Insights into the genomic evolution of insects from cricket genomes

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.

Dissecting cricket genomes for the advancement of entomology and entomophagy

“…Cricket genomes have been ever studied in various contexts, such as evolutionary biology, developmental and regenerative biology, and even entomophagy (Table 1). Out of the seven Orthoptera genomes registered in the National Center of Biotechnology Information (NCBI) Genome, the cricket genome that is currently sequenced consists of six species, namely Laupala kohalensis (Blankers et al 2018a), Teleogryllus oceanicus (Pascoal et al 2019), T. occipitalis (Kataoka et al 2020, Gryllus bimaculatus (Ylla et al 2021), Acheta domesticus (Gupta et al 2020), and Apteronemobius asahinai (Satoh et al 2021). The assembled size of current version of A. domesticus genomes registered in the NCBI (about 1.0 Gbp, GCA_014858955.1) is far less from Gupta et al 2020).…”

“…Furthermore, the QTLs associated with male mating songs and female preference have been shown to be closely coupled, suggesting genetic coupling, and include genes underlying variation in song and preference divergence, such as genes involved in the neuronal formation, rhythmic muscle activities, and signal processing in auditory systems (Xu and Shaw, 2019;Xu and Shaw, 2021). Recent analysis on gene family expansion/contraction has revealed the cricket-specific pickpocket gene family, which encodes ion channels and is involved in locomotion, neural modulation, and muscle development (Younger et al 2013;Hill et al 2017;Ylla et al 2021). L. kohalensis has been shown to contain pickpocket genes in a genomic region associated with changes in song rhythm, possibly suggesting that song production in crickets is likely to be regulated by ion channels (Ylla et al 2021).…”

“…Recent analysis on gene family expansion/contraction has revealed the cricket-specific pickpocket gene family, which encodes ion channels and is involved in locomotion, neural modulation, and muscle development (Younger et al 2013;Hill et al 2017;Ylla et al 2021). L. kohalensis has been shown to contain pickpocket genes in a genomic region associated with changes in song rhythm, possibly suggesting that song production in crickets is likely to be regulated by ion channels (Ylla et al 2021).…”

“…The two-spotted cricket Gryllus bimaculatus and house cricket Acheta domesticus are probably the most widely distributed food and feed crickets in the world today. As of November 2021, genome information of G. bimaculatus and transcriptome information of A. domesticus are available (Oppert et al 2020;Ylla et al 2021). Crickets are rich in nutrients, but this value could be further enhanced by improving their vitamin content and production of Omega-3 fatty acids.…”

Evolutionary dynamics of sex‐biased genes expressed in cricket brains and gonads

“…The CDS of our main target species G. bimaculatus were obtained from its recently available genome (Ylla et al, 2021). The annotated genome had 17,714 predicted transcripts (after selecting the longest CDS per gene; (Ylla et al, 2021)). For this gene set, we extracted the CDS with a start codon, no ambiguous nucleotides, and at least 150bp in length, yielding 15,539 CDS for study (mean length = 417.0 codons/CDS ± 3.5 (standard error [SE])) for G. bimaculatus.…”