600+ insect genomes reveal repetitive element dynamics and highlight biodiversity-scale repeat annotation challenges

Abstract

Repetitive elements (REs) are integral to the composition, structure, and function of eukaryotic genomes. Yet, RE dynamics remain understudied in many taxonomic groups, preventing holistic understanding of how genomes and species evolve. Here, we investigated REs across 601 insect species (20 orders) to better understand the RE landscape of insects and to evaluate automated RE annotation methods in the era of biodiversity genomics. We identified wide variation in the types and frequency of REs across insect groups. We quantified associations between REs and protein-coding genes and found an elevated frequency of associations in insects with abundant long interspersed nuclear elements (LINEs). Sequencing technology impacts RE detection; ~36% more REs could be identified in long-read versus short-read assemblies. Long terminal repeats (LTRs) showed markedly improved detection in long-read assemblies (162% more), while DNA transposons and LINEs showed less respective technology-related bias. We illustrate fundamental challenges to efficient study of REs in diverse groups, showing that in most insect lineages, 25-85% of repetitive sequences were unclassified compared to only ~13% of unclassified repeats in Drosophila species. Our findings suggest this RE-annotation bottleneck, driven largely by uneven taxonomic representation in RE reference databases, is worsening. Although the diversity of available insect genomes has rapidly expanded, the rate of community contributions to RE databases (essential for RE annotation) has not kept pace, preventing high resolution study of REs in most groups. We highlight the tremendous opportunity and need for the field of biodiversity genomics to embrace REs and suggest collective steps for making progress towards this goal.

Genomics, Population Divergence, and Historical Demography of the World's Largest and Endangered Butterfly, The Queen Alexandra's Birdwing

“…This proportion of repeats is relatively high compared to other Papilionidae genomes already available (22% in Papilio glaucus , 22.4% in Papilio xuthus ; Cong et al 2015 ; Lu et al 2019 ), except for the species with larger genomes such as P. bianor (55%; Lu et al 2019 ) and Parnassius apollo (65%; Podsiadlowski et al 2021 ). This is consistent with a positive correlation between assembly size and repeats content in insects ( Petersen et al 2019 ; Heckenhauer et al 2022 ; Sproul et al 2022 ). Within O. alexandrae , all individuals have similar cumulative repeat size, and no difference was detected between lowland and highland individuals despite the fact that highland individuals had a slightly larger genome assembly than lowland individuals (∼5 Mb, supplementary table S2, Supplementary Material online).…”

Exploring chromosome evolution in 250 million year old groups of dragonflies and damselflies (Insecta:Odonata)

“…The calculated proportions of repetitive elements (including unclassified repetitive elements) in the utilized genomes fell well within the range of what has been found in non-model Insecta (Sproul et al, 2022).…”

Satellite DNAs—From Localized to Highly Dispersed Genome Components

“…It is, thus, more and more evident that a complete understanding of every eukaryotic genome is possible with only a detailed insight into its repetitive fraction. This is not an easy task, and, in general, we are still far from full comprehension regarding repetitive DNA genomics and their diversity (for example, [ 21 ]). Nevertheless, the burst of methodological approaches in recent years significantly accelerated the accumulation of previously inaccessible data, broadened the number of attended species and detected repetitive DNA families, changing the views and established concepts (reviewed in [ 6 , 8 , 10 , 18 , 22 , 23 ]).…”