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 journalArticlepeer-review


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 languageEnglish
Article number5001
JournalNature Communications
Issue number1
Publication statusPublished - 12 Jun 2024


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