Unraveling the complex evolutionary history of lepidopteran chromosomes through ancestral chromosome reconstruction and novel chromosome nomenclature

Abstract Background Lepidoptera is one of the most species-rich animal groups, with substantial karyotype variations among species due to chromosomal rearrangements. Knowledge of the evolutionary patterns of lepidopteran chromosomes still needs to be improved. Results Here, we used chromosome-level genome assemblies of 185 lepidopteran insects to reconstruct an ancestral reference genome and proposed a new chromosome nomenclature. Thus, we renamed over 5000 extant chromosomes with this system, revealing the historical events of chromosomal rearrangements and their features. Additionally, our findings indicate that, compared with autosomes, the Z chromosome in Lepidoptera underwent a fast loss of conserved genes, rapid acquisition of lineage-specific genes, and a low rate of gene duplication. Moreover, we presented evidence that all available 67 W chromosomes originated from a common ancestor chromosome, with four neo-W chromosomes identified, including one generated by fusion with an autosome and three derived through horizontal gene transfer. We also detected nearly 4000 inter-chromosomal gene movement events. Notably, Geminin is transferred from the autosome to the Z chromosome. When located on the autosome, Geminin shows female-biased expression, but on the Z chromosome, it exhibits male-biased expression. This contributes to the sexual dimorphism of body size in silkworms. Conclusions Our study sheds light on the complex evolutionary history of lepidopteran chromosomes based on ancestral chromosome reconstruction and novel chromosome nomenclature.