Transposable Element-Driven PIEZO Mutation Enhances Locust Flight in Plateau Hypoxia.

Transposable elements contribute to species diversification and adaptive evolution. However, it remains challenging to reconcile the impacts of TEs on microevolution (within species) and macroevolution (among species) given their huge pool and complex dynamics in genomes. Here, we generated the genome for the notorious worldwide migratory locust, Locusta migratoria, sampled from Qinghai-Tibet Plateau. Comparative genome analyses uncovered extensive TE-driven genome size variation, and lineage-specific expansion of TEs, particularly of the PiggyBac superfamily in the locust. Whole-genome resequencing of 153 locust individuals collected across an altitudinal gradient ranging from 2 to 4100 m clarified their distinct elevational genetic divergence, which is consistent across SNP and TE insertion polymorphisms analysis. A total of 11 869 TE insertions were found within selective sweeps, including at least 279 genes associated with altitude adaptation. TEs from five superfamilies, accounting for 55.68% of the candidate adaptive TEs, exhibited significant expansion in both microevolution and macroevolution. We validated that PiggyBac insertion into the PIEZO gene induced alternative splicing and enhanced flight performance under hypoxia through AMPK pathway. These data provide robust evidence that TEs are central drivers of genomic evolution across micro- and macroevolutionary scales, shaping genomic landscape and promoting adaptive change.