The Genome of Winter Moth (Operophtera brumata) Provides a Genomic Perspective on Sexual Dimorphism and Phenology

Abstract

The winter moth (Operophtera brumata) belongs to one of the most species-rich families in Lepidoptera, the Geometridae (approximately 23,000 species). This family is of great economic importance as most species are herbivorous and capable of defoliating trees. Genome assembly of the winter moth allows the study of genes and gene families, such as the cytochrome P450 gene family, which is known to be vital in plant secondary metabolite detoxification and host-plant selection. It also enables exploration of the genomic basis for female brachyptery (wing reduction), a feature of sexual dimorphism in winter moth, and for seasonal timing, a trait extensively studied in this species. Here we present a reference genome for the winter moth, the first geometrid and largest sequenced Lepidopteran genome to date (638 Mb) including a set of 16,912 predicted protein-coding genes. This allowed us to assess the dynamics of evolution on a genome-wide scale using the P450 gene family. We also identified an expanded gene family potentially linked to female brachyptery, and annotated the genes involved in the circadian clock mechanism as main candidates for involvement in seasonal timing. The genome will contribute to Lepidopteran genomic resources and comparative genomics. In addition, the genome enhances our ability to understand the genetic and molecular basis of insect seasonal timing and thereby provides a reference for future evolutionary and population studies on the winter moth.

Keywords: Lepidoptera; circadian clock; cytochrome P450; phenology; sexual dimorphism; winter moth.

Fig. 1

—Male (left) and female (right) winter moth. The pictures show female brachyptery in winter moth.

Fig. 2

—Lepidoptera P450 gene family tree. The tree shows species-specific P450 gene family expansions in six Lepidoptera, with large winter moth expansions in CYP3 and CYP4. Branch colors represent the Cytochrome P450 clades: CYP2 (blue), CYP3 (yellow), CYP4 (red), CYP-Mito (green).

Fig. 3

—Phylogenetic tree of the four rdx(-like) orthology groups. Orthology group OG318 (yellow) contains 25 copies of an O. brumata specific rdx-like gene. The Drosophila ortholog is in group OG2662. All genes have a BZB-POZ domain to interact with CUL3 except for OG6733. Only proteins in group OG2662 also contain the MATH domain.

Fig. 4

—Circadian clock mechanism in Lepidoptera. (A) List of clock genes, identified in the winter moth genome. (B) The mechanism comprises the core transcriptional/translational feedback loop (left) and the modulatory feedback loop (right). Clock (Clk) and Cycle (Cyc) form a heterodimer and drive the transcription of period (Per), timeless (Tim), and cryptrochrome 2 (Cry2) by binding their upstream E-box elements. Cry2 is responsible for the inhibition of Clk:Cyc transcription, that is, its own activators. Per and Tim bind through a PAS domain. Casein kinase II (CkII), discs overgrown (Dbt), and the protein phosphatase 2A (Pp2A) are involved in the posttranslational modifications and activation of Per and Tim. Jetleg (Jet) is responsible for Tim degradation, modulated by Cry1, activated by light. Slimb signals Per degradation. In insects, Per and Tim are transcribed mostly during the night. Vri (negative) and Pdp1 (positive) regulate the expression of Clk in the secondary feedback loop.