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’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.