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Comparative Mitogenomic Analysis of Heptageniid Mayflies (Insecta: Ephemeroptera): Conserved Intergenic Spacer and tRNA Gene Duplication.

ABSTRACT: Large intergenic spacers and tRNA gene duplications have been reported in several insect groups, although little is known about mitogenomes of mayflies. Here, we determined complete mitogenomes of ten heptageniid species and systemically analyzed their mitogenomic features. Both a conserved intergenic spacer (IGS) and trnM duplication were detected in those mitogenomes. The IGS, which was observed in heptageniids, could be further folded into a stable stem-loop structure. The tRNA gene duplication was found in almost all analyzed mitogenomes, and a unique gene block trnI-trnM-trnQ-trnM-ND2 was also discovered. Our analysis demonstrates that the heptageniid gene arrangement pattern can be explained by the tandem duplication-random loss (TDRL) model. Phylogenetic analyses using both Bayesian inference (BI) and maximum likelihood (ML) methods based on the nucleotide and amino acid sequence data recovered the genus Epeorus as monophyletic with strong support. Our results provide a better understanding of mitogenomic evolution in Heptageniidae, as well as novel molecular markers for species identification of mayflies.

SUBMITTER: Li R

PROVIDER: S-EPMC7920270 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundMayflies are basal winged insects of crucial importance for the understanding of the early evolution of Pterygota. Unlike all other insects, they have two successive winged stages, the subimago and the imago. Their forewings feature so-called bullae, which are desclerotized spots in the anterior main veins. Up to now, they have been considered to play a major role in wing bending during flight.ResultsWe investigated bullae by multiple methods to reveal their structure and arrangement and to gain new information on the evolution of insect flight. Bullae are mostly present in the anterior negative wing veins, disrupting the otherwise rigid veins. High-speed videography reveals that mayfly wings do not bend during flight. Likewise, different arrangements of bullae in different species do not correlate with different modes of flying. Observations on the moulting of subimagines unravel that they are essential for wing bending during the extraction of the imaginal wing from the subimaginal cuticle. Bullae define predetermined bending lines, which, together with a highly flexible wing membrane enriched with resilin, permit wing bending during subimaginal moulting. Bullae are only absent in those species that remain in the subimaginal stage or that use modified modes of moulting. Bullae are also visible in fossil mayflies and can be traced back to stemgroup mayflies of the Early Permian, the 270 million years old Protereismatidae, which most probably had bullae in both fore- and hind wings.ConclusionsBullae in mayfly wings do not play a role in flight as previously thought, but are crucial for wing bending during subimaginal moulting. Thus, the presence of bullae is a reliable morphological marker for a subimaginal life stage, confirming the existence of the subimago already in Permian Protereismatidae. A thorough search for bullae in fossils of other pterygote lineages may reveal wheather they also had subimagines and at what point in evolution this life stage was lost. In mayflies, however, the subimago may have been retained due to selective advantages in connection with the transition from aquatic to terrestrial life or due to morphological requirements for a specialized mating flight.

Project description:BackgroundInsect mitochondrial genomes (mitogenomes) are the most extensively used genetic marker for evolutionary and population genetics studies of insects. The Pentatomoidea superfamily is economically important and the largest superfamily within Pentatomomorpha with over 7,000 species. To better understand the diversity and evolution of pentatomoid species, we sequenced and annotated the mitogenomes of Eurydema gebleri and Rubiconia intermedia, and present the first comparative analysis of the 11 pentatomoid mitogenomes that have been sequenced to date.ResultsWe obtained the complete mitogenome of Eurydema gebleri (16,005 bp) and a nearly complete mitogenome of Rubiconia intermedia (14,967 bp). Our results show that gene content, gene arrangement, base composition, codon usage, and mitochondrial transcription termination factor sequences are highly conserved in pentatomoid species, especially for species in the same family. Evolutionary rate analyses of protein-coding genes reveal that the highest and lowest rates are found in atp8 and cox1 and distinctive evolutionary patterns are significantly correlated with the G + C content of genes. We inferred the secondary structures for two rRNA genes for eleven pentatomoid species, and identify some conserved motifs of RNA structures in Pentatomidea. All tRNA genes in pentatomoid mitogenomes have a canonical cloverleaf secondary structure, except for two tRNAs (trnS1 and trnV) which appear to lack the dihydrouridine arm. Regions that are A + T-rich have several distinct characteristics (e.g. size variation and abundant tandem repeats), and have potential as species or population level molecular markers. Phylogenetic analyses based on mitogenomic data strongly support the monophyly of Pentatomoidea, and the estimated phylogenetic relationships are: (Urostylididae + (Plataspidae + (Pentatomidae + (Cydnidae + (Dinidoridae + Tessaratomidae))))).ConclusionsThis comparative mitogenomic analysis sheds light on the architecture and evolution of mitogenomes in the superfamily Pentatomoidea. Mitogenomes can be effectively used to resolve phylogenetic relationships of pentatomomorphan insects at various taxonomic levels. Sequencing more mitogenomes at various taxonomic levels, particularly from closely related species, will improve the annotation accuracy of mitochondrial genes, as well as greatly enhance our understanding of mitogenomic evolution and phylogenetic relationships in pentatomoids.

Dataset Information

Comparative Mitogenomic Analysis of Heptageniid Mayflies (Insecta: Ephemeroptera): Conserved Intergenic Spacer and tRNA Gene Duplication.

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