Ancient transposable elements sustain global ecological adaptation despite chronically low nucleotide diversity

Abstract

Transposable elements (TEs) are dynamic components of eukaryotic genomes and a major source of structural and regulatory variation, yet their contribution to ecological adaptation over evolutionary time remains unresolved. This uncertainty is particularly acute in species that occupy broad environmental niches despite chronically low nucleotide diversity, where conventional models predict limited adaptive potential. Here we show that ancient TE polymorphisms underpin global ecological adaptation in Spirodela polyrhiza, one of the smallest flowering plants with low genome-wide nucleotide diversity. Most TE polymorphisms predate continental population divergence. Cold-season temperature emerges as the dominant selective axis, with adaptive signals overwhelmingly associated with TE polymorphisms rather than SNPs. These adaptive TEs bear signatures of selection on standing variation and are embedded in genomic regions shaped by relaxed purifying selection rather than recent hard sweeps. Our results reveal how ancient TE variation sustains ecological adaptation despite chronically depleted nucleotide diversity, resolving a longstanding evolutionary paradox. One sentence summaryHow species adapt with little genetic diversity is a longstanding evolutionary puzzle solved by ancient transposon insertions