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 spotted cranefly, Nephrotoma appendiculata (Pierre, 1919).

We present a genome assembly from an individual male Nephrotoma appendiculata (the spotted cranefly; Arthropoda; Insecta; Diptera; Tipulidae). The genome sequence is 1,138.0 megabases in span. Most of the assembly is scaffolded into 4 chromosomal pseudomolecules, including the X sex chromosome. The mitochondrial genome has also been assembled and is 17.42 kilobases in length. Gene annotation of this assembly on Ensembl identified 17,753 protein coding genes.

The genome sequence of a hoverfly, Merodon equestris (Fabricius, 1794).

We present a genome assembly from an individual female Merodon equestris (hoverfly; Arthropoda; Insecta; Diptera; Syrphidae). The genome sequence is 873.0 megabases in span. Most of the assembly is scaffolded into 6 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 15.95 kilobases in length.

The genome sequence of the wood-carving leafcutter bee, Megachile ligniseca (Kirby, 1802).

We present a genome assembly from an individual female Megachile ligniseca (the wood-carving leafcutter bee; Arthropoda; Insecta; Hymenoptera; Megachilidae). The genome sequence is 290.0 megabases in span. Most of the assembly is scaffolded into 16 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 23.71 kilobases in length. Gene annotation of this assembly on Ensembl 11,722 protein coding genes.

The genome sequence of the Winter Shade, Tortricodes alternella [Denis & Schiffermüller], 1775.

We present a genome assembly from an individual male Tortricodes alternella (the Winter Shade; Arthropoda; None; Lepidoptera; Tortricidae). The genome sequence is 441.2 megabases in span. Most of the assembly is scaffolded into 22 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genome has also been assembled and is 15.73 kilobases in length. Gene annotation of this assembly on Ensembl identified 17,280 protein coding genes.

The genome sequence of the Emperor moth, Saturnia pavonia (Linnaeus, 1758).

We present a genome assembly from an individual male Saturnia pavonia (the Emperor moth; Arthropoda; Insecta; Lepidoptera; Saturniidae). The genome sequence is 489.9 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 15.29 kilobases in length. Gene annotation of this assembly on Ensembl identified 11,903 protein coding genes.

The genome sequence of the Four-banded Bee-grabber, Conops quadrifasciatus De Geer, 1776.

We present a genome assembly from an individual male Conops quadrifasciatus (the Four-banded Bee-grabber; Arthropoda; Insecta; Diptera; Conopidae). The genome sequence is 210.4 megabases in span. Most of the assembly is scaffolded into 7 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 18.07 kilobases in length. Gene annotation of this assembly on Ensembl identified 23,090 protein coding genes.

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 ten-spot ladybird, Adalia decempunctata (Linnaeus, 1758).

We present a genome assembly from an individual male Adalia decempunctata (the ten-spot ladybird; Arthropoda; Insecta; Coleoptera; Coccinellidae). The genome sequence is 489.4 megabases in span. Most of the assembly is scaffolded into 12 chromosomal pseudomolecules, including the X and Y sex chromosomes. The mitochondrial genome has also been assembled and is 19.68 kilobases in length.

The genome sequence of the Field Cuckoo-bee, Bombus campestris (Panzer, 1801).

We present a genome assembly from an individual male Bombus campestris (the Field Cuckoo-bee; Arthropoda; Insecta; Hymenoptera; Apidae). The genome sequence is 275 megabases in span. Most of the assembly is scaffolded into 25 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 24.7 kilobases in length. Gene annotation of this assembly on Ensembl identified 12,993 protein coding genes.

The genome sequence of the Forest Cuckoo Bee, Bombus sylvestris (Lepeletier, 1832).

We present a genome assembly from an individual male Bombus sylvestris (the Forest Cuckoo Bee; Arthropoda; Insecta; Hymenoptera; Apidae). The genome sequence is 303 megabases in span. Most of the assembly is scaffolded into 24 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 23.6 kilobases in length. Gene annotation of this assembly on Ensembl has identified 13,025 protein coding genes.

The genome sequence of a digger wasp, Ectemnius continuus (Fabricius, 1804).

We present a genome assembly from an individual female Ectemnius continuus (digger wasp; Arthropoda; Insecta; Hymenoptera; Crabronidae). The genome sequence is 260.3 megabases in span. Most of the assembly is scaffolded into 14 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 27.05 kilobases in length. Gene annotation of this assembly on Ensembl identified 9,835 protein coding genes.

The genome sequence of the Saxon Wasp, Dolichovespula saxonica (Fabricius, 1793).

We present a genome assembly from an individual male Dolichovespula saxonica (the Saxon Wasp; Arthropoda; Insecta; Hymenoptera; Vespidae). The genome sequence is 221.8 megabases in span. Most of the assembly is scaffolded into 26 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 18.97 kilobases in length. Gene annotation of this assembly on Ensembl identified 10,856 protein coding genes.

The genome sequence of Fabricius' Nomad Bee, Nomada fabriciana (Linne, 1767).

We present a genome assembly from an individual female Nomada fabriciana (Fabricius' Nomad Bee; Arthropoda; Insecta; Hymenoptera; Apidae). The genome sequence is 233.6 megabases in span. Most of the assembly is scaffolded into 12 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 19.4 kilobases in length. Gene annotation of this assembly on Ensembl identified 9,700 protein coding genes.

The genome sequence of the Orange-tailed Mining Bee, Andrena haemorrhoa (Fabricius, 1781).

We present a genome assembly from an individual female Andrena haemorrhoa (the Orange-tailed Mining Bee; Arthropoda; Insecta; Hymenoptera; Andrenidae). The genome sequence is 330.7 megabases in span. Most of the assembly is scaffolded into 7 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 16.46 kilobases in length. Gene annotation of this assembly on Ensembl identified 10,908 protein coding genes.

The genome sequence of a ground beetle, Nebria brevicollis (Fabricius, 1792).

We present a genome assembly from an individual female Nebria brevicollis (a ground beetle; Arthropoda; Insecta; Coleoptera; Carabidae). The genome sequence is 242 megabases in span. Most of the assembly is scaffolded into 15 chromosomal pseudomolecules, with the X sex chromosome assembled. The mitochondrial genome has also been assembled and is 25.2 kilobases in length. Gene annotation of this assembly on Ensembl identified 11,021 protein-coding genes.

The genome sequence of a beetle-killing wasp, Tiphia femorata (Fabricius, 1775).

We present a genome assembly from an individual female Tiphia femorata (a beetle-killing wasp; Arthropoda; Insecta; Hymenoptera; Tiphilidae). The genome sequence is 276 megabases in span. Most of the assembly (98.73%) is scaffolded into 12 chromosomal pseudomolecules. The complete mitochondrial genome was also assembled and is 22.4 kilobases in length. Annotation of the genome in Ensembl identified 10,470 protein-coding genes.

The genome sequence of an ichneumonid wasp, Heteropelma amictum (Fabricius, 1775).

We present a genome assembly from an individual female Heteropelma amictum (an ichneumonid wasp; Arthropoda; Insecta; Hymenoptera; Ichneumonidae). The genome sequence is 226.4 megabases in span. Most of the assembly is scaffolded into 10 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 20.65 kilobases in length.

The genome sequence of the Wasp Spider, Argiope bruennichi (Scopoli, 1772).

We present a genome assembly from an individual female Argiope bruennichi (the Wasp Spider; Arthropoda; Arachnida; Araneae; Araneidae). The genome sequence is 1,778.4 megabases in span. Most of the assembly is scaffolded into 13 chromosomal pseudomolecules, including the X 1 and X 2 sex chromosomes. The mitochondrial genome has also been assembled and is 14.06 kilobases in length.