Published July 5, 2024
| Version v1
Journal article
Open
The first two complete mitochondrial genomes for the genus Anagyrus (Hymenoptera, Encyrtidae) and their phylogenetic implications
Authors/Creators
- 1. Tianjin Agricultural University, Tianjin, China
Description
Anagyrus, a genus of Encyrtidae (Hymenoptera, Chalcidoidea), represents a successful group of parasitoid insects that attack various mealybug pests of agricultural and forestry plants. Until now, only 20 complete mitochondrial genomes have been sequenced, including those in this study. To enrich the diversity of mitochondrial genomes in Encyrtidae and to gain insights into their phylogenetic relationships, the mitochondrial genomes of two species of Anagyrus were sequenced, and the mitochondrial genomes of these species were compared and analyzed. Encyrtid mitochondrial genomes exhibit similarities in nucleotide composition, gene organization, and control region patterns. Comparative analysis of protein-coding genes revealed varying molecular evolutionary rates among different genes, with six genes (ATP8, ND2, ND4L, ND6, ND4 and ND5) showing higher rates than others. A phylogenetic analysis based on mitochondrial genome sequences supports the monophyly of Encyrtidae; however, the two subfamilies, Encyrtinae and Tetracneminae, are non-monophyletic. This study provides valuable insights into the phylogenetic relationships within the Encyrtidae and underscores the utility of mitochondrial genomes in the systematics of this family.
Files
ZK_article_121923.pdf
Files
(1.7 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:f8ecd534f4e0a6a561ee8ccec6de6d6d
|
1.7 MB | Preview Download |
System files
(221.7 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:40b076d8d017b8d731dc19a058c64621
|
221.7 kB | Download |
Linked records
Additional details
References
- Benson G (1999) Tandem repeats finder: A program to analyze DNA sequences. Nucleic Acids Research 27(2): 573–580. https://doi.org/10.1093/nar/27.2.573
- Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Research 27(8): 1767–1780. https://doi.org/10.1093/nar/27.8.1767
- Brown WM, George Jr M, Wilson AC (1979) Rapid evolution of animal mitochondrial DNA. Proceedings of the National Academy of Sciences of the United States of America 76(4): 1967–1971. https://doi.org/10.1073/pnas.76.4.1967
- Cameron SL (2014) Insect mitochondrial genomics: Implications for evolution and phylogeny. Annual Review of Entomology 59(1): 95–117. https://doi.org/10.1146/annurev-ento-011613-162007
- Cameron SL, Whiting MF (2008) The complete mitochondrial genome of the tobacco hornworm, Manduca sexta, (Insecta: Lepidoptera: Sphingidae), and an examination of mitochondrial gene variability within butterflies and moths. Gene 408(1–2): 112–123. https://doi.org/10.1016/j.gene.2007.10.023
- Chen SF, Zhou YQ, Chen YR, Gu J (2018) fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics (Oxford, England) 34(17): i884–i890. https://doi.org/10.1093/bioinformatics/bty560
- Cook LG, Gullan PJ, Trueman HE (2002) A preliminary phylogeny of the scale insects (Hemiptera: Sternorrhyncha: Coccoidea) based on nuclear small-subunit ribosomal DNA. Molecular Phylogenetics and Evolution 25(1): 43–52. https://doi.org/10.1016/S1055-7903(02)00248-8
- Crozier RH, Crozier YC (1992) The cytochrome b and ATPase genes of honeybee mitochondrial DNA. Molecular Biology and Evolution 9(3): 474–482. https://doi.org/10.1093/oxfordjournals.molbev.a040729
- Crozier RH, Crozier YC (1993) The mitochondrial genome of the honeybee Apis mellifera: Complete sequence and genome organization. Genetics 133(1): 97–117. https://doi.org/10.1093/genetics/133.1.97
- Cruaud A, Rasplus JY, Zhang JX, Burks R, Delvare G, Fusu L, Gumovsky A, Huber JT, Janšta P, Mitroiu MD, Noyes JS, van Noort S, Baker A, Böhmová J, Baur H, Blaimer BB, Brady SG, Bubeníková K, Chartois M, Copeland RS, Dale-Skey Papilloud N, Dal Molin A, Dominguez C, Gebiola M, Guerrieri E, Kresslein RL, Krogmann L, Lemmon E, Murray EA, Nidelet S, Nieves-Aldrey JL, Perry RK, Peters RS, Polaszek A, Sauné L, Torréns J, Triapitsyn S, Tselikh EV, Yoder M, Lemmon AR, Woolley JB, Heraty JM (2024) The Chalcidoidea bush of life: Evolutionary history of a massive radiation of minute wasps. Cladistics 40(1): 34–63. https://doi.org/10.1111/cla.12561
- Darty K, Denise A, Ponty Y (2009) VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics (Oxford, England) 25(15): 1974–1975. https://doi.org/10.1093/bioinformatics/btp250
- Donath A, Jühling F, Al-Arab M, Bernhart SH, Reinhardt F, Stadler PF, Middendorf M, Bernt M (2019) Improved annotation of protein-coding genes boundaries in metazoan mitochondrial genomes. Nucleic Acids Research 47(20): 10543–10552. https://doi.org/10.1093/nar/gkz833
- Dowton M, Castro LR, Austin AD (2002) Mitochondrial gene rearrangements as phylogenetic characters in the invertebrates: The examination of genome 'morphology'. Invertebrate Systematics 16(3): 345–356. https://doi.org/10.1071/IS02003
- Du YM, Song X, Liu XJ, Zhong BL (2019) Mitochondrial genome of Diaphorencyrtus aligarhensis (Hymenoptera: Chalcidoidea: Encyrtidae) and phylogenetic analysis. Mitochondrial DNA. Part B, Resources 4(2): 3190–3191. https://doi.org/10.1080/23802359.2019.1667913
- Fan XL, Gong YJ, Chen PY, Tan QQ, Tan JL, Wei SJ (2017) Next-generation sequencing of the mitochondrial genome of Dolichovespula panda (Hymenoptera: Vespidae) with a phylogenetic analysis of Vespidae. Journal of Asia-Pacific Entomology 20(3): 971–976. https://doi.org/10.1016/j.aspen.2017.07.009
- Gupta A, Poorani J (2009) Taxonomic studies on a collection of Chalcidoidea (Hymenoptera) from India with new distribution records. Journal of Threatened Taxa 1(5): 300–304. https://doi.org/10.11609/JoTT.o1861.300-4
- Hassanin A, Léger N, Deutsch J (2005) Evidence for multiple reversals of asymmetric mutational constraints during the evolution of the mitochondrial genome of Metazoa, and consequences for phylogenetic inferences. Systematic Biology 54(2): 277–298. https://doi.org/10.1080/10635150590947843
- Hayat M, Narendran TC, Remadevi OK, Manikandan S (2003) Parasitoids (Hymenoptera: Chalcidoidea; Ceraphronoidea) reared mainly from Coccoidea (Homoptera) attacking Sandalwood, Santalum album L. Oriental Insects 37(1): 309–334. https://doi.org/10.1080/00305316.2003.10417352
- Heraty JM, Burks RA, Cruaud A, Gibson GAP, Liljeblad J, Munro J, Rasplus JY, Delvare G, Janšta P, Gumovsky A, Huber J, Woolley JB, Krogmann L, Heydon S, Polaszek A, Schmidt S, Darling DC, Gates MW, Mottern J, Murray E, Dal Molin A, Triapitsyn S, Baur H, Pinto JD, van Noort S, George J, Yoder M (2013) A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). Cladistics 29: 466–542. https://doi.org/10.1111/cla.12006
- Howard LO, Ashmead WH (1896) On some reared parasitic hymenopterous insects from Ceylon. Proceedings of the United States National Museum 18(1092): 633–648. https://doi.org/10.5479/si.00963801.18-1092.633
- Hurst LD (2002) The Ka/Ks ratio: diagnosing the form of sequence evolution. Trends in Genetics 18(9): 486–487. https://doi.org/10.1016/S0168-9525(02)02722-1
- Japoshvili O, Hansen LO (2015) New records of Encyrtidae (Hymenoptera, Chalcidoidea) from Norway VI. Norwegian Journal of Entomology 62(2): 174–179.
- Jia CH, Zhang XM, Xu SY, Yang TY, Yanagimoto T, Gao TX (2020) Comparative analysis of the complete mitochondrial genomes of three rockfishes (Scorpaeniformes, Sebastiscus) and insights into the phylogenetic relationships of Sebastidae. Bioscience Reports 40(12): BSR20203379. https://doi.org/10.1042/BSR20203379
- Jin JJ, Yu WB, Yang JB, Song Y, dePamphilis CW, Yi TS, Li DZ (2020) GetOrganelle: A fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21(1): 241. https://doi.org/10.1186/s13059-020-02154-5
- Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: Fast model selection for accurate phylogenetic estimates. Nature Methods 14(6): 587–589. https://doi.org/10.1038/nmeth.4285
- Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20(44): 1160–1166. https://doi.org/10.1093/bib/bbx108
- Krzywinski J, Grushko OG, Besansky NJ (2006) Analysis of the complete mitochondrial DNA from Anopheles funestus: An improved dipteran mitochondrial genome annotation and a temporal dimension of mosquito evolution. Molecular Phylogenetics and Evolution 39(2): 417–423. https://doi.org/10.1016/j.ympev.2006.01.006
- Li Q, Wei SJ, Tang P, Wu Q, Shi M, Sharkey MJ, Chen XX (2016) Multiple Lines of Evidence from Mitochondrial Genomes Resolve Phylogenetic Relationships of Parasitic Wasps in Braconidae. Genome Biology and Evolution 8(9): 2651–2662. https://doi.org/10.1093/gbe/evw184
- Liu MD, Luo YF, Jallow BJJ, Meng FM (2023) Characterization of Complete Mitochondrial Genome and Phylogenetic Analysis of a Nocturnal Wasps – Provespa barthelemyi (Hymenoptera: Vespidae). Current Issues in Molecular Biology 45(12): 9368–9377. https://doi.org/10.3390/cimb45120587
- Ma Y, Zheng BY, Zhu JC, Tang P, Chen XX (2019) The mitochondrial genome of Aenasius arizonensis (Hymenoptera: Encyrtidae) with novel gene order. Mitochondrial DNA. Part B, Resources 4(1): 2023–2024. https://doi.org/10.1080/23802359.2019.1617052
- Meng GL, Li YY, Yang CT, Liu SL (2019) MitoZ: A toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Research 47(11): e63. https://doi.org/10.1093/nar/gkz173
- Munro JB, Heraty JM, Burks RA, Hawks D, Mottern J, Cruaud A, Rasplus JY, Janšta P (2011) A Molecular Phylogeny of the Chalcidoidea (Hymenoptera). PLOS ONE 6(11): e27023. https://doi.org/10.1371/journal.pone.0027023
- Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Molecular Biology and Evolution 32(1): 268–274. https://doi.org/10.1093/molbev/msu300
- Noyes JS (1980) A review of the genera of Neotropical Encyrtidae (Hymenoptera: Chalcidoidea). Bulletin of the British Museum of Natural History 41: 107–253.
- Noyes JS (2019) Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids. [Accessed on 27 Jul 2023]
- Noyes JS, Hayat M (1984) A review of the genera of Indo-Pacific Encyrtidae (Hymenoptera: Chalcidoidea). Bulletin of the British Museum of Natural History 48: 131–395.
- Noyes JS, Hayat M (1994) Oriental mealybug parasitoids of the Anagyrini (Hymenoptera: Encyrtidae). CAB International, Wallingford, 554 pp.
- Ojala D, Montoya J, Attardi G (1981) tRNA punctuation model of RNA processing in human mitochondria. Nature 290(5806): 470–474. https://doi.org/10.1038/290470a0
- Öncüer C (1991) A catalogue of the parasites and predators of insect pests of Turkey. Ege University Agricultural Faculty Press No. 505, Izmir, 204 pp.
- Peng Y, Chen B, Li TJ (2017) Sequencing and analysis of the complete mitochondrial genome of Parapolybia crocea (Hymenoptera: Vespidae). Acta Entomologica Sinica 60(4): 464–474. https://doi.org/10.16380/j.kcxb.2017.04.011
- Perna NT, Kocher TD (1995) Patterns of nucleotide composition at fourfold degenerate sites of animal mitochondrial genomes. Journal of Molecular Evolution 41(3): 353–358. https://doi.org/10.1007/BF01215182
- Ranwez V, Douzery EJP, Cambon C, Chantret N, Delsuc F (2018) MACSE v2: Toolkit for the Alignment of Coding Sequences Accounting for Frameshifts and Stop Codons. Molecular Biology and Evolution 35(10): 2582–2584. https://doi.org/10.1093/molbev/msy159
- Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (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
- Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution 34(12): 3299–3302. https://doi.org/10.1093/molbev/msx248
- Rudoy A, Zhu CD, Ferrari RR, Zhang YZ (2022) Integrative taxonomy based on morphometric and molecular data supports recognition of the three cryptic species within the Encyrtus sasakii complex (Hymenoptera, Encyrtidae). Journal of Hymenoptera Research 90: 129–152. https://doi.org/10.3897/jhr.90.75807
- Sayers EW, Cavanaugh M, Clark K, Pruitt KD, Sherry ST, Yankie L, Karsch-Mizrachi I (2024) GenBank 2024 Update. Nucleic Acids Research 52(D1): D134–D137. https://doi.org/10.1093/nar/gkad903
- Shao RF, Campbell NJH, Barker SC (2001) Numerous gene rearrangements in the mitochondrial genome of the Wallaby Louse, Heterodoxus macropus (Phthiraptera). Molecular Biology and Evolution 18(5): 858–865. https://doi.org/10.1093/oxfordjournals.molbev.a003867
- Simutnik SA, Perkovsky EE (2023) Description of a new genus and species of Encyrtidae (Hymenoptera: Chalcidoidea) from Danish amber, based on a male specimen featuring an antenna with a distinct anellus. Zootaxa 5369(3): 437–445. https://doi.org/10.11646/zootaxa.5369.3.7
- Simutnik SA, Perkovsky EE, Vasilenko DV (2022) Electronoyesella antiqua Simutnik, gen. et sp. nov. (Chalcidoidea, Encyrtidae) from Rovno amber. Journal of Hymenoptera Research 94: 105–120. https://doi.org/10.3897/jhr.94.94773
- Simutnik SA, Perkovsky EE, Pankowski MV (2023) A new genus and species of Encyrtidae (Hymenoptera: Chalcidoidea) with a four-segmented funicle from late Eocene Baltic amber. Zootaxa 5389(1): 119–127. https://doi.org/10.11646/zootaxa.5389.1.6
- Song SN (2015) Comparative mitogenomics and phylogeny of the Microsatrinae (Hymenoptera: Braconidae). PhD Thesis, Zhejiang University, Hangzhou, China.
- Talavera G, Castresana J (2007) Improvement of Phylogenies after Removing Divergent and Ambiguously Aligned Blocks from Protein Sequence Alignments. Systematic Biology 56(4): 564–577. https://doi.org/10.1080/10635150701472164
- Tamura K, Stecher G, Kumar S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution 38(7): 3022–3027. https://doi.org/10.1093/molbev/msab120
- Trjapitzin VA (1989) Parasitic Hymenoptera of the Fam. Encyrtidae of Palaearctics. Nauka, Leningrad, 489 pp.
- Wang DP, Fei L, Wang L, Huang S, Yu J (2011) Nonsynonymous substitution rate (Ka) is a relatively consistent parameter for defining fast-evolving and slow-evolving protein-coding genes. Biology Direct 6(1): 13. https://doi.org/10.1186/1745-6150-6-13
- Wang Y, Zhou QS, Qiao HJ, Zhang AB, Yu F, Wang XB, Zhu CD, Zhang YZ (2016) Formal nomenclature and description of cryptic species of the Encyrtus sasakii complex (Hymenoptera: Encyrtidae). Scientific Reports 6(1): 34372. https://doi.org/10.1038/srep34372
- Wang HY, Zhang CH, Xue H, Xi CX, Yang ZN, Zu GH (2023) Encyrtidae (Hymenoptera: Chalcidoidea) from China, with the description of two new species. Zootaxa 5361(2): 237–251. https://doi.org/10.11646/zootaxa.5361.2.5
- Wei SJ (2009) Characterization and evolution of hymenopteran mitochondrial genomes and their phylogenetic utility. PhD Thesis, Zhejiang University, Hangzhou, China.
- Wei SJ, Shi M, Sharkey MJ, van Achterberg C, Chen XX (2010) Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and the phylogenetic utility of mitochondrial genomes with special reference to Holometabolous insects. BMC Genomics 11(1): 371. https://doi.org/10.1186/1471-2164-11-371
- Wolstenholme DR (1992a) Genetic novelties in mitochondrial genomes of multicellular animals. Current Opinion in Genetics & Development 2(6): 918–925. https://doi.org/10.1016/S0959-437X(05)80116-9
- Wolstenholme DR (1992b) Animal mitochondrial DNA: Structure and evolution. International Review of Cytology 141: 173–216. https://doi.org/10.1016/S0074-7696(08)62066-5
- Xing ZP, Liang X, Wang X, Hu HY, Huang YX (2022) Novel gene rearrangement pattern in mitochondrial genome of Ooencyrtus plautus Huang & Noyes, 1994: New gene order in Encyrtidae (Hymenoptera, Chalcidoidea). ZooKeys 1124: 1–21. https://doi.org/10.3897/zookeys.1124.83811
- Xiong M, Zhou QS, Zhang YZ (2019) The complete mitochondrial genome of Encyrtus infelix (Hymenoptera: Encyrtidae). Mitochondrial DNA. Part B, Resources 4(1): 114–115. https://doi.org/10.1080/23802359.2018.1537727
- Xu W, Lin SP, Liu HY (2021) Mitochondrial genomes of five Hyphessobrycon tetras and their phylogenetic implications. Ecology and Evolution 11(18): 12754. https://doi.org/10.1002/ece3.8019
- Zhang YZ, Huang DW (2001) Two new Encyrtid parasites (Hymenoptera: Chalcidoidea) from China. Oriental Insects 35(1): 311–319. https://doi.org/10.1080/00305316.2001.10417310
- Zhang YZ, Xu ZH (2009) A review of Chinese species of Leptomastidea Mercet (Hymenoptera: Encyrtidae). Acta Entomologica Sinica 52(4): 420–423.
- Zhang JX, Lindsey ARI, Peters RS, Heraty JM, Hopper KR, Werren JH, Martinson EO, Woolley JB, Yoder MJ, Krogmann L (2020a) Conflicting signal in transcriptomic markers leads to a poorly resolved backbone phylogeny of chalcidoid wasps. Systematic Entomology 45(4): 783–802. https://doi.org/10.1111/syen.12427
- Zhang D, Gao FL, Jakovlić I, Zou H, Zhang J, Li WX, Wang GT (2020b) 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
- Zhao HF, Chen Y, Wang ZT, Chen HF, Qin YG (2021) Two complete mitogenomes of Chalcididae (Hymenoptera: Chalcidoidea): genome description and phylogenetic implications. Insects 12(12): 1049. https://doi.org/10.3390/insects12121049
- Zhou QS, Xiong M, Luo AR, Zhang YZ, Zhu CD (2021) The complete mitochondrial genome of Metaphycus eriococci (Timberlake) (Hymenoptera: Encyrtidae). Mitochondrial DNA. Part B, Resources 6(2): 550–552. https://doi.org/10.1080/23802359.2021.1872450
- Zhu JC, Tang P, Zhou BY, Wu Q, Wei SJ, Chen XX (2018) The first two mitochondrial genomes of the family Aphelinidae with novel gene orders and phylogenetic implications. International Journal of Biological Macromolecules 118(A): 386–396. https://doi.org/10.1016/j.ijbiomac.2018.06.087
- Zhu JC, Xiao H, Tang P, Li XF, Li XK, Zhu CD, Wu Q, Xiao JH, van Achterberg C, Huang DW, Chen XX (2023) Evolutionary timescale of chalcidoid wasps inferred from over one hundred mitochondrial genomes. Zoological Research 44(3): 467–482. https://doi.org/10.24272/j.issn.2095-8137.2022.379