Abstract
New sequencing technologies are providing a large-scale proliferation of sequence data, including complete mitochondrial genomes as a side effect of target capture methods. In this study, we use massively parallel sequencing to provide the nearly complete mitochondrial genome of the ant Octostruma stenognatha. The annotation of the genome revealed an interesting pattern that agrees with a recent deep reorganization in the systematics within the Formicidae family. This is the first mitogenome for the genus in a lineage, where the scarcity of mitochondrial information has restricted our understanding of its evolutionary history. This is a valuable example of the power and velocity with which products from new sequencing technologies can increase our capacity to understand evolutionary biology, especially in non-model species.
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References
Andrews S. (2010). FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
Babbucci M, Basso A, Scupola A, Patarnello T, Negrisolo E (2014) Is it an ant or a butterfly? Convergent evolution in the Mitochondrial Gene Order of Hymenoptera and Lepidoptera. Genome Biol Evol 6:3326–3343. doi:10.1093/gbe/evu265
Baroni Urbani C, de Andrade ML (1994) First description of fossil Dacetini ants with a critical analysis of the current classification of the tribe (amber collection Stuttgart: Hymenoptera, Formicidae. VI: Dacetini). Stuttgarter Beiträge zur Naturkunde Serie B 198:1–65
Berman M, Austin CM, Miller AD (2014) Characterisation of the complete mitochondrial genome and 13 microsatellite loci through next-generation sequencing for the new Caledonian spider-ant Leptomyrmex pallens. Mol Biol Rep 41:1179–1187. doi:10.1007/s11033-013-2657-5
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69:313–319. doi:10.1016/j.ympev.2012.08.023
Boore JL (1999) Animal mitochondrial genomes. Nucleic Acids Res 27:1767–1780. doi:10.1093/nar/27.8.1767
Boore JL, Lavrov DV, Brown WM (1998) Gene translocation links insects and crustaceans. Nature 392:667–668. doi:10.1038/33577
Brown WL Jr (1948) A preliminary generic revision of the higher Dacetini (Hymenoptera: Formicidae). Trans Am Entomol Soc 74:101–129
Brown WLJ (1949) Revision of the ant tribe Dacetini. I. Fauna of Japan, China and Taiwan. Muschi 20:1:25
Cameron SL (2014) Insect mitochondrial genomics: implications for evolution and Phylogeny. Annu Rev Entomol 59:95–117. doi:10.1146/annurev-ento-011613-162007
Cameron SL, Dowton M, Castro LR, Ruberu K, Whiting MF, Austin AD, Diement K, Stevens J (2008) Mitochondrial genome organization and phylogeny of two vespid wasps. Genome 51:800–808. doi:10.1139/g08-066
de Melo Rodovalho C, Lyra ML, Ferro M, Bacci Jr M (2014) The Mitochondrial genome of the leaf-cutter ant Atta laevigata: a Mitogenome with a large number of Intergenic spacers. PLoS One 9(5):e97117. doi:10.1371/journal.pone.0097117
Dlussky GM, Brothers DJ, Rasnitsyn AP (2003) The first late Cretaceous ants (Hymenoptera: Formicidae) from southern Africa, with comments on the origin of the Myrmicinae. Insect Syst Evol 35:1–13. doi:10.1163/187631204788964727
do Amaral RF, Neves LG, Resende MFR, Mobili F, Miyaki CY, Pellegrino KCM, Biondo C (2015) Ultraconserved elements Sequencing as a low-cost source of complete Mitochondrial Genomes and Microsatellite markers in non-model Amniotes. PLoS One 10:e0138446. doi:10.1371/journal.pone.0138446
Dowton M, Austin AD (1999) Evolutionary dynamics of a mitochondrial rearrangement ‘hot spot’ in the Hymenoptera. Mol Biol Evol 16:298–309. doi:10.1093/oxfordjournals.molbev.a026111
Duan X-Y, Peng X-Y, Qian Z-Q (2016) The complete mitochondrial genomes of two globally invasive ants, the Argentine ant Linepithema humile and the little fire ant Wasmannia auropunctata. Conserv Genet Resour. doi:10.1007/s12686-016-0555-6
Dunn CW, Giribet G, Edgecombe GD, Hejnol A (2014) Animal Phylogeny and its evolutionary Implications. Annu Rev Ecol Evol Syst 45:371–395. doi:10.1146/annurev-ecolsys-120213-091627
Faircloth BC (2013) Illumiprocessor: a Trimmomatic wrapper for parallel adapter and quality trimming. http://dx.doi.org/10.6079/J9ILL
Faircloth BC (2016) PHYLUCE is a software package for the analysis of conserved genomic loci. Bioinformatics 32:786–788. doi:10.1093/bioinformatics/btv646
Faircloth BC, Glenn TC (2012) Not all sequence tags are created equal: designing and validating sequence identification tags robust to Indels. PLoS One 7:e42543. doi:10.1371/journal.pone.0042543
Faircloth BC, McCormack JE, Crawford NG, Harvey MG, Brumfield RT, Glenn TC (2012) Ultraconserved elements anchor Thousands of genetic markers spanning multiple evolutionary Timescales. Syst Biol 61:717–726. doi:10.1093/sysbio/sys004
Faircloth BC, Branstetter MG, White ND, Brady SG (2014) Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera. Mol Ecol Resour 15:489–501. doi:10.1111/1755-0998.12328
Fisher S, Barry A, Abreu J, Minie B, Nolan J, Delorey TM, Young G, Fennell TJ, Allen A, Ambrogio L, Berlin AM, Blumenstiel B, Cibulskis K, Friedrich D, Johnson R, Juhn F, Reilly B, Shammas R, Stalker J, Sykes SM, Thompson J, Walsh J, Zimmer A, Zwirko Z, Gabriel S, Nicol R, Nusbaum C (2011) A scalable, fully automated process for construction of sequence-ready human exome targeted capture libraries. Genome Biol 12:R1. doi:10.1186/gb-2011-12-1-r1
Forel A (1917) Cadre synoptique actuel de la faune universelle des fourmis. Bulletin de la Société Vaudoise des Sciences Naturelles 51:229–253
Gnirke A, Melnikov A, Maguire J, Rogov P, LeProust EM, Brockman W, Fennell T, Giannoukos G, Fisher S, Russ C, Gabriel S, Jaffe DB, Lander ES, Nusbaum C (2009) Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol 27:182–189. doi:10.1038/nbt.1523
Gotzek D, Clarke J, Shoemaker D (2010) Mitochondrial genome evolution in fire ants (Hymenoptera: Formicidae). BMC Evol Biol 10:300. doi:10.1186/1471-2148-10-300
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652. doi:10.1038/nbt.1883
Gutrich JJ, VanGelder E, Loope L (2007) Potential economic impact of introduction and spread of the red imported fire ant, Solenopsis invicta, in Hawaii. Environ Sci Policy 10:685–696. doi:10.1016/j.envsci.2007.03.007
Hasegawa E, Kobayashi K, Yagi N, Tsuji K (2011) Complete mitochondrial genomes of normal and cheater morphs in the parthenogenetic ant Pristomyrmex punctatus (Hymenoptera: Formicidae). Myrmecol News 15(85):90
Havird JC, Santos SR (2014) Performance of single and Concatenated sets of Mitochondrial genes at Inferring Metazoan relationships relative to full Mitogenome data. PLoS One 9:e84080. doi:10.1371/journal.pone.0084080
Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University Press, Cambridge
Hung C-M, Lin R-C, Chu J-H, Yeh C-F, Yao C-J, Li S-H (2013) The de novo assembly of Mitochondrial Genomes of the extinct passenger pigeon (Ectopistes migratorius) with next generation sequencing. PLoS One 8:e56301. doi:10.1371/journal.pone.0056301
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 28:1647–1649. doi:10.1093/bioinformatics/bts199
Le TH, Blair D, Agatsuma T, Humair P-F, Campbell NJH, Iwagami M, Littlewood DTJ, Peacock B, Johnston DA, Bartley J, Rollinson D, Herniou EA, Zarlenga DS, McManus DP (2000) Phylogenies inferred from Mitochondrial gene orders–a cautionary tale from the parasitic Flatworms. Mol Biol Evol 17:1123–1125. doi:10.1093/oxfordjournals.molbev.a026393
Liu G-H, Shao R, Li J-Y, Zhou D-H, Li H, Zhu X-Q (2013) The complete mitochondrial genomes of three parasitic nematodes of birds: a unique gene order and insights into nematode phylogeny. BMC Genom 14:414. doi:10.1186/1471-2164-14-414
Liu N, Duan X-Y, Qian Z-Q, Wang X-Y, Li X-L, Ding M-Y (2016) Characterization of the complete mitochondrial genome of the Myrmicine ant Vollenhovia emeryi (Insecta: Hymenoptera: Formicidae). Conserv Genet Resour. doi:10.1007/s12686-016-0535-x
Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B (2012) RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucl Acids Res 40:W622–W627. doi:10.1093/nar/gks540
Mao M, Valerio A, Austin AD, Dowton M, Johnson NF (2012) The first mitochondrial genome for the wasp superfamily Platygastroidea: the egg parasitoid Trissolcus basalis. Genome 55:194–204. doi:10.1139/g2012-005
Mao M, Gibson T, Dowton M (2015) Higher-level phylogeny of the Hymenoptera inferred from mitochondrial genomes. Mol Phylogenet Evol 84:34–43. doi:10.1016/j.ympev.2014.12.009
Moritz C (1987) Evolution of animal Mitochondrial Dna: relevance for population biology and systematics. Annu Rev Ecol Syst 18:269–292. doi:10.1146/annurev.ecolsys.18.1.269
Pérez SP, Corley JC, Farji-Brener AG (2010) Potential impact of the leaf-cutting ant Acromyrmex lobicornis on conifer plantations in northern Patagonia, Argentina. Agric For Entomol 13:191–196. doi:10.1111/j.1461-9563.2010.00515.x
Perseke M, Golombek A, Schlegel M, Struck TH (2013) The impact of mitochondrial genome analyses on the understanding of deuterostome phylogeny. Mol Phylogenet Evol 66:898–905. doi:10.1016/j.ympev.2012.11.019
Picardi E, Pesole G (2012) Mitochondrial genomes gleaned from human whole-exome sequencing. Nat Methods 9:523–524. doi:10.1038/nmeth.2029
Ramakodi MP, Singh B, Wells JD, Guerrero F, Ray DA (2015) A 454 sequencing approach to dipteran mitochondrial genome research. Genomics 105:53–60. doi:10.1016/j.ygeno.2014.10.014
Rohland N, Reich D (2012) Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture. Genome Res 22:939–946. doi:10.1101/gr.128124.111
Saito S, Tamura K, Aotsuka T (2005) Replication origin of mitochondrial DNA in insects. Genetics 171:1695–1705
Sankoff D, Bryant D, Deneault M, Lang BF, Burger G (2000) Early Eukaryote evolution based on Mitochondrial Gene Order Breakpoints. J Comput Biol 7:521–535. doi:10.1089/10665270075005092
Shen H, Braband A, Scholtz G (2015) The complete mitogenomes of lobsters and crayfish (Crustacea: Decapoda: Astacidea) reveal surprising differences in closely related taxa and convergences to Priapulida. J Zool Syst Evol Res 53:273–281. doi:10.1111/jzs.12106
Smith MJ, Arndt A, Gorski S, Fajber E (1993) The phylogeny of echinoderm classes based on mitochondrial gene arrangements. J Mol Evol 36:545–554. doi:10.1007/bf00556359
Song S-N, Tang P, Wei S-J, Chen X-X (2016) Comparative and phylogenetic analysis of the mitochondrial genomes in basal hymenopterans. Sci Rep 6:20972. doi:10.1038/srep20972
Tan MH, Gan HM, Schultz MB, Austin CM (2015) Corrigendum to ‘MitoPhAST, a new automated mitogenomic phylogeny tool in the post-genomic era with a case study of 89 decapod mitogenomes including eight new freshwater crayfish mitogenomes’ [Mol. Phylogenet. Evol. 85 (2015) 180–188]. Mol Phylogenet Evol 87:118. doi: 10.1016/j.ympev.2015.03.017
Ward PS, Brady SG, Fisher BL, Schultz TR (2014) The evolution of Myrmicine ants: phylogeny and biogeography of a hyperdiverse ant clade (Hymenoptera: Formicidae). Syst Entomol 40:61–81. doi:10.1111/syen.12090
Way M (1992) Role of ants in pest-management. Annu Rev Entomol 37:479–503. doi:10.1146/annurev.ento.37.1.479
Wei S, Shi M, Sharkey MJ, van Achterberg C, Chen X (2010) Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and the phylogenetic utility of mitochondrial genomes with special reference to Holometabolous insects. BMC Genom 11:371. doi:10.1186/1471-2164-11-371
Xiao J-H, Jia J-G, Murphy RW, Huang D-W (2011) Rapid evolution of the Mitochondrial genome in Chalcidoid Wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. PLoS One 6:e26645. doi:10.1371/journal.pone.0026645
Yang S, Li X, Cai L-G, Qian Z-Q (2016) Characterization of the complete mitochondrial genome of Formica selysi (Insecta: Hymenoptera: Formicidae: Formicinae). Mitochondrial DNA 27(5):3378–3380
Yuan Y, Li Q, Yu H, Kong L (2012) The complete Mitochondrial Genomes of Six Heterodont Bivalves (Tellinoidea and Solenoidea): variable gene arrangements and phylogenetic implications. PLoS ONE 7:e32353. doi:10.1371/journal.pone.0032353
Acknowledgements
We thank Rogério R. Silva for providing the specimen used in this project. We also thank Michael Branstetter for sharing his specific laboratory protocol and two anonymous reviewers for constructive criticism of our manuscript. This study was funded by a grant from Conselho Nacional de Desenvolvimento Científico e Tecnológico (486843/2012-2) to MRP.
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Ströher, P.R., Zarza, E., Tsai, W.L.E. et al. The mitochondrial genome of Octostruma stenognatha and its phylogenetic implications. Insect. Soc. 64, 149–154 (2017). https://doi.org/10.1007/s00040-016-0525-8
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DOI: https://doi.org/10.1007/s00040-016-0525-8