Multiscale analysis of the randomization limits of the chromosomal gene organization between Lepidoptera and Diptera

Abstract

How chromosome gene organization and gene content evolve among distantly related and structurally malleable genomes remains unresolved. This is particularly the case when considering different insect orders. We have compared the highly contiguous genome assemblies of the lepidopteranDanaus plexippusand the dipteranDrosophila melanogaster,which shared a common ancestor around 290 Ma. The gene content of 23 out of 30D. plexippuschromosomes was significantly associated with one or two of the six chromosomal elements of theDrosophilagenome, denoting common ancestry. Despite the phylogenetic distance, 9.6% of the 1-to-1 orthologues still reside within the same ancestral genome neighbourhood. Furthermore, the comparisonD. plexippus–Bombyx moriindicated that the rates of chromosome repatterning are lower in Lepidoptera than in Diptera, although still within the same order of magnitude. Concordantly, 14 developmental gene clusters showed a higher tendency to retain full or partial clustering inD. plexippus,further supporting that the physical association between the SuperHox and NK clusters existed in the ancestral bilaterian. Our results illuminate the scope and limits of the evolution of the gene organization and content of the ancestral chromosomes to the Lepidoptera and Diptera while helping reconstruct portions of the genome in their most recent common ancestor.