Draft Genome Assemblies and Annotations ofAgrypnia vestitaWalker, andHesperophylax magnusBanks Reveal Substantial Repetitive Element Expansion in Tube Case-making Caddisflies (Insecta: Trichoptera)

Abstract

Trichoptera (caddisflies) play an essential role in freshwater ecosystems; for instance, larvae process organic material from the water and are food for a variety of predators. Knowledge on the genomic diversity of caddisflies can facilitate comparative and phylogenetic studies thereby allowing scientists to better understand the evolutionary history of caddisflies. While Trichoptera are the most diverse aquatic insect order, they remain poorly represented in terms of genomic resources. To date, all long-read based genomes have been sequenced from individuals in the retreat-making suborder, Annulipalpia, leaving ∼275 Ma of evolution without high-quality genomic resources. Here, we report the first long-read based de novo genome assemblies of two tube case-making Trichoptera from the suborder Integripalpia, Agrypnia vestita Walker and Hesperophylax magnus Banks. We find that these tube case-making caddisflies have genome sizes that are at least three-fold larger than those of currently sequenced annulipalpian genomes and that this pattern is at least partly driven by major expansion of repetitive elements. In H. magnus, long interspersed nuclear elements (LINEs) alone exceed the entire genome size of some annulipalpian counterparts suggesting that caddisflies have high potential as a model for understanding genome size evolution in diverse insect lineages.SignificanceThere is a lack of genomic resources for aquatic insects. So far, only three high-quality genomes have been assembled, all from individuals in the retreat-making suborder Annulipalpia. In this article, we report the first high-quality genomes of two case-making species from the suborder Integripalpia, which are essential for studying genomic diversity across this ecologically diverse insect order. Our research reveals larger genome sizes in the tube case-makers (suborder Integripalpia, infraorder Phryganides), accompanied by a disproportionate increase of repetitive DNA. This suggests that genome size is at least partly driven by a major expansion of repetitive elements. Our work shows that caddisflies have high potential as a model for understanding how genomic diversity might be linked to functional diversification and forms the basis for detailed studies on genome size evolution in caddisflies.Data depositionThis project has been deposited at NCBI under the Bioproject ID: PRJNA668166

Characterization of primary structure of the major silk gene,h-fibroin, across caddisfly suborders (Trichoptera)

“…Structurally, this would correspond to defining each repeat as beginning with a single (SX) n E ß-strand [5]. In presenting the new h-fibroin sequences reported here, we have defined the repeating modules as each having two parts: first, a region comprising a variable number (1-6) of (SX) n E motifs, each separated by short (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) stretches of intervening amino acids, and, second, a variable length (8-144 residues) G(glycine) -or G(glycine)-P(proline)-rich region. Schematically, in figure 2, the two parts are represented by different symbols in each block.…”

“…The combination of long-and short-read sequencing approaches resulted in the assembly of two full-length h-fibroin sequences [10,14]. However, the hfibroin could not be assembled in more than 20 species with these sequencing techniques [15,16].…”

Genome size evolution in the diverse insect order Trichoptera

“…Based on the genomes of six trichopteran species, Olsen et al [30] found a 3-fold suborderspecific increase of genome size and hypothesized that genome size variation is correlated with their phylogeny. To test this hypothesis, we first reconstructed phylogenetic relationships by analyzing ~2,000 single-copy BUSCO genes from the 26 study species (Figs.…”

“…In insects, the known 3 genomic proportion of TEs ranges from 1% in the antarctic midge Belgica antarctica [26] to 65% in the migratory locust Locusta migratoria [27]. Broad-scale analysis of TE abundance in insects suggests that some order-specific signatures are present, however, major shifts in TE abundance are also common at shallow taxonomic levels [28], [29], including in Trichoptera [30]. The movement and proliferation of REs can have deleterious consequences on gene function and genome stability [31], [32], [33], [34], [35].…”

“…An initial comparison of six caddisfly species found wide genome size variation in Trichoptera (ranging from 230 Mbp to 1.4 Gbp). In that study, we hypothesized that the observed variation was correlated with caddisfly phylogeny and that TEs contributed to a suborder-specific increase of genome size [30].…”