Comparative Analysis of Mitochondrial Genomes in Gryllidea (Insecta: Orthoptera): Implications for Adaptive Evolution in Ant-Loving Crickets

Abstract

Species of infraorder Gryllidea, or crickets, are useful invertebrate models for studying developmental biology and neuroscience. They have also attracted attention as alternative protein sources for human food and animal feed. Mitochondrial genomic information on related invertebrates, such as katydids, and locusts, has recently become available in attempt to clarify the controversial classification schemes, although robust phylogenetic relationships with emphasis on crickets remain elusive. Here, we report newly sequenced complete mitochondrial genomes of crickets to study their phylogeny, genomic rearrangements, and adaptive evolution. First, we conducted de novo assembly of mitochondrial genomes from eight cricket species and annotated protein-coding genes (PCGs) and transfer and ribosomal RNAs using automatic annotations and manual curation. Next, by combining newly described PCGs with public data of the complete Gryllidea genomes and gene annotations, we performed phylogenetic analysis and found gene order rearrangements in several branches. We further analyzed genetic signatures of selection in ant-loving crickets (Myrmecophilidae), which are small wingless crickets that inhabit ant nests. Three distinct approaches revealed two positively selected sites in the cox1 gene in these crickets. Protein 3D structural analyses suggested that these selected sites could influence the interaction of respiratory complex proteins, conferring benefits to ant-loving crickets with a unique ecological niche and morphology. These findings enhance our understanding of the genetic basis of cricket evolution without relying on estimates based on a limited number of molecular markers.

Mitogenomic Comparison of the Mole Crickets Gryllotalpidae with the Phylogenetic Implications (Orthoptera: Ensifera)

“…A similar situation was observed between P12 and P12R trees, reflecting that the exclusion of the rRNA genes can improve branch supports of phylogenetic trees. The monophyly of the infraorder Gryllidea was well supported by all datasets with high nodal supports (PPs = 1; BSs = 100), and consistent with the results proposed by Chintauan-Marquier et al [ 17 ], Zhou et al [ 48 ], Chang et al [ 10 ], Song et al [ 8 ] and Sanno et al [ 18 ].…”

“…Most of them are complete triplet bases TAA/TAG, and others are incomplete T/TA immediately followed by or partially overlapped with a tRNA gene. Incomplete stop codons are fairly common in the orthopteran mitogenomes and can be converted into a potential stop codon via polyadenylation to TAA [ 18 , 39 , 40 , 55 ]. The results of RSCU analyses show that the PCGs exhibit strong biases toward the nucleotides A and U in the codon usage.…”

“…Owing to the limited molecular data, the phylogenetic position of Gryllotalpidae in Gryllidea is still controversial. Gryllotalpidae is sister to Myrmecophilidae based on multilocus analysis [ 17 ], but has conflicting phylogenetic positions in mitogenome-based trees [ 8 , 18 ].…”

Dissecting cricket genomes for the advancement of entomology and entomophagy

“…2). Recent studies using the mitochondrial genome and a combination of nuclear and mitochondrial genes have shown that Grylloidea and Gryllotalpoidea are monophyletic sister groups (Song et al 2015;Chintauan-Marquier et al 2016;Zhou et al 2017;Yang et al 2021;Sanno et al 2021). However, other studies or approaches have either not confirmed this relationship or have produced conflicting phylogenetic relationships (Song et al 2020;Sanno et al 2021).…”

“…Recent studies using the mitochondrial genome and a combination of nuclear and mitochondrial genes have shown that Grylloidea and Gryllotalpoidea are monophyletic sister groups (Song et al 2015;Chintauan-Marquier et al 2016;Zhou et al 2017;Yang et al 2021;Sanno et al 2021). However, other studies or approaches have either not confirmed this relationship or have produced conflicting phylogenetic relationships (Song et al 2020;Sanno et al 2021). To fully understand the phylogenetic relationship between Grylloidea and Gryllotalpoidea, we need genome sequences of a wide range of species included in this infraorder, which enable usage of single-copy gene sequences for building Fig.…”