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 lepidopteran Danaus plexippus and the dipteran Drosophila melanogaster, which shared a common ancestor around 290 Ma. The gene content of 23 out of 30 D. plexippus chromosomes was significantly associated with one or two of the six chromosomal elements of the Drosophila genome, 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 comparison D. plexippus-Bombyx mori indicated 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 in D. 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.

A detailed knowledge of gene function in the monarch butterfly is still lacking. Here we generate a genome assembly from a Mexican nonmigratory population and used RNA-seq data from 14 biological samples for gene annotation and to construct an atlas portraying the breadth of gene expression during most of the monarch life cycle. Two thirds of the genes show expression changes, with long noncoding RNAs being particularly finely regulated during adulthood, and male-biased expression being four times more common than female-biased. The two portions of the monarch heterochromosome Z, one ancestral to the Lepidoptera and the other resulting from a chromosomal fusion, display distinct association with sex-biased expression, reflecting sample-dependent incompleteness or absence of dosage compensation in the ancestral but not the novel portion of the Z. This study presents extended genomic and transcriptomic resources that will facilitate a better understanding of the monarch's adaptation to a changing environment.