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Mitochondrial Genomes from Two Specialized Subfamilies of Reduviidae (Insecta: Hemiptera) Reveal Novel Gene Rearrangements of True Bugs.

ABSTRACT: Reduviidae, a hyper-diverse family, comprise 25 subfamilies with nearly 7000 species and include many natural enemies of crop pests and vectors of human disease. To date, 75 mitochondrial genomes (mitogenomes) of assassin bugs from only 11 subfamilies have been reported. The limited sampling of mitogenome at higher categories hinders a deep understanding of mitogenome evolution and reduviid phylogeny. In this study, the first mitogenomes of Holoptilinae (Ptilocnemus lemur) and Emesinae (Ischnobaenella hainana) were sequenced. Two novel gene orders were detected in the newly sequenced mitogenomes. Combined 421 heteropteran mitogenomes, we identified 21 different gene orders and six gene rearrangement units located in three gene blocks. Comparative analyses of the diversity of gene order for each unit reveal that the tRNA gene cluster trnI-trnQ-trnM is the hotspot of heteropteran gene rearrangement. Furthermore, combined analyses of the gene rearrangement richness of each unit and the whole mitogenome among heteropteran lineages confirm Reduviidae as a 'hot-spot group' of gene rearrangement in Heteroptera. The phylogenetic analyses corroborate the current view of phylogenetic relationships between basal groups of Reduviidae with high support values. Our study provides deeper insights into the evolution of mitochondrial gene arrangement in Heteroptera and the early divergence of reduviids.

SUBMITTER: Ye F

PROVIDER: S-EPMC8392325 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Assassin bugs are one of the most successful clades of predatory animals based on their species numbers (∼6,800 spp.) and wide distribution in terrestrial ecosystems. Various novel prey capture strategies and remarkable prey specializations contribute to their appeal as a model to study evolutionary pathways involved in predation. Here, we reconstruct the most comprehensive reduviid phylogeny (178 taxa, 18 subfamilies) to date based on molecular data (5 markers). This phylogeny tests current hypotheses on reduviid relationships emphasizing the polyphyletic Reduviinae and the blood-feeding, disease-vectoring Triatominae, and allows us, for the first time in assassin bugs, to reconstruct ancestral states of prey associations and microhabitats. Using a fossil-calibrated molecular tree, we estimated divergence times for key events in the evolutionary history of Reduviidae. Our results indicate that the polyphyletic Reduviinae fall into 11-14 separate clades. Triatominae are paraphyletic with respect to the reduviine genus Opisthacidius in the maximum likelihood analyses; this result is in contrast to prior hypotheses that found Triatominae to be monophyletic or polyphyletic and may be due to the more comprehensive taxon and character sampling in this study. The evolution of blood-feeding may thus have occurred once or twice independently among predatory assassin bugs. All prey specialists evolved from generalist ancestors, with multiple evolutionary origins of termite and ant specializations. A bark-associated life style on tree trunks is ancestral for most of the lineages of Higher Reduviidae; living on foliage has evolved at least six times independently. Reduviidae originated in the Middle Jurassic (178 Ma), but significant lineage diversification only began in the Late Cretaceous (97 Ma). The integration of molecular phylogenetics with fossil and life history data as presented in this paper provides insights into the evolutionary history of reduviids and clears the way for in-depth evolutionary hypothesis testing in one of the most speciose clades of predators.

Project description:BackgroundMost previous studies of morphological and molecular data have consistently supported the monophyly of the true water bugs (Hemiptera: Nepomorpha). An exception is a recent study by Hua et al. (BMC Evol Biol 9: 134, 2009) based on nine nepomorphan mitochondrial genomes. In the analysis of Hua et al. (BMC Evol Biol 9: 134, 2009), the water bugs in the group Pleoidea formed the sister group to a clade that consisted of Nepomorpha (the remaining true water bugs) + Leptopodomorpha (shore bugs) + Cimicomorpha (assassin bugs and relatives) + Pentatomomorpha (stink bugs and relatives), thereby suggesting that fully aquatic hemipterans evolved independently at least twice. Based on these results, Hua et al. (BMC Evol Biol 9: 134, 2009) elevated the Pleoidea to a new infraorder, the Plemorpha.ResultsOur reanalysis suggests that the lack of support for the monophyly of the true water bugs (including Pleoidea) by Hua et al. (BMC Evol Biol 9: 134, 2009) likely resulted from inadequate taxon sampling. In particular, long-branch attraction (LBA) between the distant outgroup taxa and Pleoidea, as well as LBA among taxa in the ingroup, made Nepomorpha appear to be polyphyletic. We used three complementary strategies to test and alleviate the effects of LBA: (1) the removal of distant outgroups from the analysis; (2) the addition of closely related outgroups; and (3) the addition of a mitochondrial genome from a second family of Pleoidea. We also performed likelihood-ratio tests to examine the support for monophyly of Nepomorpha with different combinations of taxa included in the analysis. Furthermore, we found that specimens of Helotrephes sp. were misidentified as Paraplea frontalis (Fieber, 1844) by Hua et al. (BMC Evol Biol 9: 134, 2009).ConclusionsAll analyses that included the addition of more taxa significantly and consistently supported the placement of Pleoidea within the Nepomorpha (i.e., supported the monophyly of the traditional true water bugs). Our analyses further support a close relationship between Notonectoidea and Pleoidea within Nepomorpha, and the superfamilies Nepoidea, Ochteroidea, Naucoroidea, and Pleoidea are resolved as monophyletic in all trees with strong support. Our results also confirmed that monophyly of Nepomorpha clearly is not refuted by the mitochondrial genome data.

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Mitochondrial Genomes from Two Specialized Subfamilies of Reduviidae (Insecta: Hemiptera) Reveal Novel Gene Rearrangements of True Bugs.

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