Abstract
Among Scarabaeidae, the phytophagous scarab lineage including Melolonthinae, Cetoniinae, Dynastinae, and Rutelinae is considered important due to its members’ roles as agricultural pests or pollinators. In this study, the near-complete mitochondrial genomes of seven species from six genera in the phytophagous scarab lineage were newly sequenced: Anomala russiventris (Fairmaire, 1893); Apogonia cf. basalis (Moser, 1915); Apogonia splendida (Boheman, 1858); Coenochilus striatus (Westwood, 1874); Trichogomphus mongol (Arrow, 1908); Sophrops subrugatus (Moser, 1921) and Tetraserica leishanica (Liu, Bai, Yang & Ahrens, 2014). The complete mitochondrial genomes from the 6 species include 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), 2 ribosomal RNA genes (rRNAs), and 1 control region, which have a highly conserved gene arrangement, except for Tr. mongol with the rearrangement of 2 tRNA genes (tRNA-Ile and tRNA-Gln), which is a potential identified subfamily-level character of Dynastinae. In order to test whether the mitogenomic data are suited for high-level phylogenetic inferences, the substitution saturation and heterogeneity were analyzed. The results showed no sign that the phylogenetic inferences were biased by substitution saturation or the low heterogeneity of the sequence composition for most pairwise comparisons between the sequences for the entire dataset (13 PCGs) and the amino acids dataset (13 PCGs_AA). Based on the combined data of 13 PCGs and 13 PCGs_AA from the mitogenomes of 37 taxa, the phylogeny of the phytophagous lineage was explored using RAxML and Bayesian methods. The results confirmed that Cetoniinae, Rutelinae, and Dynastinae are monophyletic, and that the latter two are sister groups. Melolonthinae is a paraphyletic group, and its tribes, Diplotaxini, Euchirini, Melolonthini, Rhizotrogini, and Sericini, are a monophyletic group. The subfamily rank of Dynastinae and the tribe rank of Anomalini and Adoretini are supported.
References
Ahrens, D. (2006) The phylogeny of Sericini and their position within the Scarabaeidae based on morphological characters (Coleoptera: Scarabaeidae). Systematic Entomology, 31 (1), 113–144. https://doi.org/10.1111/j.1365-3113.2005.00307.x
Ahrens, D. & Vogler, A.P. (2008) Towards the phylogeny of chafers (Sericini): analysis of alignment-variable sequences and the evolution of segment numbers in the antennal club. Molecular Phylogenetics and Evolution, 47 (2), 783–798. https://doi.org/10.1016/j.ympev.2008.02.010
Ahrens, D., Scott, M. & Vogler, A.P. (2011) The phylogeny of monkey beetles based on mitochondrial and ribosomal RNA genes (Coleoptera: Scarabaeidae: Hopliini). Molecular Phylogenetics and Evolution, 60 (3), 408–415. https://doi.org/10.1016/j.ympev.2011.04.011
Ahrens, D., Schwarzer, J. & Vogler, A.P. (2014) The evolution of scarab beetles tracks the sequential rise of angiosperms and mammals. Proceedings the Royal Society B-Biological Sciences, 281 (1791), 20141470. https://doi.org/10.1098/rspb.2014.1470
Ayivi, S.P.G., Tong, Y., Storey, K.B., Yu, D.N. & Zhang, J.Y. (2021) The Mitochondrial Genomes of 18 New Pleurosticti (Coleoptera: Scarabaeidae) Exhibit a Novel trnQ-NCR-trnI-trnM Gene Rearrangement and Clarify Phylogenetic Relationships of Subfamilies within Scarabaeidae. Insects, 12, 1025.
https://doi.org/10.3390/insects12111025
Ballard, J.W. & Whitlock, M.C. (2004) The incomplete natural history of mitochondria. Molecular Ecology, 13 (4), 729–744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A. & Pevzner, P.A. (2012) SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing. Journal of Computational Biology, 19 (5), 455–477. https://doi.org/10.1089/cmb.2012.0021
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 (2), 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Breeschoten, T., Doorenweerd, C., Tarasov, S. & Vogler, A.P. (2016) Phylogenetics and biogeography of the dung beetle genus Onthophagus inferred from mitochondrial genomes. Molecular Phylogenetics and Evolution, 105, 86–95. https://doi.org/10.1016/j.ympev.2016.08.016
Browne, D.J. & Scholtz, C.H. (1998) Evolution of the scarab hindwing articulation and wing base: a contribution toward the phylogeny of the Scarabaeidae (Scarabaeoidea: Coleoptera). Systematic Entomology, 23 (4), 307–326. https://doi.org/10.1046/j.1365-3113.1998.00059.x
Cameron, S.L., Sullivan, J., Song, H., Miller, K.B. & Whiting, M.F. (2009) A mitochondrial genome phylogeny of the Neuropterida (lace-wings, alderflies and snakeflies) and their relationship to the other holometabolous insect orders. Zoologica Scripta, 38 (6), 575–590. https://doi.org/10.1111/j.1463-6409.2009.00392.x
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
Castresana, J. (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17 (4), 540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Cheng, C.T., Jeng, M.L., Tsai, J.F., Li, C.K. & Wu, L.W. (2021) Two mitochondrial genomes of Taiwanese rhinoceros beetles, Oryctes rhinoceros and Eophileurus chinensis (Coleoptera: Scarabaeidae). Mitochondrial DNA Part B, 6 (8), 2260–2262. https://doi.org/10.1080/23802359.2021.1948364
Choi, E.H., Mun, S., Baek, S.Y., Hwang, J. & Hwang, U.W. (2020) The complete mitochondrial genome of a whiter-spotted flower chafer, Protaetia brevitarsis (Coleoptera: Scarabaeidae). Mitochondrial DNA Part B, 5 (3), 3602–3604. https://doi.org/10.1080/23802359.2020.1824592
Coca-Abia, M. (2007) Phylogenetic relationships of the subfamily Melolonthinae (Coleoptera, Scarabaeidae). Insect Systematics & Evolution, 38 (4), 447–472. https://doi.org/10.1163/187631207794760921
Erichson, W.F. (1847) Naturgeschichte der Insecten Deutschlands. Erste Abtheilung. Coleoptera. Vol. 3. Nicolaischen Buchhandlung, Berlin, 481–640 pp.
Frew, A., Barnett, K., Nielsen, U.N., Riegler, M., & Johnson, S.N. (2016) Belowground ecology of scarabs feeding on grass roots: current knowledge and future directions for management in Australasia. Frontiers in Plant Science, 7, 321. https://doi.org/10.3389/fpls.2016.00321
Filipović, I., Hereward, J.P., Rašić, G., Devine, G.J., Furlong, M.J. & Etebari, K. (2021) The complete mitochondrial genome sequence of Oryctes rhinoceros (Coleoptera: Scarabaeidae) based on long-read nanopore sequencing. PeerJ, 9, e10552. https://doi.org/10.7717/peerj.10552
Grant, J.R. & Stothard, P. (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Research, 36, 181–184. https://doi.org/:10.1093/nar/gkn179
Gunter, N.L., Weir, T.A., Slipinksi, A., Bocak, L. & Cameron, S.L. (2016) If Dung Beetles (Scarabaeidae: Scarabaeinae) Arose in Association with Dinosaurs, Did They Also Suffer a Mass Co-Extinction at the K-Pg Boundary? PLoS One, 11 (5), e0153570. https://doi.org/10.1371/journal.pone.0153570
Howden, H.F. (1982) Larval and adult characters of Frickius Germain, its relationship to the Geotrupini, and a phylogeny of some major taxa in the Scarabaeoidea (Insecta: Coleoptera). Canadian Journal of Zoology, 60 (11), 2713–2724. https://doi.org/10.1139/z82-347
Jin, J.J., Yu, W.B., Yang, J.B., Song, Y., dePamhilis, C.W., Y., Yi, T.S. & Li, D.Z. (2018) GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology, 21 (1), 241. https://doi.org/10.1101/256479
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30 (4), 772–780. https://doi.org/10.1093/molbev/mst010
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. & Drummond, A. (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28 (12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kim, M.J., Kim, K.G. & Kim, I. (2013) Description of Nearly Completed Mitochondrial Genome Sequences of the Garden Chafer Polyphylla laticollis manchurica, Endangered in Korea (Insecta: Coleoptera). International Journal of Industrial Entomology, 27 (1), 185–202. https://doi.org/10.7852/ijie.2013.27.1.185
Kim, M.J., Jeong, S.Y., Jeong, J.C., Kim, S.S. & Kim, I. (2016) Complete mitochondrial genome of the endangered flower chafer Osmoderma opicum (Coleoptera: Scarabaeidae). Mitochondrial DNA Part B, 1 (1), 148–149. https://doi.org/10.1080/23802359.2016.1144104
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution, 33 (7), 1870–1874. https://doi.org/10.1093/molbev/msw054
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), 1–15.
https://doi.org/10.1186/1471-2105-15-294
Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T. & Calcott, B. (2016) PartitionFinder 2: newmethods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34 (3), 772–773. https://doi.org/10.1093/molbev/msw260
Li, Z., Li, X., Song, N., Tang, H. & Yin, X. (2020) The Mitochondrial Genome of Amara aulica (Coleoptera, Carabidae, Harpalinae) and Insights into the Phylogeny of Ground Beetles. Genes, 11 (2), 181. https://doi.org/10.3390/genes11020181
Mayer, C., Soka, G. & Picker, M. (2006) The importance of monkey beetle (Scarabaeidae: Hopliini) pollination for Aizoaceae and Asteraceae in grazed and ungrazed areas at Paulshoek, Succulent Karoo, South Africa. Journal of Insect conservation, 10 (4), 323–333. https://doi.org/10.1007/s10841-006-9006-0
McKenna, D.D., Farrell, B.D., Caterino, M.S., Farnum, C.W., Hawks, D.C., Maddison, D.R., Seago, A.E., Short, A.E.Z., Newton, A.F. & Thayer, M.K. (2015) Phylogeny and evolution of Staphyliniformia and Scarabaeiformia: forest litter as a stepping stone for diversification of nonphytophagous beetles. Systematic Entomology, 40 (1), 35–60. https://doi.org/10.1111/syen.12093
Miller, M.A., W. Pfeiffer, T. & Schwartz, T. (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Gateway Computing Environments Workshop (GCE). New Orleans, LA, p. 1–8.
Nie, R.E., Yang, M.X., Xue, H.J., Yang, Y.R., Tong, Y.J., Qiu, T.F., Bai, M. & Yang, X.K. (2017) The application and effectiveness of a flight interception trap for insect collecting. Chinese Journal of Applied Entomology, 54 (3), 530–535. https://doi.org/10.7679/j.issn.2095-1353.2017.065
Nie, R.E., Breeschoten, T., Timmermans, M.J.T.N., Nadein, K., Xue, H.J., Bai, M., Huang, Y., Yang, X.K. & Vogler, A.P. (2018) The phylogeny of Galerucinae (Coleoptera: Chrysomelidae) and the performance of mitochondrial genomes in phylogenetic inference compared to nuclear rRNA genes. Cladistics, 34 (2), 113–130. https://doi.org/10.1111/cla.12196
Nie, R.E., Andújar, C., Gómez-Rodríguez, C., Bai, M., Xue, H.J., Tang, M., Yang, C.T., Tang, P., Yang, X.K. & Vogler, A. P. (2020) The phylogeny of leaf beetles (Chrysomelidae) inferred from mitochondrial genomes. Systematic Entomology, 45 (1), 188–204. https://doi.org/10.1111/syen.12387
Nie, R.E., Vogler, A.P., Yang, X.K. & Lin, M.Y. (2021) Higher-level phylogeny of longhorn beetles (Coleoptera: Chrysomeloidea) inferred from mitochondrial genomes. Systematic Entomology, 46 (1), 56–70. https://doi.org/10.1111/syen.12447
Rambaut, A., Drummond, A.J., Xie, D., Baele, G. and Suchard, M.A., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Software for Systematics and Evolution. 67, 901–904.
https://doi.org/10.1093/sysbio/syy032
Ronquist, F., Teslenko, M., Mark, P.V.D., 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 (3), 539–542. https://doi.org/10.1093/sysbio/sys029
Rubinoff, D. & Holland, B.S. (2005) Between Two Extremes: Mitochondrial DNA is neither the Panacea nor the Nemesis of Phylogenetic and Taxonomic Inference. Systematic Biology, 54 (6), 952–961.
https://doi.org/10.1080/10635150500234674
Schattner, P., Brooks, A.N. & Lowe T.M. (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Research, 33, 686–689. http://doi.org/10.1093/nar/gki366
Scholtz, C.H. (1988) Biology of Sparrmannia flava Arrow (Scarabaeidae: Melolonthinae). The Coleopterists Bulletin, 42 (1), 57–62. https://doi.org/stable/4008564
Scholtz, C.H. & Grebennikov, V.V. (2016) 15. Scarabaeoidea Latreille, 1802. In: Beutel R. G. & Kristensen N. P. (Eds.), Handbook of Zoology, Arthropoda: Insecta, Coleoptera, Beetles. Volume 1. Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga partim) 2nd edition. De Gruyter, Berlin, pp. 443–525.
Shao, L.L., Huang, D.Y., Sun, X.Y., Hao, J.S., Cheng, C.H., Zhang, W. & Yang, Q. (2014) Complete mitochondrial genome sequence of Cheirotonus jansoni (Coleoptera: Scarabaeidae). Genetics and Molecular Research, 13 (1), 1047–1058. https://doi.org/10.4238/2014.February.20.6
Sharp, P.M. & Li, W.H. (1986) An evolutionary perspective on synonymous codon usage in unicellular organisms. Journal of Molecular Evolution, 24 (1–2), 28–38. https://doi.org/10.1007/BF02099948
Song, N. & Zhang, H. (2018) The Mitochondrial Genomes of Phytophagous Scarab Beetles and Systematic Implications. Journal of Insect Science, 18 (6), 1–11. https://doi.org/10.1093/jisesa/iey076
Smith, A.B.T., Hawks, D.C. & Heraty, J.M. (2006) An Overview of the Classification and Evolution of the Major Scarab Beetle Clades (Coleoptera: Scarabaeoidea) Based on Preliminary Molecular Analyses. The Coleopterists Bulletin, 60 (5), 35–46. https://doi.org/10.1649/0010065X(2006)60[35:AOOTCA]2.0.CO;2
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30 (9), 1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Timmermans, M.J., Barton, C., Haran, J., Ahrens, D., Culverwell, C.L., Ollikainen, A., Dodsworth, S., Foster, P.G., Bocak, L. & Vogler, A.P. (2016) Family-Level Sampling of Mitochondrial Genomes in Coleoptera: Compositional Heterogeneity and Phylogenetics. Genome Biology and Evolution, 8 (1), 161–175. https://doi.org/10.1093/gbe/evv241
Wickham, H. (2009) ggplot2: Elegant Graphics for Data Analysis (Use R). Springer: New York, NY, USA, Volume 10, p. 978. https://doi.org/10.1080/15366367.2019.1565254
Xia, X. (2018) DAMBE 7: New and Improved Tools for Data Analysis in Molecular Biology and Evolution. Molecular Biology and Evolution, 35 (6), 1550–1552.
https://doi.org/10.1093/molbev/msy073
Yang, C., Zhu, E.J., He, Q.J., Yi, C.H., Hu, S.J. & Wang, X.B. (2020) Complete mitochondrial genome of the Endangered long-armed scarab Cheirotonus gestroi (Coleoptera: Euchiridae). Mitochondrial DNA Part B, 5 (1), 869–870. https://doi.org/10.1080/23802359.2020.1715888
Yang, W., Zhang, Y., Feng, S., Liu, L. & Li, Z. (2018) The first complete mitochondrial genome of the Japanese beetle Popillia japonica (Coleoptera: Scarabaeidae) and its phylogenetic implications for the superfamily Scarabaeoidea. International Journal of Biological Macromolecules, 118, 1406–1413. https://doi.org/10.1016/j.ijbiomac.2018.06.131
Yang, X.Z., Zhang, L., Feng, R.Q., Zhang, L.J., Luo, F.Z. & Yuan, M.L. (2018) Mitochondrial genome of Amphimallon solstitiale (Coleoptera: Scarabaeidae: Melolonthinae) and phylogenetic analysis. Mitochondrial DNA Part B, 4 (1), 110–111.
https://doi.org/10.1080/23802359.2018.1536482
Yu, X.L., Tan, W., Zhang, H.Y., Jiang, W.L., Gao, H., Wang, W.X., Liu, Y.X., Wang, Y. & Tian, X.X. (2019) Characterization of the Complete Mitochondrial Genome of Harpalus sinicus and Its Implications for Phylogenetic Analyses. Genes, 10 (9), 724. https://doi.org/10.3390/genes10090724
Yuan, M.L., Zhang. Q.L., Zhang. L., Guo. Z.L., Liu. Y.J., Shen. Y.Y. & Shao, R. (2016) High-level phylogeny of the Coleoptera inferred with mitochondrial genome sequences, Molecular Phylogenetics and Evolution, 11 (2016), 99–111.
https://doi.org/10.1016/j.ympev.2016.08.002
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 (1), 348–355. https://doi.org/10.1111/1755-0998.13096
Zhou, Y.T., Yan, J.Y. & Qi, H.X. (2021) Complete mitochondrial genome of Polyphylla gracilicornis (Coleoptera: Scarabaeoidea). Mitochondrial DNA Part B, 6 (2), 435–436. https://doi.org/10.1080/23802359.2020.1870895