Lineage-specific evolution of LTR retrotransposons under natural selection drives genomic divergence in diploid Oryza species

Abstract

LTR retrotransposons (LTR-RTs) are major drivers of plant genome evolution. However, the principles governing how natural selection shapes their lineage-specific dynamics across closely related species remain elusive. Here, we performed a comprehensive comparative analysis of LTR-RTs across 15 diploid Oryza species, representing all major genome types. We reconstructed the spatiotemporal distribution and evolutionary trajectories of LTR-RTs, revealing three distinct evolutionary patterns influenced by natural selection: lineage-specific expansion under purifying selection, balanced co-evolution under balancing selection, and lineage-specific retention under strong positive selection. We further demonstrated that species-specific LTR-RT families significantly contribute to highly diverged regions (HDRs) and non-aligned regions (NOTALs), drive segmental duplications, and influence genome size variation. Notably, the removal of LTR-RTs, particularly from medium-removal-rate families, is a key factor in genome size contraction. Our study provides a population-genetic perspective on LTR-RT evolution and highlights their critical role in shaping genomic divergence and adaptation in Oryza. Our findings provide a population-genetic framework for understanding how the co-evolutionary dynamics between TEs and their hosts shape genome architecture and adaptation in closely related species.