Transposable elements underlie chromosomal fusions and fissions in a highly species-rich group of butterflies

Abstract

Chromosomal fusions and fissions reshape karyotypes, recombination landscapes and patterns of speciation, yet the molecular mechanisms underlying their formation remain poorly understood. Comparing 37 chromosome-level Erebia genomes, a butterfly genus with exceptionally high rates of chromosomal rearrangements, we identify more than 250 fusion and fission events and characterise over one hundred breakpoints. Breakpoints and homologous regions in the most closely related species with the unfused chromosomal state are significantly enriched for repetitive elements, particularly R1-like LINE retrotransposons. This provides evidence for the implication of a specific LINE family in inter-chromosomal rearrangements that promote species diversification. R1-like elements at breakpoints are longer than copies in other genomic regions, consistent with ectopic recombination requiring sufficient sequence length and similarity. However, the burst of rearrangements in the youngest and most species-rich Erebia clade does not coincide with increased R1-like activity, indicating that repeat dynamics does not solely account for the elevated rates of fusion and fission. Indeed, we detect lineage-specific gains and losses of genes involved in DNA repair and chromatin organisation that coincide with this burst, suggesting a genomic context that facilitates chromosomal fusions and fissions. Our findings refine the role of repetitive elements in inter-chromosomal rearrangements, identify a candidate substrate for ectopic recombination in Lepidoptera, and establish a framework for understanding how karyotypic diversity arises.