The mitochondrial gene order and CYTB gene evolution in insects

Over millions of years of evolution, the genomes of modern insects have accumulated a significant number of mutations, which often can lead up a blind alley when carrying out phylogenetic research. Genomic differences between some representatives belonging to the same family or group are often so great that they demand using nonconventional methods of the phylogenetic analysis. It is known that molecular evolution goes by the way of not only single nucleotide substitutions, but also by larger genomic reorganizations, such as insertion or deletion of large genome fragments, and even changing the order of genes. Mitochondrial DNA genes (mtDNA) are quite often used as markers for phylogenetic research into many organisms including arthropods, because mtDNA is multicopied, is inherited maternally, does not undergo recombination and accumulates mutations quickly enough (relative to the nuclear genome). To date, a large number of full nucleotide sequences of mitogenomes (thousands of organisms) has been deposited in public databases; however, their phylogenetic analysis has obstacles, especially for representatives of the insects (Insecta), whose evolution takes a considerable part of geological time. In this work we describe the application and a comparison of two ways of the phylogenetic analysis for different groups of insects. The first method uses the variability of the nucleotide sequence of mtDNA, and the second one analyses the order of genes in full mitochondrial genomes of insects that can be used as an additional marker in phylogenetic research into representatives of the order Hymenoptera.

gene order, mitochondrial DNA, Insects, Hymenoptera, mitoSpider, CYTB, phylogeny

1. Adams K.L., Palmer J.D. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 2003; 29(3):380-395. DOI 10.1016/S1055-7903(03)00194-5.

2. Babbucci M., Basso A., Scupola A., Patarnello T., Negrisolo E. Is it an ant or a butterfly? Convergent evolution in the mitochondrial gene order of Hymenoptera and Lepidoptera. Genome Biol. Evol. 2014; 6(12):3326-3343. DOI 10.1093/gbe/evu265.

3. Berg O.G., Kurland C.G. Why mitochondrial genes are most often found in nuclei. Mol. Biol. Evol. 2000;17(6):951-961.

4. Boore J.L., Brown W.M. Big trees from little genomes: Mitochondrial gene order as a phylogenetic tool. Curr. Opin. Genet. Dev. 1998;8:668-674. DOI 10.1016/S0959-437X (98)80035-X.

5. Castellana S., Vicario S., Saccone C. Evolutionary patterns of the mitochondrial genome in Metazoa: exploring the role of mutation and selection in mitochondrial protein coding genes. Genome Biol. Evol. 2011;3:1067-1079. DOI 10.1093/gbe/evr040.

6. Dowton M. Relationships among the cyclostome braconid (Hymenoptera, Braconidae) subfamilies inferred from a mitochondrial tRNA gene rearrangement. Mol. Phylogenet. Evol. 1999;11:283-287. DOI 10.1006/mpev.1998.0580.

7. Dowton M., Austin A.D. Evolutionary dynamics of a mitochondrial rearrangement “hot spot” in the Hymenoptera. Mol. Biol. Evol. 1999; 16:298-309.

8. Gissi C., Iannelli F., Pesole G. Evolution of the mitochondrial genome of Metazoa as exemplified by comparison of congeneric species. Heredity (Edinb). 2008;101(4):301-320. DOI 10.1038/hdy.2008.62.

9. Goloboff P.A., Farris J.S., Nixon K.C. TNT, a free program for phylogenetic analysis. Cladistics. 2008;24:774-786. DOI 10.1111/j.10960031.2008. 00217.x.

10. Hu F., Lin Y., Tang J. MLGO: phylogeny reconstruction and ancestral inference from gene-order data. BMC Bioinformatics. 2014;15(1): 354. DOI 10.1186/s12859-014-0354-6.

11. Huerta-Cepas J., Dopazo J., Gabaldón T. ETE: a python Environment for Tree Exploration. BMC Bioinformatics. 2010;11:24. DOI 10.1186/1471-2105-11-24.

12. Jiang P., Li H., Song F., Cai Y., Wang J., Liu J., Cai W. Duplication and remolding of tRNA genes in the mitochondrial genome of Reduvius tenebrosus (Hemiptera: Reduviidae). Int. J. Mol. Sci. 2016;17(6): 951. DOI 10.3390/ijms17060951.

13. Kayal E., Bentlage B., Collins A.G., Kayal M., Pirro S., Lavrov D.V. Evolution of linear mitochondrial genomes in medusozoan cnidarians. Genome Biol. Evol. 2012;4(1):1-12. DOI 10.1093/gbe/evr123.

14. Kim M.J., Hong E.J., Kim I. Complete mitochondrial genome of Camponotus atrox (Hymenoptera: Formicidae): a new tRNA arrangement in Hymenoptera. Genome. 2016;59(1):59-74. DOI 10.1139/gen-2015-0080.

15. Kumar S., Stecher G., Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016;33(7):1870-1874. DOI 10.1093/molbev/msw054.

16. Li H., Liu H., Shi A., Stys P., Zhou X., Cai W. The complete mitochondrial genome and novel gene arrangement of the unique-headed bug Stenopirates sp. (Hemiptera: Enicocephalidae). PLoS ONE. 2012; 7(1):e29419. DOI 10.1371/journal.pone.0029419.

17. Mao M., Gibson T., Dowton M. Higher-level phylogeny of the Hymenoptera inferred from mitochondrial genomes. Mol. Phylogenet. Evol. 2015;84:34-43. DOI 10.1016/j.ympev.2014.12.009.

18. Marcet-Houben M., Gabaldón T. TreeKO a duplication aware algorithm for the comparison of phylogenetic trees. Nucl. Acids Res. 2011;39(10):e66.

19. Nedoluzhko A., Sharko F., Boulygina E., Tsygankova S., Sokolov A., Mazur A., Polilov A., Prokhortchouk E., Skryabin K. The complete mitochondrial genome of the smallest known free-living insect Scydosella musawasensis. Mitochondrial DNA. Part B. 2016;1(1):171172. DOI 10.1080/23802359.2016.1149785.

20. Rastorguev S.M., Nedoluzhko A.V., Mazur A.M., Gruzdeva N.M., Volkov A.A., Barmintseva A.E., Mugue N.S., Prokhortchouk E.B. High-throughput SNP-genotyping analysis of the relationships among Ponto-Caspian sturgeon species. Ecol. Evol. 2013;3(8):26122618. DOI 10.1002/ece3.659.

21. Sokolov A.S., Nedoluzhko A.V., Boulygina E.S., Tsygankova S.V., Sharko F.S., Gruzdeva N.M., Shishlov A.V., Kolpakova A.V., Rezepkin A.D., Skryabin K.G., Prokhortchouk E.B. Six complete mitochondrial genomes from Early Bronze Age humans in the North Caucasus. J. Archaeol. Sci. 2016;73:138-144. DOI 10.1016/j.jas.2016.07.017.