Evolution of mitogenomic gene order in Orthoptera

Abstract

Mitochondrial gene order has contributed to the elucidation of evolutionary relationships in several animal groups. It generally has found its application as a phylogenetic marker for deep nodes. Yet, in Orthoptera limited research has been performed on the gene order, although the group represents one of the oldest insect orders. We performed a comprehensive study on mitochondrial genome rearrangements (MTRs) within Orthoptera in the context of mitogenomic sequence-based phylogeny. We used 280 published mitogenome sequences from 256 species, including three outgroup species, to reconstruct a molecular phylogeny. Using a heuristic approach, we assigned MTR scenarios to the edges of the phylogenetic tree and reconstructed ancestral gene orders to identify possible synapomorphies in Orthoptera. We found all types of MTRs in our dataset: inversions, transpositions, inverse transpositions, and tandem-duplication/random loss events (TDRL). Most of the suggested MTRs were in single and unrelated species. Out of five MTRs which were unique in subgroups of Orthoptera, we suggest four of them to be synapomorphies; those were in the infraorder Acrididea, in the tribe Holochlorini, in the subfamily Pseudophyllinae, and in the two families Phalangopsidae and Gryllidae or their common ancestor (leading to the relationship ((Phalangopsidae + Gryllidae) + Trigonidiidae)). However, similar MTRs have been found in distant insect lineages. Our findings suggest convergent evolution of specific mitochondrial gene orders in several species, deviant from the evolution of the mitogenome DNA sequence. As most MTRs were detected at terminal nodes, a phylogenetic inference of deeper nodes based on MTRs is not supported. Hence, the marker does not seem to aid resolving the phylogeny of Orthoptera, but adds further evidence for the complex evolution of the whole group, especially at the genetic and genomic levels.The results indicate a high demand for more research on patterns and underlying mechanisms of MTR events in Orthoptera.

Phylomitogenomics of two Neotropical species of long-legged crickets Endecous Saussure, 1878 (Orthoptera: Phalangopsidae)

“…In our study, we observed discrepancies between the ML and BI analyses, and as previously observed, the BI trees exhibited higher support ( Ma and Miao, 2022 ). However, one discrepancy involves the positioning of the Myrmecophilus and Ornebius genera, where the ML tree was consistent with findings from previous studies ( Yang et al, 2021 ; Dan et al, 2022 ; Ma and Miao, 2022 ; Gaugel et al, 2023 ). Incorporating the third codon position might lead to more robust tree topologies ( Ma and Miao, 2022 ).…”

“…This type is characterized by featuring the typical trnN-trnS1-trnE gene order and the transposition of trnV to the site between 12S and the T+A-rich region ( Ma and Li, 2018 ). The trnV relocation is also observed in Trigonidiidae, implying that it occurred independently in these two branches ( Gaugel et al, 2023 ). Moreover, Type IVG differs from Type IV described by Dan et al .…”

“…These genes comprise 13 protein-coding genes (PCGs), 22 transfer RNAs (tRNA), two ribosomal RNA (rRNA), and a T+A-rich region ( Flook et al, 1995 ; Boore, 1999 ; Kim et al, 2005 ; Sheffield et al, 2010 ). This region is the site for replication and transcription initiation and displays high variability across insect species ( Boore and Brown, 1998 ; Fenn et al, 2008 ; Gaugel et al, 2023 ). Mitogenomes are generally haploid with maternal inheritance and exhibit a pronounced AT-bias, characterized by a high percentage of thymine and adenine ( Flook et al ., 1995 ; Fenn et al ., 2007 ; Erler et al, 2010 ; Sheffield et al ., 2010 ).…”

“…The first assembled orthopteran mitogenome was of Locusta migratoria (Caelifera), characterized by a 76% AT content ( Flook et al, 1995 ). Despite limited knowledge about many groups of Orthoptera, events such as inversions, transpositions, and gene duplications and losses have been documented ( Ma and Li, 2018 ; Yang et al, 2021 ; Gaugel et al, 2023 ).…”

Species delimitation and molecular phylogeny of the grasshopper subfamily Gomphocerinae (Orthoptera: Acrididae) from Algeria based on mitochondrial and nuclear DNA markers

“…The phylogenetic position of Chorthippus marocanus aligns with the classification adopted in the Orthoptera Species File, which places it within the species group biguttulus (Linnaeus, 1758). The complex relationships within the Gomphocerini tribe have been previously observed and explained in various molecular studies (e.g., Dumas et al 2010;Nattier et al 2011;Vedenina and Mugue 2011;Hawlitschek et al 2017;Sukhikh et al 2019;Nolen et al 2020;Hawlitschek et al 2022Hawlitschek et al , 2023Gaugel et al 2023). Additionally, Hodjat and Saboori (2021) addressed the challenges and instability in the taxonomic classification of Gomphocerini species, attributing them to variations and plasticity in morphological characteristics, behaviour and acoustic communication influenced by environmental stress and hybridisation between populations.…”