The horned gall aphid Schlechtendalia chinensis, is an economically important insect that induces galls valuable for medicinal and chemical industries. S. chinensis manipulates its host plant to form well-organized horned galls during feeding. So far, more than twenty aphid genomes have been reported; however, all of those are derived from free-living aphids. Here we generated a high-quality genome assembly of S. chinensis, representing the first genome sequence of a galling aphid. The final genome assembly was 280.43 Mb, with 97% of the assembled sequences anchored into thirteen chromosomes. S. chinensis presents the smallest aphid genome size among available aphid genomes to date. The contig and scaffold N50 values were 3.39 Mb and 20.58 Mb, respectively. The assembly included 96.4% of conserved arthropod and 97.8% of conserved Hemiptera single-copy orthologous genes based on BUSCO analysis. A total of 13,437 protein-coding genes were predicted. Phylogenomic analysis showed that S. chinensis formed a single clade between the Eriosoma lanigerum clade and the Aphidini+Macrosiphini aphid clades. In addition, salivary proteins were found to be differentially expressed when S. chinensis underwent host alternation, indicating their potential roles in gall formation and plant defense suppression. A total of 36 cytochrome P450 genes were identified in S. chinensis, considerably fewer compared to other aphids, probably due to its small host plant range. The high-quality S. chinensis genome assembly and annotation provide an essential genetic background for future studies to reveal the mechanism of gall formation and to explore the interaction between aphids and their host plants.

The horned gall aphid Schlechtendalia chinensis, is an economically important insect that induces galls valuable for medicinal and chemical industries. S. chinensis manipulates its host plant to form well-organized horned galls during feeding. So far, more than twenty aphid genomes have been reported; however, all of those are derived from free-living aphids. Here we generated a high-quality genome assembly of S. chinensis, representing the first genome sequence of a galling aphid. The final genome assembly was 280.43 Mb, with 97% of the assembled sequences anchored into thirteen chromosomes. S. chinensis presents the smallest aphid genome size among available aphid genomes to date. The contig and scaffold N50 values were 3.39 Mb and 20.58 Mb, respectively. The assembly included 96.4% of conserved arthropod and 97.8% of conserved Hemiptera single-copy orthologous genes based on BUSCO analysis. A total of 13,437 protein-coding genes were predicted. Phylogenomic analysis showed that S. chinensis formed a single clade between the Eriosoma lanigerum clade and the Aphidini+Macrosiphini aphid clades. In addition, salivary proteins were found to be differentially expressed when S. chinensis underwent host alternation, indicating their potential roles in gall formation and plant defense suppression. A total of 36 cytochrome P450 genes were identified in S. chinensis, considerably fewer compared to other aphids, probably due to its small host plant range. The high-quality S. chinensis genome assembly and annotation provide an essential genetic background for future studies to reveal the mechanism of gall formation and to explore the interaction between aphids and their host plants.

Scale insects are hemimetabolous, showing “incomplete” metamorphosis and no true pupal stage. Ericerus pela, commonly known as the white wax scale insect (hereafter, WWS), is a wax-producing insect found in Asia and Europe. WWS displays dramatic sexual dimorphism, with notably different metamorphic fates in males and females. Males develop into winged adults, while females are neotenic and maintain a nymph-like appearance, which are flightless and remain stationary. Here we report the de novo assembly of the WWS genome with its size of 638.30 Mb (69.68Mb for scaffold N50) by PacBio sequencing and Hi-C. From these data, we constructed a robust phylogenetic analysis of 24,923 gene families from 16 representative insect genomes, which indicates that holometabola evolved from incomplete metamorphosis insects in the Late Carboniferous, about 50 million years earlier than previously thought. To study the distinct development of males and females, we analyzed the methylome landscape in either sex. Surprisingly, WWS displayed high levels of methylation (4.42% for males) when compared to other insects. We observed differential methylation patterns for genes involved in steroid and sesquiterpenoids production as well as related fatty acid metabolism pathways. We show here that both males and females exhibit distinct titer profiles for ecdysone, the principal insect steroid hormone, and juvenile hormone (a sesquiterpenoid), suggesting that these hormones are the primary drivers of sexually dimorphic features. Our results provide a comprehensive genomic and epigenomic resource of scale insects that provide new insights into the evolution of metamorphosis and sexual dimorphism in insects.

Scale insects are hemimetabolous, showing “incomplete” metamorphosis and no true pupal stage. Ericerus pela, commonly known as the white wax scale insect (hereafter, WWS), is a wax-producing insect found in Asia and Europe. WWS displays dramatic sexual dimorphism, with notably different metamorphic fates in males and females. Males develop into winged adults, while females are neotenic and maintain a nymph-like appearance, which are flightless and remain stationary. Here we report the de novo assembly and analysis of the WWS genome. From these data, we constructed a robust phylogenetic analysis of 24,923 gene families from 16 representative insect genomes, which indicates that holometabola evolved from hemimetabolous insects in the Late Carboniferous, about 50 million years earlier than previously thought. To study the distinct development of males and females, we analyzed the methylome landscape in either sex. Surprisingly, WWS displayed high levels of methylation (4.42%) when compared to other insects. We observed differential methylation patterns for genes involved in steroid and sesquiterpenoids production as well as related fatty acid metabolism pathways. We show here that both males and females produce distinct profiles of ecdysone (the principal insect steroid hormone) and juvenile hormone (a sesquiterpenoid), consistent with their different development fates. Our results provide a comprehensive genomic and epigenomic resource of scale insects that provide new insights into the evolution of metamorphosis and sexual dimorphism in insects.