Comparative Analysis of the Mitochondrial Genomes of Three Species of Yangiella (Hemiptera: Aradidae) and the Phylogenetic Implications of Aradidae
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Specimen Collection, Extraction, and Sequencing
2.2. Gene Assembly, Annotation, and Analysis
2.3. Phylogenetic Analysis
2.4. Divergence Time Estimation
3. Results
3.1. General Characteristics of the Mitochondrial Genome of the Genus Yangiella
3.2. Codon Preference Analysis
3.3. Neutrality Plot Analysis and ENC-Plot Analysis
3.4. Base Substitution Saturation Analysis
3.5. Nucleotide Diversity (Pi) and Nonsynonymous (Ka)/Synonymous (Ks) Mutation Rate Ratios
3.6. Heterogeneity Analysis
3.7. Phylogenetic Analyses
3.8. Divergence Time Estimation
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
- Grebennikov, V.V.; Heiss, E. DNA barcoding of flat bugs (Hemiptera: Aradidae) with phylogenetic implications. Arthropod Syst. Phylog. 2014, 72, 213–219. [Google Scholar] [CrossRef]
- Kormilev, N.A.; Froeschner, R.C. Flat bugs of the world. A synonymic list (Heteroptera: Aradidae). Entomography 1987, 5, 1–246. [Google Scholar]
- Hsiao, T.Y. Results of the zoologico-botanical expedition to Southwest China 1955–1957. Acta Entomol. Sinica 1964, 13, 587–605. [Google Scholar]
- Heikkala, O.; Martikainen, P.; Kouki, J. Prescribed burning is an effective and quick method to conserve rare pyrophilous forest-dwelling flat bugs. Insect Conserv. Divers. 2017, 10, 32–41. [Google Scholar] [CrossRef]
- Zhang, W.; Bai, X.; Heiss, E.; Cai, W. Notes on Yangiella Hsiao (Hemiptera: Aradidae: Mezirinae), with description of a new species from China. Zootaxa 2010, 2530, 29–38. [Google Scholar] [CrossRef]
- Liu, Y.Q.; Li, H.; Song, F.; Zhao, Y.S.; Wilson, J.J.; Cai, W.Z. Higher-level phylogeny and evolutionary history of Pentatomomorpha (Hemiptera: Heteroptera) inferred from mitochondrial genome sequences. Syst. Entomol. 2019, 44, 810–819. [Google Scholar] [CrossRef]
- Li, Q.; Yang, L.X.; Xiang, D.B.; Wan, Y.; Wu, Q.; Huang, W.L.; Zhao, G. The complete mitochondrial genomes of two model ectomycorrhizal fungi (Laccaria): Features, intron dynamics and phylogenetic implications. Int. J. Biol. Macromol. 2020, 145, 974–984. [Google Scholar] [CrossRef]
- Cameron, S.L. Insect mitochondrial genomics: Implications for evolution and phylogeny. Annu. Rev. Entomol. 2014, 59, 95–117. [Google Scholar] [CrossRef] [PubMed]
- Song, S.N.; Tang, P.; Wei, S.J.; Chen, X.X. Comparative and phylogenetic analysis of the mitochondrial genomes in basal hymenopterans. Sci. Rep. 2016, 6, 20972. [Google Scholar] [CrossRef]
- Wolstenholme, D.R. Animal mitochondrial DNA: Structure and evolution. Int. Rev. Cytol. 1992, 141, 173–216. [Google Scholar]
- Zhang, D.X.; Hewitt, G.M. Insect mitochondrial control region: A review of its structure, evolution and usefulness in evolutionary studies. Biochem. Syst. Ecol. 1997, 25, 99–120. [Google Scholar] [CrossRef]
- Heiss, E.; Grebennikov, V. Monophyly, review, six new species and DNA barcode of micropterous Afromontane Afropictinus (Heteroptera: Aradidae). Zootaxa 2016, 4208, 149–160. [Google Scholar] [CrossRef] [PubMed]
- Grebennikov, V.V.; Heiss, E. Survey and DNA barcoding of flat bugs (Hemiptera: Aradidae) in the Tanzanian Forest Archipelago reveal a phylogeographically structured fauna largely unknown at the species level. Eur. J. Entomol. 2018, 115, 512–523. [Google Scholar] [CrossRef]
- Marchal, L.; Guilbert, E. Cladistic analysis of Aradidae (Insecta, Heteroptera) based on morphological and molecular characters. Zool. Scr. 2016, 45, 273–285. [Google Scholar] [CrossRef]
- Yan, Z.T.; Fan, Z.H.; He, S.L.; Wang, X.Q.; Chen, B.; Luo, S.T. Mitogenomes of Eight Nymphalidae Butterfly Species and Reconstructed Phylogeny of Nymphalidae (Nymphalidae: Lepidoptera). Genes 2023, 14, 1018. [Google Scholar] [CrossRef] [PubMed]
- Fenn, J.D.; Song, H.; Cameron, S.L.; Whiting, M.F. A preliminary mitochondrial genome phylogeny of Orthoptera (Insecta) and approaches to maximizing phylogenetic signal found within mitochondrial genome data. Mol. Phylogenet. Evol. 2008, 49, 59–68. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Zhou, Y.; Chen, Y.; Gu, J. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018, 34, 884–890. [Google Scholar] [CrossRef] [PubMed]
- Bankevich, A.; Nurk, S.; Antipov, D.; Gurevich, A.A.; Dvorkin, M.; Kulikov, A.S.; Lesin, V.M.; Nikolenko, S.I.; Son, P.; Prjibelski, A.D.; et al. SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. J. Comput. Biol. 2012, 19, 455–477. [Google Scholar] [CrossRef]
- Donath, A.; Juehling, F.; Al-Arab, M.; Bernhart, S.H.; Reinhardt, F.; Stadler, P.F.; Middendorf, M.; Bernt, M. Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes. Nucleic Acids Res. 2019, 47, 10543–10552. [Google Scholar] [CrossRef]
- Kearse, M.; Moir, R.; Wilson, A.; Stones-Havas, S.; Cheung, M.; Sturrock, S.; Buxton, S.; Cooper, A.; Markowitz, S.; Duran, C.; et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012, 28, 1647–1649. [Google Scholar] [CrossRef]
- Chan, P.P.; Lowe, T.M. tRNAscan-SE: Searching for tRNA Genes in Genomic Sequences. Methods Mol. Biol. 2019, 1962, 1–14. [Google Scholar] [PubMed]
- Grant, J.R.; Stothard, P. The CGView Server: A comparative genomics tool for circular genomes. Nucleic Acids Res. 2008, 36, W181–W184. [Google Scholar] [CrossRef] [PubMed]
- Kumar, S.; Stecher, G.; Li, M.; Knyaz, C.; Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol. Biol. Evol. 2018, 35, 1547–1549. [Google Scholar] [CrossRef] [PubMed]
- Perna, N.T.; Kocher, T.D. Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. J. Mol. Evol. 1995, 41, 353–358. [Google Scholar] [CrossRef] [PubMed]
- Librado, P.; Rozas, J. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25, 1451–1452. [Google Scholar] [CrossRef] [PubMed]
- Sueoka, N. Directional mutation pressure and neutral molecular evolution. Proc. Natl. Acad. Sci. USA 1988, 85, 2653–2657. [Google Scholar] [CrossRef] [PubMed]
- Xiao, Y.; Huang, H.X.; Chen, Y.X.; Zheng, S.; Chen, J.L.; Zou, Z.J.; Mehmood, N.; Ullah, I.; Liao, X.; Wang, J.Y. Insight on genetic features prevalent in five Ipomoea species using comparative codon pattern analysis reveals differences in major codons and reduced GC content at the 5? end of CDS. Biochem. Biophys. Res. Commun. 2023, 657, 92–99. [Google Scholar] [CrossRef] [PubMed]
- Novembre, J.A. Accounting for background nucleotide composition when measuring codon usage bias. Mol. Biol. Evol. 2002, 19, 1390–1394. [Google Scholar] [CrossRef]
- Xia, X. DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution. Mol. Biol. Evol. 2018, 35, 1550–1552. [Google Scholar] [CrossRef]
- Xiang, C.Y.; Gao, F.; Jakovlić, I.; Lei, H.P.; Hu, Y.; Zhang, H.; Zou, H.; Wang, G.T.; Zhang, D. Using PhyloSuite for molecular phylogeny and tree-based analyses. iMeta 2023, 2, e87. [Google Scholar] [CrossRef]
- Nakamura, T.; Yamada, K.D.; Tomii, K.; Katoh, K. Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 2018, 34, 2490–2492. [Google Scholar] [CrossRef] [PubMed]
- Ranwez, V.; Douzery, E.J.P.; Cambon, C.; Chantret, N.; Delsuc, F. MACSE v2: Toolkit for the Alignment of Coding Sequences Accounting for Frameshifts and Stop Codons. Mol. Biol. Evol. 2018, 35, 2582–2584. [Google Scholar] [CrossRef] [PubMed]
- Castresana, J. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 2000, 17, 540–552. [Google Scholar] [CrossRef] [PubMed]
- Capella-Gutiérrez, S.; Silla-Martínez, J.M.; Gabaldón, T. trimAl: A tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009, 25, 1972–1973. [Google Scholar] [CrossRef] [PubMed]
- Kueck, P.; Longo, G.C. FASconCAT-G: Extensive functions for multiple sequence alignment preparations concerning phylogenetic studies. Front. Zool. 2014, 11, 81. [Google Scholar] [CrossRef] [PubMed]
- Kueck, P.; Meid, S.A.; Gross, C.; Waegele, J.W.; Misof, B. AliGROOVE—Visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support. BMC Bioinf. 2014, 15, 294. [Google Scholar] [CrossRef] [PubMed]
- Kalyaanamoorthy, S.; Bui Quang, M.; Wong, T.K.F.; von Haeseler, A.; Jermiin, L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods 2017, 14, 586–588. [Google Scholar] [CrossRef] [PubMed]
- Aberer, A.J.; Kobert, K.; Stamatakis, A. ExaBayes: Massively Parallel Bayesian Tree Inference for the Whole-Genome Era. Mol. Biol. Evol. 2014, 31, 2553–2556. [Google Scholar] [CrossRef] [PubMed]
- Minh, B.Q.; Schmidt, H.A.; Chernomor, O.; Schrempf, D.; Woodhams, M.D.; von Haeseler, A.; Lanfear, R. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol. Biol. Evol. 2020, 37, 1530–1534. [Google Scholar] [CrossRef]
- Hoang, D.T.; Chernomor, O.; von Haeseler, A.; Minh, B.Q.; Vinh, L.S. UFBoot2: Improving the Ultrafast Bootstrap Approximation. Mol. Biol. Evol. 2018, 35, 518–522. [Google Scholar] [CrossRef]
- Xie, J.; Chen, Y.; Cai, G.; Cai, R.; Hu, Z.; Wang, H. Tree Visualization By One Table (tvBOT): A web application for visualizing, modifying and annotating phylogenetic trees. Nucleic Acids Res. 2023, 51, W587–W592. [Google Scholar] [CrossRef] [PubMed]
- Drummond, A.J.; Rambaut, A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7, 214. [Google Scholar] [CrossRef] [PubMed]
- Song, F.; Li, H.; Shao, R.; Shi, A.; Bai, X.; Zheng, X.; Heiss, E.; Cai, W. Rearrangement of mitochondrial tRNA genes in flat bugs (Hemiptera: Aradidae). Sci. Rep. 2016, 6, 25725. [Google Scholar] [CrossRef] [PubMed]
- Lin, Q.B. Late Triassic insect fauna from Toksun, Xinjiang. Acta Pal. Sin. 1992, 31, 313–335. [Google Scholar]
- Rambaut, A.; Drummond, A.J.; Xie, D.; Baele, G.; Suchard, M.A. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst. Biol. 2018, 67, 901–904. [Google Scholar] [CrossRef]
- Dowton, M.; Castro, L.R.; Austin, A.D. Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: The examination of genome ‘morphology’. Invertebr. Syst. 2002, 16, 345–356. [Google Scholar] [CrossRef]
- Shi, A.; Li, H.; Bai, X.; Dai, X.; Chang, J.; Guilbert, E.; Cai, W. The complete mitochondrial genome of the flat bug Aradacanthia heissi (Hemiptera: Aradidae). Zootaxa 2012, 3238, 23–38. [Google Scholar] [CrossRef]
- Xu, S.W.; Wu, Y.F.; Liu, Y.Q.; Zhao, P.; Chen, Z.; Song, F.; Li, H.; Cai, W.Z. Comparative Mitogenomics and Phylogenetic Analyses of Pentatomoidea (Hemiptera: Heteroptera). Genes 2021, 12, 1306. [Google Scholar] [CrossRef]
- Dowton, M.; Cameron, S.L.; Dowavic, J.I.; Austin, A.D.; Whiting, M.F. Characterization of 67 Mitochondrial tRNA Gene Rearrangements in the Hymenoptera Suggests That Mitochondrial tRNA Gene Position Is Selectively Neutral. Mol. Biol. Evol. 2009, 26, 1607–1617. [Google Scholar] [CrossRef]
- Lu, C.C.; Huang, X.L.; Deng, J. Mitochondrial genomes of soft scales (Hemiptera: Coccidae): Features, structures and significance. BMC Genom. 2023, 24, 37. [Google Scholar] [CrossRef]
- Hamilton, W.L.; Claessens, A.; Otto, T.D.; Kekre, M.; Fairhurst, R.M.; Rayner, J.C.; Kwiatkowski, D. Extreme mutation bias and high AT content in Plasmodium falciparum. Nucleic Acids Res. 2017, 45, 1889–1901. [Google Scholar] [PubMed]
- Simon, C.; Frati, F.; Beckenbach, A.; Crespi, B.; Liu, H.; Flook, P. Evolution, Weighting, and Phylogenetic Utility of Mitochondrial Gene Sequences and a Compilation of Conserved Polymerase Chain Reaction Primers. Ann. Entomol. Soc. Am. 1994, 87, 651–701. [Google Scholar] [CrossRef]
- Wei, S.J.; Shi, M.; Chen, X.X.; Sharkey, M.J.; van Achterberg, C.; Ye, G.Y.; He, J.H. New Views on Strand Asymmetry in Insect Mitochondrial Genomes. PLoS ONE 2010, 5, e12708. [Google Scholar] [CrossRef] [PubMed]
- Hassanin, A.; Léger, N.; Deutsch, J. Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Syst. Biol. 2005, 54, 277–298. [Google Scholar] [CrossRef] [PubMed]
- Rousset, F.; Pelandakis, M.; Solignac, M. Evolution of compensatory substitutions through G.U intermediate state in Drosophila rRNA. Proc. Natl. Acad. Sci. USA 1991, 88, 10032–10036. [Google Scholar] [CrossRef] [PubMed]
- Golden, M.; Murrell, B.; Martin, D.; Pybus, O.G.; Hein, J. Evolutionary Analyses of Base-Pairing Interactions in DNA and RNA Secondary Structures. Mol. Biol. Evol. 2020, 37, 576–592. [Google Scholar] [CrossRef] [PubMed]
- Varani, G.; McClain, W.H. The G × U wobble base pair. A fundamental building block of RNA structure crucial to RNA function in diverse biological systems. EMBO Rep. 2000, 1, 18–23. [Google Scholar] [CrossRef] [PubMed]
- Yokobori, S.; Paabo, S. Transfer RNA editing in land snail mitochondria. Proc. Natl. Acad. Sci. USA 1995, 92, 10432–10435. [Google Scholar] [CrossRef] [PubMed]
- Chakraborty, S.; Yengkhom, S.; Uddin, A. Analysis of codon usage bias of chloroplast genes in Oryza species Codon usage of chloroplast genes in Oryza species. Planta 2020, 252, 67. [Google Scholar] [CrossRef] [PubMed]
- Bu, Y.F.; Wu, B.X.; Sun, N.; Man, Y.; Jing, Y.P. Codon usage bias predicts the functional MYB10 gene in Populus. J. Plant Physiol. 2021, 265, 153491. [Google Scholar] [CrossRef]
- Chakraborty, S.; Nag, D.; Mazumder, T.H.; Uddin, A. Codon usage pattern and prediction of gene expression level in Bungarus species. Gene 2017, 604, 48–60. [Google Scholar] [CrossRef] [PubMed]
- Demari-Silva, B.; Foster, P.G.; de Oliveira, T.M.P.; Bergo, E.S.; Sanabani, S.S.; Pessôa, R.; Sallum, M.A.M. Mitochondrial genomes and comparative analyses of Culex camposi, Culex coronator, Culex usquatus and Culex usquatissimus (Diptera: Culicidae), members of the coronator group. BMC Genom. 2015, 16, 831. [Google Scholar] [CrossRef] [PubMed]
- Hurst, L.D. The Ka/Ks ratio:: Diagnosing the form of sequence evolution. Trends Genet. 2002, 18, 486–487. [Google Scholar] [CrossRef] [PubMed]
- Meiklejohn, C.D.; Montooth, K.L.; Rand, D.M. Positive and negative selection on the mitochondrial genome. Trends Genet. 2007, 23, 259–263. [Google Scholar] [CrossRef] [PubMed]
- Chang, H.H.; Qiu, Z.Y.; Yuan, H.; Wang, X.Y.; Li, X.J.; Sun, H.M.; Guo, X.Q.; Lu, Y.C.; Feng, X.L.; Majid, M.; et al. Evolutionary rates of and selective constraints on the mitochondrial genomes of Orthoptera insects with different wing types. Mol. Phylogenet. Evol. 2020, 145, 106734. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Chen, J.; Jiang, L.Y.; Qiao, G.X. Hemipteran Mitochondrial Genomes: Features, Structures and Implications for Phylogeny. Int. J. Mol. Sci. 2015, 16, 12382–12404. [Google Scholar] [CrossRef]
- Popov, Y.A. New fossil Hemiptera (Heteroptera and Coleorrhyncha) from the Mesozoic of Mongolia. Neues Jahrb. Für Geol. Und Paläontologie. Monatshefte 1989, 3, 166–181. [Google Scholar] [CrossRef]
- Heiss, E.; Grimaldi, D.A. New Aradidae in Mesozoic Burmese Amber (Hemiptera, Heteroptera). Ann. Naturhist. Mus. Wien Serie A 2012, 114, 307–316. [Google Scholar]
Specimens | Date of Collection | Collection Site | Longitude (E) | Latitude (N) | GB Numbers |
---|---|---|---|---|---|
Y. mimetica | 16 January 2011 | Jinping, Yunnan | 103.2383 | 22.9067 | PP545373 |
Y. montana | 31 October 2019 | Yingjiang Tongbiguan, Yunnan | 97.9364 | 24.7031 | PP708566 |
Yangiella sp. | 27 May 2023 | Shuangbai Dutian Forest farm, Yunnan | 101.4556 | 24.5447 | PP708567 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ji, L.; Jia, Z.; Bai, X. Comparative Analysis of the Mitochondrial Genomes of Three Species of Yangiella (Hemiptera: Aradidae) and the Phylogenetic Implications of Aradidae. Insects 2024, 15, 533. https://doi.org/10.3390/insects15070533
Ji L, Jia Z, Bai X. Comparative Analysis of the Mitochondrial Genomes of Three Species of Yangiella (Hemiptera: Aradidae) and the Phylogenetic Implications of Aradidae. Insects. 2024; 15(7):533. https://doi.org/10.3390/insects15070533
Chicago/Turabian StyleJi, Liangpeng, Zhancheng Jia, and Xiaoshuan Bai. 2024. "Comparative Analysis of the Mitochondrial Genomes of Three Species of Yangiella (Hemiptera: Aradidae) and the Phylogenetic Implications of Aradidae" Insects 15, no. 7: 533. https://doi.org/10.3390/insects15070533