Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2021 Jun 14;4(1):733.
doi: 10.1038/s42003-021-02197-9.

Insights into the genomic evolution of insects from cricket genomes

Guillem Ylla  1 , Taro Nakamura  2   3 , Takehiko Itoh  4 , Rei Kajitani  4 , Atsushi Toyoda  5   6 , Sayuri Tomonari  7 , Tetsuya Bando  8 , Yoshiyasu Ishimaru  7 , Takahito Watanabe  7 , Masao Fuketa  9 , Yuji Matsuoka  7   10 , Austen A Barnett  2   11 , Sumihare Noji  7 , Taro Mito  12 , Cassandra G Extavour  13   14
Affiliations

Insights into the genomic evolution of insects from cricket genomes

Guillem Ylla et al. Commun Biol. .

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.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. The G. bimaculatus genome.
a The cricket G. bimaculatus (top and side views of an adult male), commonly called the two-spotted cricket, owes its name to the two yellow spots on the base of the forewings. b Circular representation of the G. bimaculatus genome, displaying the N50 (pink) and N90 (purple) scaffolds, repetitive content density (green), the high- (yellow) and low- (light blue) CpGo/e value genes, pickpocket gene clusters (dark blue), and gene density (orange). c The proportion of the genome made up of transposable elements (TEs) is similar between G. bimaculatus and L. kohalensis (28.9 and 34.5%, respectively), but the specific TE family composition varies widely between the two species.
Fig. 2
Fig. 2. CpGo/e bimodal distribution across distant insects.
a The distribution of CpGo/e values within the CDS regions displays a bimodal distribution in the two cricket species studied here, as well as in the honeybee A. mellifera and the thrips F. occidentalis. We modeled each peak with a normal distribution and defined their intersection (red line) as a threshold to separate genes into low- and high- CpGo/e value categories, represented in yellow and blue respectively. b UpSet plot showing the top three intersections (linked dots) in terms of the number of orthogroups (OGs) commonly present in the same category (low- and high- CpG o/e) across the four insect species. The largest intersection corresponds to 2182 OGs whose genes have low CpGo/e in the four insect species, followed by the 728 OGs whose genes have high CpGo/e levels in all four species, and 666 OGs whose genes have low CpGo/e in the three hemimetabolous species and high CpGo/e in the holometabolous honeybee. Extended plot with 50 intersections is shown in Supplementary Fig. 4. c Percentage of species-specific genes within low CpGo/e (yellow) and high CpGo/e.(blue) categories in each insect, indicating that more such genes tend to have high CpGo/e values. d One-to-one orthologous genes with low CpGo/e values in both crickets have significantly lower dN/dS values than genes with high CpGo/e values.
Fig. 3
Fig. 3. Functional differences between high- and low- CpGo/e genes.
Enriched GO terms with a p value <0.00001 in at least one of the eight categories, which are high CpGo/e and low CpGo/e genes of G. bimaculatus, L. kohalensis, F. occidentalis, and A. mellifera, respectively. The dot diameter is proportional to the percentage of significant genes with that GO term within the gene set. The dot color represents the p value level: blue >0.05, orange [0.05, 0.001), red <0.001. Extended figure with all significant GO terms (p value <0.05) available as Supplementary Fig. 3.
Fig. 4
Fig. 4. Cricket genomes in the context of insect evolution.
A phylogenetic tree including 16 insect species calibrated at four different time points (red watch symbols) based on Misof et al. (2014), suggests that G. bimaculatus and L. kohalensis diverged ca. 89.2 Mya. The number of expanded (blue text) and contracted (red text) gene families is shown for each insect, and for the branches leading to crickets. The density plots show the CpGo/e distribution for all genes for each species. The genome size in Gb was obtained from the genome fasta files (Supplementary Data 1).
Fig. 5
Fig. 5. The pickpocket gene family class V is expanded in crickets.
pickpocket gene tree with all the genes belonging to the seven OGs that contain the D. melanogaster pickpocket genes. All OGs predominantly contain members of a single ppk family. The OG0000167 orthogroup contains members of two pickpocket classes, II and VI. The orthogroup OG0000072 containing most pickpocket class V genes (circular cladogram) was significantly expanded in crickets relative to other insects.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Belles, X. Origin and Evolution of Insect Metamorphosis (John Wiley & Sons, Ltd, 2011).
    1. Engel MS, Grimaldi DA. New light shed on the oldest insect. Nature. 2004;427:627–630. doi: 10.1038/nature02291. - DOI - PubMed
    1. Gregory TR. Genome size and developmental complexity. Genetica. 2002;115:131–146. doi: 10.1023/A:1016032400147. - DOI - PubMed
    1. Camacho JP, et al. A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs. Chromosoma. 2015;124:263–275. doi: 10.1007/s00412-014-0499-0. - DOI - PubMed
    1. Bewick AJ, Vogel KJ, Moore AJ, Schmitz RJ. Evolution of DNA methylation across insects. Mol. Biol. Evol. 2016;34:654–665. - PMC - PubMed

Publication types

Substances

-