using temporal genomics and a high-quality chromosome-level cricket genome. In this population, a mutation, flatwing, silences males and rapidly spread due to an acoustically-orienting parasitoid. Our sampling spanned a social transition during which flatwing fixed and the population went silent. We find long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to negative flatwing-associated effects. We develop a combinatorial enrichment approach using transcriptome data to test for compensatory, intragenomic coevolution. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population{\textquoteright}s transition to silence, particularly behavioural responses to silent environments. Our results demonstrate how {\textquoteleft}adaptation begets adaptation{\textquoteright}; changes to the sociogenetic environment accompanying rapid trait evolution can generate selection provoking further, compensatory adaptation.",

author = "Xiao Zhang and Mark Blaxter and Wood, {Jonathan M.D.} and Alan Tracey and Shane McCarthy and Peter Thorpe and Rayner, {Jack G.} and Shangzhe Zhang and Sikkink, {Kirstin L.} and Balenger, {Susan L.} and Bailey, {Nathan W.}",

note = "This study was supported with funding from the UK Natural Environment Research Council to N.W.B. (NE/T000619/1, NE/T014806/1, NE/L011255/1) and M.B. (NE/W001519/1). We are grateful for bioinformatics support from Iain Milne and the use of the UK\u2019s Crop Diversity Bioinformatics HPC, funded by the UK Biotechnology and Biological Sciences Research Council (BB/S019669/1), as well as the St Andrews Bioinformatics Unit, funded by a Wellcome Trust ISSF award (105621/Z/14/Z).",

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AU - Rayner, Jack G.

AU - Zhang, Shangzhe

AU - Sikkink, Kirstin L.

AU - Balenger, Susan L.

AU - Bailey, Nathan W.

N1 - This study was supported with funding from the UK Natural Environment Research Council to N.W.B. (NE/T000619/1, NE/T014806/1, NE/L011255/1) and M.B. (NE/W001519/1). We are grateful for bioinformatics support from Iain Milne and the use of the UK\u2019s Crop Diversity Bioinformatics HPC, funded by the UK Biotechnology and Biological Sciences Research Council (BB/S019669/1), as well as the St Andrews Bioinformatics Unit, funded by a Wellcome Trust ISSF award (105621/Z/14/Z).

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N2 - Theory predicts that compensatory genetic changes reduce negative indirect effects of selected variants during adaptive evolution, but evidence is scarce. Here, we test this in a wild population of Hawaiian crickets using temporal genomics and a high-quality chromosome-level cricket genome. In this population, a mutation, flatwing, silences males and rapidly spread due to an acoustically-orienting parasitoid. Our sampling spanned a social transition during which flatwing fixed and the population went silent. We find long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to negative flatwing-associated effects. We develop a combinatorial enrichment approach using transcriptome data to test for compensatory, intragenomic coevolution. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population’s transition to silence, particularly behavioural responses to silent environments. Our results demonstrate how ‘adaptation begets adaptation’; changes to the sociogenetic environment accompanying rapid trait evolution can generate selection provoking further, compensatory adaptation.

AB - Theory predicts that compensatory genetic changes reduce negative indirect effects of selected variants during adaptive evolution, but evidence is scarce. Here, we test this in a wild population of Hawaiian crickets using temporal genomics and a high-quality chromosome-level cricket genome. In this population, a mutation, flatwing, silences males and rapidly spread due to an acoustically-orienting parasitoid. Our sampling spanned a social transition during which flatwing fixed and the population went silent. We find long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to negative flatwing-associated effects. We develop a combinatorial enrichment approach using transcriptome data to test for compensatory, intragenomic coevolution. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population’s transition to silence, particularly behavioural responses to silent environments. Our results demonstrate how ‘adaptation begets adaptation’; changes to the sociogenetic environment accompanying rapid trait evolution can generate selection provoking further, compensatory adaptation.

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Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution

Abstract

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Projects

NSF with Lincoln: MULTIDISCIPLINARY APPROACH TO BIOACOUSTICS: Integrating phylogenomics, biophysics, and functional genomics to unravel the evolution of hearing and sin

Nathan Bailey: How repeatable is adaptvie evolution? Testing what promotes rapid adaptation in a replicated natural system

Institutional Strategic Support Fund 2: ISSF 2

Cite this