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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., Ranz et al. present a high-quality genome assembly for the monarch butterfly Danaus plexippus and a comprehensive set of RNA sequencing data across different tissues and life stages. The authors construct an atlas portraying the breadth of gene expression during the monarch life cycle, which will facilitate a better understanding of D. plexippus’ adaptation to a changing environment.

The monarch butterfly epitomizes insect biodiversity decline. Understanding the genetic basis of the adaptation of the monarch to a changing environment requires genomic and transcriptomic resources that better reflect its genetic diversity while being informative about gene functionality during life cycle. We report a reference-quality genome assembly from an individual resident at a nonmigratory colony in Mexico, and a new gene annotation and expression atlas for 14,865 genes, including 492 unreported long noncoding RNA (lncRNA) genes, based on RNA-seq data from 14 larval and pupal stages, plus adult morphological sections. Two thirds of the genes show significant expression changes associated with a life stage or section, with lncRNAs being more finely regulated during adulthood than protein-coding genes, and male-biased expression being four times more common than female-biased. The two portions of the heterochromosome Z display distinct patterns of differential expression between the sexes, reflecting that dosage compensation is either absent or incomplete –depending on the sample– in the ancestral but not in the novel portion of the Z. This study represents a major advance in the genomic and transcriptome resources available for D. plexippus while providing the first systematic analysis of its transcriptional program across most of its life cycle.