Lepidopteran Genomes Have Denser Transposable Elements in Smaller Chromosomes, Likely Driven by Non-allelic Homologous Recombination.

Abstract

Transposable elements (TEs) drive major genome size and structural variations, yet evolutionary forces affecting their accumulation and removal remain unclear. Classical models predict that higher recombination rates lead to more efficient purifying selection, such as TE removal. However, in the painted lady butterfly (Vanessa cardui), smaller chromosomes harbor denser TE content than larger ones despite higher recombination rates. This unexpected pattern raises questions about whether similar trends occur across other Lepidoptera species and what evolutionary forces are behind this pattern. Across ten species spanning ten lepidopteran families, we investigated the relationship between chromosome size and TE organization using comparative genomics. We observed that smaller chromosomes consistently have higher TE densities in all the investigated species. Chromosome size had positive correlations with average inter-TE distance for both young (<5% divergence) and old TEs (5% to 10% divergence). However, the ratio of these distances (young/old TEs) was negatively correlated with chromosome size in eight of ten species, with two showing no statistically significant correlation, suggesting that smaller chromosomes have higher removal rates of sequence between TEs, potentially due to nonallelic homologous recombination, causing the loss of unique sequences between nonallelic homologs. Population genomics analyses showed inconsistent correlations between chromosome size and genetic diversity or selection coefficients between Danaus plexippus and Spodoptera frugiperda, ruling out the efficiency of purifying selection or selective constraint as the main driver. Taken together, we demonstrate that Lepidoptera has a unique genomic feature of denser TEs in smaller chromosomes, with nonallelic homologous recombination as a potential driving force.