Diversity, duplication, and genomic organization of homeobox genes in Lepidoptera.

Homeobox genes encode transcription factors with essential roles in patterning and cell fate in developing animal embryos. Many homeobox genes, including Hox and NK genes, are arranged in gene clusters, a feature likely related to transcriptional control. Sparse taxon sampling and fragmentary genome assemblies mean that little is known about the dynamics of homeobox gene evolution across Lepidoptera or about how changes in homeobox gene number and organization relate to diversity in this large order of insects. Here we analyze an extensive data set of high-quality genomes to characterize the number and organization of all homeobox genes in 123 species of Lepidoptera from 23 taxonomic families. We find most Lepidoptera have around 100 homeobox loci, including an unusual Hox gene cluster in which the lab gene is repositioned and the ro gene is next to pb A topologically associating domain spans much of the gene cluster, suggesting deep regulatory conservation of the Hox cluster arrangement in this insect order. Most Lepidoptera have four Shx genes, divergent zen-derived loci, but these loci underwent dramatic duplication in several lineages, with some moths having over 165 homeobox loci in the Hox gene cluster; this expansion is associated with local LINE element density. In contrast, the NK gene cluster content is more stable, although there are differences in organization compared with other insects, as well as major rearrangements within butterflies. Our analysis represents the first description of homeobox gene content across the order Lepidoptera, exemplifying the potential of newly generated genome assemblies for understanding genome and gene family evolution.

Opsin Gene Duplication in Lepidoptera: Retrotransposition, Sex Linkage, and Gene Expression.

Color vision in insects is determined by signaling cascades, central to which are opsin proteins, resulting in sensitivity to light at different wavelengths. In certain insect groups, lineage-specific evolution of opsin genes, in terms of copy number, shifts in expression patterns, and functional amino acid substitutions, has resulted in changes in color vision with subsequent behavioral and niche adaptations. Lepidoptera are a fascinating model to address whether evolutionary change in opsin content and sequence evolution are associated with changes in vision phenotype. Until recently, the lack of high-quality genome data representing broad sampling across the lepidopteran phylogeny has greatly limited our ability to accurately address this question. Here, we annotate opsin genes in 219 lepidopteran genomes representing 33 families, reconstruct their evolutionary history, and analyze shifts in selective pressures and expression between genes and species. We discover 44 duplication events in opsin genes across ∼300 million years of lepidopteran evolution. While many duplication events are species or family specific, we find retention of an ancient long-wavelength-sensitive (LW) opsin duplication derived by retrotransposition within the speciose superfamily Noctuoidea (in the families Nolidae, Erebidae, and Noctuidae). This conserved LW retrogene shows life stage-specific expression suggesting visual sensitivities or other sensory functions specific to the early larval stage. This study provides a comprehensive order-wide view of opsin evolution across Lepidoptera, showcasing high rates of opsin duplications and changes in expression patterns.

The genome sequence of the Dotted Grey Groundling, Athrips mouffetella (Linnaeus, 1758).

We present a genome assembly from an individual female Athrips mouffetella (the Dotted Grey Groundling; Arthropoda; Insecta; Lepidoptera; Gelechiidae). The genome sequence is 869.7 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z and W sex chromosomes. The mitochondrial genome has also been assembled and is 15.23 kilobases in length. Gene annotation of this assembly on Ensembl identified 22,889 protein coding genes.

The genome sequence of the Brown Oak Tortrix, Archips crataeganus (Hübner, 1796).

We present a genome assembly from an individual female Archips crataeganus (the Brown Oak Tortrix; Arthropoda; Insecta; Lepidoptera; Tortricidae). The genome sequence is 626.9 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z and W sex chromosomes. The mitochondrial genome has also been assembled and is 16.64 kilobases in length. Gene annotation of this assembly on Ensembl identified 19,596 protein coding genes.

The genome sequence of the Marbled White Spot, Protodeltote pygarga (Hufnagel, 1766).

We present a genome assembly from an individual male Protodeltote pygarga (the Marbled White Spot; Arthropoda; Insecta; Lepidoptera; Noctuidae). The genome sequence is 421.1 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.48 kilobases in length. Gene annotation of this assembly on Ensembl identified 17,784 protein coding genes.

The genome sequence of the White-point, Mythimna albipuncta (Denis & Schiffermüller, 1775).

We present a genome assembly from an individual male Mythimna albipuncta (the White-point; Arthropoda; Insecta; Lepidoptera; Noctuidae). The genome sequence is 698.6 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.38 kilobases in length. Gene annotation of this assembly on Ensembl identified 13,679 protein coding genes.

The genome sequence of the Mottled Pug, Eupithecia exiguata (Hübner, 1813).

We present a genome assembly from an individual male Eupithecia exiguata (the Mottled Pug; Arthropoda; Insecta; Lepidoptera; Geometridae). The genome sequence is 372.9 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 16.39 kilobases in length. Gene annotation of this assembly on Ensembl identified 11,194 protein coding genes.

The genome sequence of the Water Veneer, Acentria ephemerella (Denis & Schiffermüller, 1775).

We present a genome assembly from an individual male Acentria ephemerella (the Water Veneer; Arthropoda; Insecta; Lepidoptera; Crambidae). The genome sequence is 340.8 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.35 kilobases in length. Gene annotation of this assembly on Ensembl identified 17,748 protein coding genes.

The genome sequence of the Tipped Oak Case-bearer, Coleophora flavipennella (Duponchel 1843).

We present a genome assembly from an individual female Coleophora flavipennella (the Tipped Oak Case-bearer; Arthropoda; Insecta; Lepidoptera; Coleophoridae). The genome sequence is 989.3 megabases in span. Most of the assembly is scaffolded into 57 chromosomal pseudomolecules, including the W and Z sex chromosomes. The mitochondrial genome has also been assembled and is 15.77 kilobases in length.

The genome sequence of the Summer Chafer, Amphimallon solstitiale (Linnaeus, 1758).

We present a genome assembly from an individual male Amphimallon solstitiale (the Summer Chafer; Arthropoda; Insecta; Coleoptera; Scarabaeidae). The genome sequence is 1,584.1 megabases in span. Most of the assembly is scaffolded into 11 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 19.29 kilobases in length.

The genome sequence of the Chequered Fruit-tree Tortrix, Pandemis corylana (Fabricius, 1794).

We present a genome assembly from an individual male Pandemis corylana (the Chequered Fruit-tree Tortrix; Arthropoda; Insecta; Lepidoptera; Tortricidae). The genome sequence is 441.6 megabases in span. Most of the assembly is scaffolded into 30 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.53 kilobases in length. Gene annotation of this assembly on Ensembl identified 19,608 protein coding genes.

The genome sequence of the Six-belted Clearwing, Bembecia ichneumoniformis (Denis & Schiffermüller, 1775).

We present a genome assembly from an individual male Bembecia ichneumoniformis (the Six-belted Clearwing; Arthropoda; Insecta; Lepidoptera; Sesiidae). The genome sequence is 511.4 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.32 kilobases in length. Gene annotation of this assembly on Ensembl identified 12,114 protein coding genes.

The genome sequence of the Diamondback Moth, Plutella xylostella (Linnaeus, 1758).

We present a genome assembly from an individual male Plutella xylostella (the Diamondback Moth; Arthropoda; Insecta; Lepidoptera; Plutellidae). The genome sequence is 323.3 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 35.12 kilobases in length. Gene annotation of this assembly on Ensembl identified 17,190 protein coding genes.

The genome sequence of the Powdered Quaker, Orthosia gracilis (Schiffermüller, 1775).

We present a genome assembly from an individual male Orthosia gracilis (the powdered quaker; Arthropoda; Insecta; Lepidoptera; Noctuidae). The genome sequence is 715.5 megabases in span. Most of the assembly is scaffolded into 14 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.43 kilobases in length.

The genome sequence of the Dotted Border, Agriopis marginaria (Fabricius, 1776).

We present a genome assembly from an individual male Agriopis marginaria (the Dotted Border, Arthropoda; Insecta; Lepidoptera; Geometridae). The genome sequence is 500.9 megabases in span. Most of the assembly is scaffolded into 29 chromosomal pseudomolecules, including the assembled Z sex chromosome. The mitochondrial genome has also been assembled and is 16.9 kilobases in length. Gene annotation of this assembly on Ensembl identified 12,443 protein coding genes.

The genome sequence of the White-shouldered Marble, Apotomis turbidana (Hübner, 1825).

We present a genome assembly from an individual male Apotomis turbidana (the White-shouldered Marble; Arthropoda; Insecta; Lepidoptera; Tortricidae). The genome sequence is 720.5 megabases in span. Most of the assembly is scaffolded into 28 chromosomal pseudomolecules, including the assembled Z sex chromosome. The mitochondrial genome has also been assembled and is 16.8 kilobases in length. Gene annotation of this assembly on Ensembl identified 22,646 protein coding genes.

The genome sequence of the Elbow-stripe Grass-veneer, Agriphila geniculea (Haworth, 1811).

We present a genome assembly from an individual female Agriphila geniculea (the Elbow-stripe Grass-veneer; Arthropoda; Insecta; Lepidoptera; Crambidae). The genome sequence is 781.6 megabases in span. Most of the assembly is scaffolded into 30 chromosomal pseudomolecules, including the Z and W sex chromosomes. The mitochondrial genome has also been assembled and is 15.4 kilobases in length. Gene annotation of this assembly on Ensembl identified 22,132 protein coding genes.

The genome sequence of the Lesser Swallow Prominent, Pheosia gnoma (Fabricius, 1777).

We present a genome assembly from an individual male Pheosia gnoma (the Lesser Swallow Prominent; Arthropoda; Insecta; Lepidoptera; Notodontidae). The genome sequence is 271.3 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 17.0 kilobases in length. Gene annotation of this assembly on Ensembl identified 11,628 protein coding genes.

The genome sequence of the Gold Triangle, Hypsopygia costalis (Fabricius, 1775).

We present a genome assembly from an individual male Hypsopygia costalis (the Gold Triangle; Arthropoda; Insecta; Lepidoptera; Pyralidae). The genome sequence is 818 megabases in span. Most of the assembly is scaffolded into 31 chromosomal pseudomolecules with the Z sex chromosome assembled. The mitochondrial genome has also been assembled and is 15.3 kilobases in length. Gene annotation of this assembly on Ensembl identified 19,248 protein coding genes.

The genome sequence of the long-horned flat-body, Carcina quercana (Fabricius, 1775).

We present a genome assembly from an individual male Carcina quercana (the long-horned flat-body; Arthropoda; Insecta; Lepidoptera; Depressariidae). The genome sequence is 409 megabases in span. Most of the assembly (99.96%) is scaffolded into 30 chromosomal pseudomolecules, including the assembled Z sex chromosome. The complete mitochondrial genome was also assembled and is 15.3 kilobases in length. Gene annotation of this assembly on Ensembl identified 18,108 protein coding genes.