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Type: Article
Published: 2022-03-24
Page range: 128-142
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Four new stink bug mitogenomes corroborate the internal inconsistencies in the classification of Pentatomidae (Hemiptera)

Laboratório de Drosophila, Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil 2Programa de Pós-Graduação em Genética e Biologia Molecular, Universidade Federal do Rio Grande do Sul, RS, Brazil
Programa de Pós-Graduação em Genética e Biologia Molecular, Universidade Federal do Rio Grande do Sul, RS, Brazil 3Laboratório de Evolução Molecular, Departamento de Genética, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil.
Laboratório de Entomologia Sistemática, Departamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil. Programa de Pós-Graduação em Biologia Animal, Universidade Federal do Rio Grande do Sul, RS, Brazil
Hemiptera Asopinae crop pest evolution mitogenome phylogeny

Abstract

Stink bugs (Pentatomidae) are a speciose group of insects that feed mostly on plants. Many species are considered agricultural pests of economically important crops around the globe. Mitochondrial genomes are valuable for evolutionary and phylogenetic studies, but have been little explored for Pentatomidae. Here, we characterized the mitochondrial genomes of four pentatomid species (Diceraeus melacanthus, Euschistus heros, Piezodorus guildinii, and Stiretrus anchorago) and performed a comparative analysis for this family and its subfamilies. Stink bug mitogenomes disclosed a conserved gene order and content, although we detected two uncommon armless tRNAs in E. heros and D. melacanthus. Phylogenetic results indicate that Pentatominae is polyphyletic, showing that internal relationships of Pentatomidae should be further investigated. Stink bug mitochondrial genes are under strong purifying selection, except for ATP8 which showed signs of positive selection.

 

References

  1. Andrews, S. (2010) FastQC: A Quality Control Tool for High Throughput Sequence Data.
    Barros, L.D., Barão, K.R. & Grazia, J. (2020) Systematics of the Mecocephala group (Hemiptera: Heteroptera: Pentatomidae) based on a phylogenetic perspective: Inclusion of Hypanthracos, description of three new genera, and redescription of Ogmocoris. Arthropod Systematics & Phylogeny, 78 (2), 321–360. https://doi.org/10.26049/ASP78-2-2020-07
    Benjamini, Y. & Yekutieli, D. (2001) The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics, 29 (4), 1165–1188. https://doi.org/10.1214/aos/1013699998
    Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G., Pütz, J., Middendorf, M. & Stadler, P.F. (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69, 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
    Bianchi, F.M., Barão, K.R., Grassi, A. & Ferrari, A. (2021) A milestone for Pentatomoidea: Grazia et al. 2008—What do we know and where can we go? Zootaxa, 4958 (1), 406–429. https://doi.org/10.11646/zootaxa.4958.1.26
    Bianchi, F.M. & Gonçalves, L.T. (2021) Borrowing the Pentatomomorpha tome from the DNA barcode library: Scanning the overall performance of cox1 as a tool. Journal of Zoological Systematics and Evolutionary Research, 59, 992–1012. https://doi.org/10.1111/jzs.12476
    Bolger, A.M., Lohse, M. & Usadel, B. (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–20. https://doi.org/10.1093/bioinformatics/btu170
    Cameron, S.L. (2014) Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology, 59, 95–117. https://doi.org/10.1146/annurev-ento-011613-162007
    Caorsi, V., Cornara, D., Wells, K.E., Moser, D., Berardo, A., Miselli, R., Torriani, M., Pugno, N.M., Tasin, M., Maistrello, L. & Mazzoni, V. (2021) Design of ideal vibrational signals for stinkbug male attraction through vibrotaxis experiments. Pest Management Science, 77 (12), 5498–5508. https://doi.org/10.1002/ps.6590
    Chang, H., Qiu, Z., Yuan, H., Wang, X., Li, X., Sun, H., Guo, X., Lu, Y., Feng, X., Majid, M. & Huang, Y. (2020) Evolutionary rates of and selective constraints on the mitochondrial genomes of Orthoptera insects with different wing types. Molecular Phylogenetics and Evolution, 145, 106734. https://doi.org/10.1016/j.ympev.2020.106734
    Chen, C., Wei, J., Ji, W. & Zhao, Q. (2017) The first complete mitochondrial genome from the subfamily Phyllocephalinae (Heteroptera: Pentatomidae) and its phylogenetic analysis. Mitochondrial DNA Part B, 2, 938–939. https://doi.org/10.1080/23802359.2017.1413313
    Chen, Q., Niu, X., Fang, Z. & Weng, Q. (2020) The complete mitochondrial genome of Eysarcoris guttigerus (Hemiptera: Pentatomidae). Mitochondrial DNA Part B, 5, 687–688. https://doi.org/10.1080/23802359.2020.1714498
    Chen, W.-T., Zhang, L.-J., Cao, Y. & Yuan, M.-L. (2021) The complete mitochondrial genome of Palomena viridissima (Hemiptera: Pentatomidae) and phylogenetic analysis. Mitochondrial DNA Part B, 6, 1326–1327. https://doi.org/10.1080/23802359.2021.1909442
    Dierckxsens, N., Mardulyn, P. & Smits, G. (2017) NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Research, 45, e18. https://doi.org/10.1093/nar/gkw955
    Dowling, D.K., Friberg, U. & Lindell, J. (2008) Evolutionary implications of non-neutral mitochondrial genetic variation. Trends in Ecology & Evolution, 23, 546–54. https://doi.org/10.1016/j.tree.2008.05.011
    Gao, F., Chen, C., Arab, D.A., Du, Z., He, Y. & Ho, S.Y.W. (2019) EasyCodeML: A visual tool for analysis of selection using CodeML. Ecology and Evolution, 9, 3891–3898. https://doi.org/10.1002/ece3.5015
    Gao, S., Ren, Y., Sun, Y., Wu, Z., Ruan, J., He, B., Zhang, T., Yu, X., Tian, X. & Bu, W. (2016) PacBio full-length transcriptome profiling of insect mitochondrial gene expression. RNA biology, 13, 820–825. https://doi.org/10.1080/15476286.2016.1197481
    Gapud, V.P. (1991) A generic revision of the subfamily Asopinae, with consideration of its phylogenetic position in the family Pentatomidae and superfamily Pentatomoidea (Hemiptera Heteroptera). Philippines Entomology, 8, 865–961.
    Genevcius, B.C., Greve, C., Koehler, S., Simmons, R.B., Rider, D.A., Grazia, J. & Schwertner, C.F. (2021) Phylogeny of the stink bug tribe Chlorocorini (Heteroptera, Pentatomidae) based on DNA and morphological data: the evolution of key phenotypic traits. Systematic Entomology, 46, 327–338. https://doi.org/10.1111/syen.12464
    Grazia, J., Panizzi, A.R., Greve, C., Schwertner, C.F., Campos, L.A., de A. Garbelotto, T. & Fernandes, J.A.M. (2015) Stink Bugs (Pentatomidae). In: Panizzi, A.R. & Grazia, J. (Eds.), True Bugs (Heteroptera) of the Neotropics. Entomology in Focus. Springer Netherlands, Dordrecht, pp. 681–756. https://doi.org/10.1007/978-94-017-9861-7_22
    Grazia, J., Schuh, R.T. & Wheeler, W.C. (2008) Phylogenetic relationships of family groups in Pentatomoidea based on morphology and DNA sequences (Insecta: Heteroptera). Cladistics, 24, 932–976. https://doi.org/10.1111/j.1096-0031.2008.00224.x
    Hebert, P.D.N., Cywinska, A., Ball, S.L. & DeWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society B: Biological Sciences, 270, 313–321. https://doi.org/10.1098/rspb.2002.2218
    Hickmann, F., Moraes, T., Bianchi, F.M., Corrêa, A.S. & Schwertner, C.F. (2019) Integrating data to redescribe Euschistus taurulus Berg (Hemiptera: Pentatomidae). Zootaxa, 4688 (1), 119–134. https://doi.org/10.11646/zootaxa.4688.1.7
    Hua, J., Li, M., Dong, P., Cui, Y., Xie, Q. & Bu, W. (2008) Comparative and phylogenomic studies on the mitochondrial genomes of Pentatomomorpha (Insecta: Hemiptera: Heteroptera). BMC Genomics, 9, 610. https://doi.org/10.1186/1471-2164-9-610
    Jalili, V., Afgan, E., Gu, Q., Clements, D., Blankenberg, D., Goecks, J., Taylor, J. & Nekrutenko, A. (2020) The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2020 update. Nucleic Acids Research, 48, W395–W402. https://doi.org/10.1093/nar/gkaa434
    James, J.E., Piganeau, G. & Eyre-Walker, A. (2016) The rate of adaptive evolution in animal mitochondria. Molecular Ecology, 25, 67–78. https://doi.org/10.1111/mec.13475
    Jühling, F., Pütz, J., Bernt, M., Donath, A., Middendorf, M., Florentz, C. & Stadler, P.F. (2012) Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Research, 40, 2833–2845. https://doi.org/10.1093/nar/gkr1131
    Katoh, K., Rozewicki, J. & Yamada, K.D. (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20, 1160–1166. https://doi.org/10.1093/bib/bbx108
    Kerpedjiev, P., Hammer, S. & Hofacker, I.L. (2015) Forna (force-directed RNA): Simple and effective online RNA secondary structure diagrams. Bioinformatics (Oxford, England), 31, 3377–9. https://doi.org/10.1093/bioinformatics/btv372
    Kück, P., Meid, S.A., Groß, C., Wägele, J.W. & Misof, B. (2014) AliGROOVE–visualization of heterogeneous sequence divergence within multiple sequence alignments and detection of inflated branch support. BMC Bioinformatics, 15, 294. https://doi.org/10.1186/1471-2105-15-294
    Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. (2018) MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Molecular Biology and Evolution, 35, 1547–1549. https://doi.org/10.1093/molbev/msy096
    Lanfear, R., Calcott, B., Ho, S.Y.W. & Guindon, S. (2012) Partitionfinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29, 1695–701. https://doi.org/10.1093/molbev/mss020
    Laslett, D. & Canbäck, B. (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics (Oxford, England), 24, 172–5. https://doi.org/10.1093/bioinformatics/btm573
    Lee, W., Kang, J., Jung, C., Hoelmer, K., Lee, S.H. & Lee, S. (2009) Complete mitochondrial genome of brown marmorated stink bug Halyomorpha halys (Hemiptera: Pentatomidae), and phylogenetic relationships of hemipteran suborders. Molecules and Cells, 28, 155–165. https://doi.org/10.1007/s10059-009-0125-9
    Lee, Y., Kwak, H., Shin, J., Kim, S.-C., Kim, T. & Park, J.-K. (2019) A mitochondrial genome phylogeny of Mytilidae (Bivalvia: Mytilida). Molecular Phylogenetics and Evolution, 139, 106533. https://doi.org/10.1016/j.ympev.2019.106533
    Li, H., Leavengood, J.M., Chapman, E.G., Burkhardt, D., Song, F., Jiang, P., Liu, J., Zhou, X. & Cai, W. (2017) Mitochondrial phylogenomics of Hemiptera reveals adaptive innovations driving the diversification of true bugs. Proceedings of the Royal Society B: Biological Sciences, 284. https://doi.org/10.1098/rspb.2017.1223
    Li, X.-D., Jiang, G.-F., Yan, L.-Y., Li, R., Mu, Y. & Deng, W.-A. (2018) Positive selection drove the adaptation of mitochondrial genes to the demands of flight and high-altitude environments in grasshoppers. Frontiers in Genetics, 9, 605. https://doi.org/10.3389/fgene.2018.00605
    Lis, J.A., Ziaja, D.J., Lis, B. & Gradowska, P. (2017) Non-monophyly of the “cydnoid” complex within Pentatomoidea (Hemiptera: Heteroptera) revealed by Bayesian phylogenetic analysis of nuclear rDNA sequences. Arthropod Systematics & Phylogeny, 75, 481–496.
    Liu, Y., Li, H., Song, F., Zhao, Y., Wilson, J.-J. & Cai, W. (2019) Higher-level phylogeny and evolutionary history of Pentatomomorpha (Hemiptera: Heteroptera) inferred from mitochondrial genome sequences. Systematic Entomology, 44, 810–819. https://doi.org/10.1111/syen.12357
    López-Giráldez, F. & Townsend, J.P. (2011) PhyDesign: an online application for profiling phylogenetic informativeness. BMC Evolutionary Biology, 11, 152. https://doi.org/10.1186/1471-2148-11-152
    Massardo, D., VanKuren, N.W., Nallu, S., Ramos, R.R., Ribeiro, P.G., Silva-Brandão, K.L., Brandão, M.M., Lion, M.B., Freitas, A.V.L., Cardoso, M.Z. & Kronforst, M.R. (2020) The roles of hybridization and habitat fragmentation in the evolution of Brazil’s enigmatic longwing butterflies, Heliconius nattereri and H. hermathena. BMC Biology, 18, 84. https://doi.org/10.1186/s12915-020-00797-1
    Mendonça, M.T.S., Nunes, B.M. & Fernandes, J.A.M. (2021) Description of fifteen new species of the Hypoxys balteatus species group (Hemiptera: Heteroptera: Pentatomidae). Acta Entomologica Musei Nationalis Pragae, 289–318. https://doi.org/10.37520/aemnp.2021.017
    Miller, M.A., Pfeiffer, W. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE). IEEE, pp. 1–8.
    Mitterboeck, T.F., Liu, S., Adamowicz, S.J., Fu, J., Zhang, R., Song, W., Meusemann, K. & Zhou, X. (2017) Positive and relaxed selection associated with flight evolution and loss in insect transcriptomes. GigaScience, 6, 1–14. https://doi.org/10.1093/gigascience/gix073
    Ojala, D., Montoya, J. & Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature, 290, 470–4. https://doi.org/10.1038/290470a0
    Okonechnikov, K., Golosova, O., Fursov, M. & team, U. (2012) Unipro UGENE: a unified bioinformatics toolkit. Bioinformatics (Oxford, England), 28, 1166–7. https://doi.org/10.1093/bioinformatics/bts091
    Oliveira, D.C.S.G., Raychoudhury, R., Lavrov, D.V. & Werren, J.H. (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Molecular Biology and Evolution, 25, 2167–80. https://doi.org/10.1093/molbev/msn159
    Padial, J.M., Miralles, A., Riva, I.D. la & Vences, M. (2010) The integrative future of taxonomy. Frontiers in Zoology, 7, 16. https://doi.org/10.1186/1742-9994-7-16
    Palomares-Rius, J.E., Cantalapiedra-Navarrete, C., Archidona-Yuste, A., Blok, V.C. & Castillo, P. (2017) Mitochondrial genome diversity in dagger and needle nematodes (Nematoda: Longidoridae). Scientific Reports, 7, 41813. https://doi.org/10.1038/srep41813
    Paradis, E. & Schliep, K. (2019) ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics (Oxford, England), 35, 526–528. https://doi.org/10.1093/bioinformatics/bty633
    Perna, N.T. & Kocher, T.D. (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution, 41, 353–8. https://doi.org/10.1007/BF00186547
    Pond, S.L.K., Frost, S.D.W. & Muse, S.V. (2005) HyPhy: hypothesis testing using phylogenies. Bioinformatics (Oxford, England), 21, 676–9. https://doi.org/10.1093/bioinformatics/bti079
    Quicke, D.L.J. (1993) Principles and Techniques of Contemporary Taxonomy. Springer Netherlands, Dordrecht. Available from: http://link.springer.com/10.1007/978-94-011-2134-7 (accessedn6 October 2021)
    Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. In: Susko, E. (Ed.), Systematic Biology, 67, 901–904. https://doi.org/10.1093/sysbio/syy032
    Rider, D.A., Schwertner, C.F., Vilímová, J., Rédei, D., Kment, P. & Thomas, D.B. (2018) Higher Systematics of the Pentatomoidea. In: McPherson, J.E. (Ed.), Invasive Stink Bugs and Related Species (Pentatomoidea). CRC Press, Boca Raton, Florida, pp. 25–201. https://doi.org/10.1201/9781315371221-2
    Roca-Cusachs, M., Schwertner, C.F., Kim, J., Eger, J., Grazia, J. & Jung, S. (2022) Opening Pandora’s box: molecular phylogeny of the stink bugs (Hemiptera: Heteroptera: Pentatomidae) reveals great incongruences in the current classification. Systematic Entomology, 47, 36–51. https://doi.org/10.1111/syen.12514
    Roe, A., Dupuis, J. & Sperling, F. (2017) Molecular Dimensions of Insect Taxonomy in the Genomics Era. In: Foottit, R.G. & Adler, P.H. (Eds.), Insect Biodiversity. John Wiley & Sons, Ltd, Chichester, UK, pp. 547–573. https://doi.org/10.1002/9781118945568.ch16
    Ronquist, F., Teslenko, M., Mark, P. van der, Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–42. https://doi.org/10.1093/sysbio/sys029
    Salini, S. & Roca-Cusachs, M. (2021) Review of the Oriental species of the genus Brachycerocoris Costa, 1863 (Hemiptera: Pentatomoidea: Pentatomidae: Podopinae s.l.) with description of two new species. Zootaxa, 5040 (4), 507–527. https://doi.org/10.11646/zootaxa.5040.4.3
    Schuh, R.T. & Weirauch, C. (2020) True Bugs of the World (Hemiptera: Heteroptera): Classification and Natural History. 2nd ed. Siri Scientific Press, 800 pp.
    Sessa, L., Calderón-Fernández, G.M., Abreo, E., Altier, N., Mijailovsky, S.J., Girotti, J.R. & Pedrini, N. (2021) Epicuticular hydrocarbons of the redbanded stink bug Piezodorus guildinii (Heteroptera: Pentatomidae): sexual dimorphism and alterations in insects collected in insecticide-treated soybean crops. Pest Management Science, ps.6528. https://doi.org/10.1002/ps.6528
    Singh, D., Kabiraj, D., Sharma, P., Chetia, H., Mosahari, P.V., Neog, K. & Bora, U. (2017) The mitochondrial genome of Muga silkworm (Antheraea assamensis) and its comparative analysis with other lepidopteran insects. PLoS ONE, 12, e0188077. https://doi.org/10.1371/journal.pone.0188077
    Smith, D.R. (2015) The past, present and future of mitochondrial genomics: have we sequenced enough mtDNAs? Briefings in Functional Genomics, elv027. https://doi.org/10.1093/bfgp/elv027
    Song, N., Zhang, H. & Zhao, T. (2019) Insights into the phylogeny of Hemiptera from increased mitogenomic taxon sampling. Molecular Phylogenetics and Evolution, 137, 236–249. https://doi.org/10.1016/j.ympev.2019.05.009
    Townsend, J.P. (2007) Profiling phylogenetic informativeness. Systematic Biology, 56, 222–31. https://doi.org/10.1080/10635150701311362
    Vieira, G.A. & Prosdocimi, F. (2019) Accessible molecular phylogenomics at no cost: obtaining 14 new mitogenomes for the ant subfamily Pseudomyrmecinae from public data. PeerJ, 7, e6271. https://doi.org/10.7717/peerj.6271
    Wang, J., Ji, Y., Li, H., Song, F., Zhang, L. & Wang, M. (2021) Characterization of the complete mitochondrial genome of Pentatoma semiannulata (Hemiptera: Pentatomidae). Mitochondrial DNA Part B, 6, 750–752. https://doi.org/10.1080/23802359.2021.1875912
    Wang, Q. & Tang, G. (2018) The mitochondrial genomes of two walnut pests, Gastrolina depressa depressa and G . depressa thoracica (Coleoptera: Chrysomelidae), and phylogenetic analyses. PeerJ, 6, e4919. https://doi.org/10.7717/peerj.4919
    Wang, Y., Duan, Y. & Yang, X. (2019) The complete mitochondrial genome of Plautia crossota (Hemiptera: Pentatomidae). Mitochondrial DNA Part B, 4, 2281–2282. https://doi.org/10.1080/23802359.2019.1627924
    Wei, S.J., Shi, M., Chen, X.X., Sharkey, M.J., Achterberg, C. van, Ye, G.Y. & He, J.H. (2010) New views on strand asymmetry in insect mitochondrial genomes. PLoS ONE, 5, 1–10. https://doi.org/10.1371/journal.pone.0012708
    Wolstenholme, D.R. (1992) Animal mitochondrial DNA: structure and evolution. International Review of Cytology, 141, 173–216. https://doi.org/10.1016/s0074-7696(08)62066-5
    Wu, Y., Yang, H., Zhou, W., Song, F., Cai, W. & Li, H. (2020) Characterization of the complete mitochondrial genome of Arma custos (Hemiptera: Pentatomidae). Mitochondrial DNA Part B, 5, 2624–2626. https://doi.org/10.1080/23802359.2020.1780985
    Xia, X. (2018) DAMBE7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution. Molecular Biology and Evolution, 35, 1550–1552. https://doi.org/10.1093/molbev/msy073
    Xia, X. & Lemey, P. (2009) Assessing substitution saturation with DAMBE. In: Lemey, P., Salemi, M. & Vandamme, A.-M. (Eds.), The Phylogenetic Handbook. Cambridge University Press, Cambridge, pp. 615–630. https://doi.org/10.1017/CBO9780511819049.022
    Xia, X., Xie, Z., Salemi, M., Chen, L. & Wang, Y. (2003) An index of substitution saturation and its application. Molecular Phylogenetics and Evolution, 26, 1–7. https://doi.org/10.1016/s1055-7903(02)00326-3
    Xu, S., Wu, Y., Liu, Y., Zhao, P., Chen, Z., Song, F., Li, H. & Cai, W. (2021) Comparative Mitogenomics and Phylogenetic Analyses of Pentatomoidea (Hemiptera: Heteroptera). Genes, 12, 1306. https://doi.org/10.3390/genes12091306
    Xue, X.-F., Guo, J.-F., Dong, Y., Hong, X.-Y. & Shao, R. (2016) Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites. Scientific Reports, 6, 18920. https://doi.org/10.1038/srep18920
    Yang, H., Li, T., Dang, K. & Bu, W. (2018) Compositional and mutational rate heterogeneity in mitochondrial genomes and its effect on the phylogenetic inferences of Cimicomorpha (Hemiptera: Heteroptera). BMC Genomics, 19, 264. https://doi.org/10.1186/s12864-018-4650-9
    Yang, Y., Xu, S., Xu, J., Guo, Y. & Yang, G. (2014) Adaptive evolution of mitochondrial energy metabolism genes associated with increased energy demand in flying insects. PLoS ONE, 9, e99120. https://doi.org/10.1371/journal.pone.0099120
    Yang, Z. (2007) PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24, 1586–91. https://doi.org/10.1093/molbev/msm088
    Yang, Z. & Nielsen, R. (2000) Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Molecular Biology and Evolution, 17, 32–43. https://doi.org/10.1093/oxfordjournals.molbev.a026236
    Yang, Z., Wong, W.S.W. & Nielsen, R. (2005) Bayes empirical bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution, 22, 1107–18. https://doi.org/10.1093/molbev/msi097
    Yuan, M.-L., Zhang, Q.-L., Guo, Z.-L., Wang, J. & Shen, Y.-Y. (2015) Comparative mitogenomic analysis of the superfamily Pentatomoidea (Insecta: Hemiptera: Heteroptera) and phylogenetic implications. BMC Genomics, 16, 460. https://doi.org/10.1186/s12864-015-1679-x
    Zhang, D., Gao, F., Jakovlić, I., Zou, H., Zhang, J., Li, W.X. & Wang, G.T. (2020) PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Molecular Ecology Resources, 20, 348–355. https://doi.org/10.1111/1755-0998.13096
    Zhang, Q.-L., Yang, X.-Z., Zhang, L., Feng, R.-Q., Zhu, Q.-H., Chen, J.-Y. & Yuan, M.-L. (2019) Adaptive evidence of mitochondrial genomes in Dolycoris baccarum (Hemiptera: Pentatomidae) to divergent altitude environments. Mitochondrial DNA Part A, 30, 9–15. https://doi.org/10.1080/24701394.2018.1446951
    Zhao, Q., Cassis, G., Zhao, L., He, Y., Zhang, H. & Wei, J. (2020) The complete mitochondrial genome of Zicrona caerulea (Linnaeus) (Hemiptera: Pentatomidae: Asopinae) and its phylogenetic implications. Zootaxa, 4747 (3), 547–561. https://doi.org/10.11646/zootaxa.4747.3.8
    Zhao, Q., Chen, C., Liu, J. & Wei, J. (2019a) Characterization of the complete mitochondrial genome of Eysarcoris aeneus (Heteroptera: Pentatomidae), with its phylogenetic analysis. Mitochondrial DNA Part B, 4, 2096–2097. https://doi.org/10.1080/23802359.2019.1622465
    Zhao, Q., Wang, J., Wang, M.-Q., Cai, B., Zhang, H.-F. & Wei, J.-F. (2018) Complete Mitochondrial Genome of Dinorhynchus dybowskyi (Hemiptera: Pentatomidae: Asopinae) and Phylogenetic Analysis of Pentatomomorpha Species. Journal of Insect Science, 18. https://doi.org/10.1093/jisesa/iey031
    Zhao, Q., Wei, J., Zhao, W., Cai, B., Du, X. & Zhang, H. (2017a) The first mitochondrial genome for the subfamily Asopinae (Heteroptera: Pentatomidae) and its phylogenetic implications. Mitochondrial DNA Part B, 2, 804–805. https://doi.org/10.1080/23802359.2017.1398599
    Zhao, W., Zhao, Q., Li, M., Wei, J., Zhang, X. & Zhang, H. (2017b) Characterization of the complete mitochondrial genome and phylogenetic implications for Eurydema maracandica (Hemiptera: Pentatomidae). Mitochondrial DNA Part B, 2, 550–551. https://doi.org/10.1080/23802359.2017.1365649
    Zhao, W., Zhao, Q., Li, M., Wei, J., Zhang, X. & Zhang, H. (2019b) Comparative Mitogenomic Analysis of the Eurydema Genus in the Context of Representative Pentatomidae (Hemiptera: Heteroptera) Taxa M. Allen (Ed.), Journal of Insect Science, 19, 20. https://doi.org/10.1093/jisesa/iez122

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