Insights into the genomic evolution of insects from cricket genomes

Guillem Ylla,Atsushi Toyoda,Sumihare Noji,Yoshiyasu Ishimaru,Sayuri Tomonari,Takahito Watanabe,Yuji Matsuoka,Rei Kajitani,Masao Fuketa,Taro Nakamura,Tetsuya Bando,Cassandra G Extavour,Austen A Barnett,Taro Mito,Takehiko Itoh

doi:10.1038/s42003-021-02197-9

Abstract

Most of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation. In contrast, Hemimetabolous insects undergo the presumed ancestral process of incomplete metamorphosis, and have larger genomes with high levels of DNA methylation. Hemimetabolous species from the Orthopteran order (grasshoppers and crickets) have some of the largest known insect genomes. What drives the evolution of these unusual insect genome sizes, remains unknown. Here we report the sequencing, assembly and annotation of the 1.66-Gb genome of the Mediterranean field cricket Gryllus bimaculatus, and the annotation of the 1.60-Gb genome of the Hawaiian cricket Laupala kohalensis. We compare these two cricket genomes with those of 14 additional insects and find evidence that hemimetabolous genomes expanded due to transposable element activity. Based on the ratio of observed to expected CpG sites, we find higher conservation and stronger purifying selection of methylated genes than non-methylated genes. Finally, our analysis suggests an expansion of the pickpocket class V gene family in crickets, which we speculate might play a role in the evolution of cricket courtship, including their characteristic chirping.

Highlights

Most of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation
The 1.66 Gb size predicted by the assembly is similar in size to a previous estimation of 1.68 Gb, obtained from a k-mer analysis performed on an independent dataset (Supplementary Note 1). 50% of the genome is contained within the 71 longest scaffolds (L50), the shortest of them having a length of 6.3 Mb (N50), and 90% of the genome is contained within 307 scaffolds (L90)
Since the first sequenced insect genome, that of D. melanogaster, was made publicly available in 200031, the field of holometabolous genomics has flourished, and this clade became the main source of subsequent genomic information for insects

Summary

Introduction

Most of our knowledge of insect genomes comes from Holometabolous species, which undergo complete metamorphosis and have genomes typically under 2 Gb with little signs of DNA methylation. 1234567890():,; Much of what we know about insect genome structure and evolution comes from examination of the genomes of insects belonging to a single clade, the Holometabola This group includes species such as flies and beetles, and is characterized by undergoing complete, or holometabolous, metamorphosis. While most holometabolan species have relatively small genomes (0.2–1.5 pg), hemimetabolous species, and polyneopterans (a taxon comprising ten major hemimetabolous orders of winged insects with fan-like extensions of the hind wings), display a much larger range of genome sizes (up to 8 pg)[3]. This has led to the hypothesis that there is a genome size threshold at 2 pg (~2 Gb) for holometabolan insect genomes[3]. The role of DNA methylation in polyneopteran species, and why it appears to have been lost in many holometabolans, is not clear

Methods

Results

Conclusion