Temporal genomics in Hawaiian crickets reveals compensatory intragenomic coadaptation during adaptive evolution
Modern adaptation genomics almost exclusively focuses on characterizing genomic hotspots of adaptation, rather than compensatory genetic changes mitigating negative pleiotropy and other indirect effects of adaptive variants.  We addressed this using temporal population genomics in a wild population of Hawaiian crickets undergoing contemporary adaptation. A mutation, flatwing, silences males and rapidly spread under selection from an acoustically-orienting parasitoid. Our sampling spanned a major social transition during which the last singing male died and the population went silent, which we predicted would cause genome-wide selection. By generating a high-quality chromosome-level cricket genome and resequencing data, we found that long-range linkage disequilibrium around the putative flatwing locus was maintained over time, and hitchhiking genes had functions related to known flatwing-associated effects. We developed a combinatorial enrichment approach using gene expression data to test for compensatory, intragenomic coevolution provoked by the spread of flatwing. Temporal changes in genomic selection were distributed genome-wide and functionally associated with the population's transition to silence. Selected regions were enriched for genes expressed during immune challenge by parasitoid infestation and behavioural plasticity to silent environments. Our results demonstrate how 'adaptation begets adaptation' and suggest that feedback from the sociogenetic environment is an overlooked component of rapid adaptive evolution.