vavilovВавиловский журнал генетики и селекцииVavilov Journal of Genetics and Breeding2500-3259Institute of Cytology and Genetics of Siberian Branch of the RAS10.18699/vjgb-25-94vavilov-4814Research ArticleФИЛОГЕНЕТИКАHIGH-THROUGHPUT PHENOTYPINGНовый молекулярный маркер для филогенетических исследований стрекоз (Insecta, Odonata), включающий части консервативных генов гистонов Н3 и Н4 и спейсер между ними, применимый и к другим организмамA new molecular marker including parts of conservative histone H3 and H4 genes and the spacer between them for phylogenetic studies in dragonflies (Insecta, Odonata), extendable to other organismsМглинецА. В.MglinetsA. V.

 Новосибирск 

 Novosibirsk 

БулгаковаВ. С.BulgakovaV. S.

 Новосибирск 

 Novosibirsk 

КостеринО. Э.KosterinO. E.

 Новосибирск 

 Novosibirsk 

kosterin@bionet.nsc.ruФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наукРоссияInstitute of Cytology and Genetics of the Siberian Branch of the Russian Academy of SciencesRussian FederationФедеральный исследовательский центр Институт цитологии и генетики Сибирского отделения Российской академии наук; Новосибирский национальный исследовательский государственный университетРоссияInstitute of Cytology and Genetics of the Siberian Branch of the Russian Academy of Sciences; Novosibirsk State UniversityRussian Federation202509102025296868882Copyright © Мглинец А.В., Булгакова В.С., Костерин О.Э., 20252025Мглинец А.В., Булгакова В.С., Костерин О.Э.Mglinets A.V., Bulgakova V.S., Kosterin O.E.This work is licensed under a Creative Commons Attribution 4.0 License.https://vavilov.elpub.ru/jour/article/view/4814

Несмотря на значительный прогресс в геномных исследованиях, до сих пор существует потребность в молекулярных маркерах, удобных для секвенирования по Сэнгеру и позволяющих делать филогенетические реконструкции на коротких эволюционных дистанциях. Предложен новый молекулярный маркер, район генов гистонов Н3 и Н4, содержащий части кодирующих последовательностей генов гистонов Н3 и Н4 и некодирующий спейсер между ними. Он может быть удобен для молекулярно-филогенетических исследований на родовом, видовом и даже внутривидовом уровне у насекомых и некоторых других групп, в том числе из других типов. Высококонсервативные кодирующие последовательности гистоновых генов обеспечивают универсальность праймеров и однозначность первичного выравнивания, тогда как вариабельный некодирующий спейсер содержит достаточно изменчивости для анализа на коротких эволюционных дистанциях. У насекомых гены гистонов находятся в гистоновом повторе, тандемно повторенном в десятках или сотнях копий в так называемом гистоновом кластере. Это обеспечивает высокую концентрацию матрицы для нового маркера в препаратах геномной ДНК. Однако порядок и ориентация конкретных генов у разных отрядов изменчива, что налагает определенные ограничения на использование предлагаемого маркера. В нашей работе эффективность маркера продемонстрирована на материале отряда стрекоз (Odonata), где он хорошо разрешил семейства, роды и виды. Новый маркер также выявил интересный паттерн взаимоотношения двух видов рода Sympetrum, S. croceolum и S. uniforme, показав последовательности последнего в качестве ветви среди последовательностей первого. Та же комбинация разработанных нами оригинальных праймеров будет работать и в отряде двукрылых (Diptera).

In spite of recent substantial progress in genomic approaches, there is still a need for molecular markers convenient for Sanger sequencing and providing good phylogenetic reconstructions at short evolutionary distances. A new molecular marker, the histone H3–H4 region, containing partial coding sequences of the genes for histones H3 and H4 and the non-coding spacer between them, is proposed. This marker is potentially useful for molecular phylogenetic studies at the generic, species, and even intra-species level in insects and some other organisms, even from other phyla. The highly conserved histone-coding sequences ensure the universality of primers and the ease of primary alignment, while the highly variable non-coding spacer provides enough variation for analyses at short evolutionary distances. In insects, the histone genes reside in the histone repeat which is tandemly repeated in dozens to hundred copies forming the so-called histone cluster. This ensures a high concentration of the template for the marker in genomic DNA preparations. However, the order and orientation of the histone genes in the histone repeat is variable among orders, which puts some limitations on the use of the proposed marker. The marker efficacy is hereby shown for Odonata (dragonflies and damselflies), where it provided good resolution at the family, genus and species levels. The new marker also provided an interesting pattern in the relationship of two Sympetrum species, S. croceolum and S. uniforme, showing the sequences of the latter as a branch nested among those of the former. The same combination of the proposed original primers should also work in Diptera.

гистоновый повторгистон Н3гистон Н4межгенный спейсерOdonataстрекозынасекомыемолекулярный маркерфилогенетические исследованияhistone repeathistone H3histone H4intergenic spacerOdonatadragonfliesinsectsmolecular markerphylogenetic studiesThe work was supported by the project FWNR-2022-0019 of the Institute of Cytology and Genetics SB RAS. DNA sequencing was performed at the SB RAS Genomics Core Facility, Novosibirsk. Assembly of sequences from the SRA archive was performed at the Siberian SuperComputer Computational Facility, Novosibirsk.ReferencesAvise J.C. Phylogeography: retrospect and prospect. J Biogeogr. 2009; 36:3-15. doi 10.1111/j.1365-2699.2008.02032.x Ballard J.W.O., Whitlock M.C. The incomplete natural history of mitochondria. Mol Ecol. 2004;13:729-744. doi 10.1046/j.1365-294x. 2003.02063.xAvise J.C. Phylogeography: retrospect and prospect. J Biogeogr. 2009; 36:3-15. doi 10.1111/j.1365-2699.2008.02032.x Ballard J.W.O., Whitlock M.C. The incomplete natural history of mitochondria. Mol Ecol. 2004;13:729-744. doi 10.1046/j.1365-294x. 2003.02063.xBerdnikov V.A. Evolution and Progress. Sofia; Moscow: Pensoft, 1999 Bybee S.M., Kalkman V.J., Erickson R.J., Frandsen P.B., Breinholt J.W., Suvorov A., Dijkstra K.B., … Abbott J.C., Sanchez Herrera M., Lemmon A.R., Moriarty Lemmon E., Ware J.L. Phylogeny and classification of Odonata using targeted genomics. Mol Phyl Evol. 2021;160:107115. doi 10.1016/j.ympev.2021.107115Berdnikov V.A. Evolution and Progress. Sofia; Moscow: Pensoft, 1999 Bybee S.M., Kalkman V.J., Erickson R.J., Frandsen P.B., Breinholt J.W., Suvorov A., Dijkstra K.B., … Abbott J.C., Sanchez Herrera M., Lemmon A.R., Moriarty Lemmon E., Ware J.L. Phylogeny and classification of Odonata using targeted genomics. Mol Phyl Evol. 2021;160:107115. doi 10.1016/j.ympev.2021.107115Carle F.L., Kjer K.M., May M.L. A molecular phylogeny and classification of Anisoptera. Arthropod Syst Phylo. 2015;73(2):281-301. doi 10.3897/asp.73.e31805Carle F.L., Kjer K.M., May M.L. A molecular phylogeny and classification of Anisoptera. Arthropod Syst Phylo. 2015;73(2):281-301. doi 10.3897/asp.73.e31805Cheng Y.-C., Chen M.-Y., Wang J.-F., Liang A.P., Lin C.-P. Some mitochondrial genes perform better for damselfly phylogenetics: species- and population-level analyses of four complete mitogenomes of Euphaea sibling species. Syst Entomol. 2018;43(4):702-715. doi 10.1111/syen.12299Cheng Y.-C., Chen M.-Y., Wang J.-F., Liang A.P., Lin C.-P. Some mitochondrial genes perform better for damselfly phylogenetics: species- and population-level analyses of four complete mitogenomes of Euphaea sibling species. Syst Entomol. 2018;43(4):702-715. doi 10.1111/syen.12299Cheng Z., Li Q., Deng J., Liu Q., Huang X. The devil is in the details: Problems in DNA barcoding practices indicated by systematic evaluation of insect barcodes. Front Ecol Evol. 2023;11:1149839. doi 10.3389/fevo.2023.1149839Cheng Z., Li Q., Deng J., Liu Q., Huang X. The devil is in the details: Problems in DNA barcoding practices indicated by systematic evaluation of insect barcodes. Front Ecol Evol. 2023;11:1149839. doi 10.3389/fevo.2023.1149839Chevreux B., Wetter T., Suhai S. Genome sequence assembly using trace signals and additional sequence information. In: Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB). 1999;99:45-56Chevreux B., Wetter T., Suhai S. Genome sequence assembly using trace signals and additional sequence information. In: Computer Science and Biology: Proceedings of the German Conference on Bioinformatics (GCB). 1999;99:45-56Deng J., Assandri G., Chauhan P., Futahashi R., Galimberti A., Hansson B., Lancaster L.T., Takahashi Y., Svensson E.I., Douploy A. Wolbachia-driven selective sweep in a range expanding insect species. BMC Ecol Evol. 2021;21:181. doi 10.1186/s12862-021-01906-6Deng J., Assandri G., Chauhan P., Futahashi R., Galimberti A., Hansson B., Lancaster L.T., Takahashi Y., Svensson E.I., Douploy A. Wolbachia-driven selective sweep in a range expanding insect species. BMC Ecol Evol. 2021;21:181. doi 10.1186/s12862-021-01906-6Dijkstra K.D.B., Bechly G., Bybee S.M., Dow R.A., Dumont H.J., Fleck G., Garrison R.W., … Theischinger G., Trueman J.W.H., Van Tol J., Von Ellenrieder N., Ware J. The classification and diversity of dragonflies and damselflies (Odonata). Zootaxa. 2013;3703(1): 36-45. doi 10.11646/zootaxa.3703.1.9Dijkstra K.D.B., Bechly G., Bybee S.M., Dow R.A., Dumont H.J., Fleck G., Garrison R.W., … Theischinger G., Trueman J.W.H., Van Tol J., Von Ellenrieder N., Ware J. The classification and diversity of dragonflies and damselflies (Odonata). Zootaxa. 2013;3703(1): 36-45. doi 10.11646/zootaxa.3703.1.9Dijkstra J.P., Kalkman V. Taxonomy. In: Boudot J.P., Kalkman V.J. (Eds). Atlas of the European dragonflies and damselflies. The Netherlands: KNNNV Publishing, 2015;15-25 Doenecke D., Albig V., Bode C., Drabent B., Franke K., Gavenis K., Witt O. Histones: genetic diversity and tissue-specific gene expression. Histochem Cell Biol. 1997;107:1-10. doi 10.1007/s0041800 50083Dijkstra J.P., Kalkman V. Taxonomy. In: Boudot J.P., Kalkman V.J. (Eds). Atlas of the European dragonflies and damselflies. The Netherlands: KNNNV Publishing, 2015;15-25 Doenecke D., Albig V., Bode C., Drabent B., Franke K., Gavenis K., Witt O. Histones: genetic diversity and tissue-specific gene expression. Histochem Cell Biol. 1997;107:1-10. doi 10.1007/s0041800 50083Dow R.A., Butler S.G., Reels G.T., Steinhoff O.M., Stokvis F., Unggang L. Previously unpublished Odonata records from Sarawak, Borneo, part IV: Bintulu Division including the Planted Forest Project and Similajau National Park. J Int Dragonfly Fund. 2019;27: 1-66Dow R.A., Butler S.G., Reels G.T., Steinhoff O.M., Stokvis F., Unggang L. Previously unpublished Odonata records from Sarawak, Borneo, part IV: Bintulu Division including the Planted Forest Project and Similajau National Park. J Int Dragonfly Fund. 2019;27: 1-66Dubatolov V.V., Kosterin O.E. Nemoral species of Lepidoptera (Insecta) in Siberia: a novel view on their history and the timing of their range disjunctions. Entomol Fennica. 2000;11(3):141-166. doi 10.33338/ef.84061Dubatolov V.V., Kosterin O.E. Nemoral species of Lepidoptera (Insecta) in Siberia: a novel view on their history and the timing of their range disjunctions. Entomol Fennica. 2000;11(3):141-166. doi 10.33338/ef.84061Dumont H.J., Vierstraete A., Vanfleteren J.R. Molecular phylogeny of the Odonata (Insecta). Syst Entomol. 2010;35(1):6-18. doi 10.1111/ j.1365-3113.2009.00489.xDumont H.J., Vierstraete A., Vanfleteren J.R. Molecular phylogeny of the Odonata (Insecta). Syst Entomol. 2010;35(1):6-18. doi 10.1111/ j.1365-3113.2009.00489.xEirín-López J.M., González-Romero R., Dryhurst D., Méndez J., Ausio J. Long-term evolution of histone families: old notions and new insights into their mechanisms of diversification across euka­ ryotes. In: Pontarotti P. (Ed.). Evolutionary Biology: Concept, Modeling, and Application. Heidelberg: Springer, 2009;139-162. doi 10.1007/978-3-642-00952-5_8Eirín-López J.M., González-Romero R., Dryhurst D., Méndez J., Ausio J. Long-term evolution of histone families: old notions and new insights into their mechanisms of diversification across euka­ ryotes. In: Pontarotti P. (Ed.). Evolutionary Biology: Concept, Modeling, and Application. Heidelberg: Springer, 2009;139-162. doi 10.1007/978-3-642-00952-5_8Eldredge N., Gould S.L. Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf T.J.M. (Ed.). Models in Palaeobiology. San Francisco: Freeman, Cooper & Co., 1972;82-115Eldredge N., Gould S.L. Punctuated equilibria: an alternative to phyletic gradualism. In: Schopf T.J.M. (Ed.). Models in Palaeobiology. San Francisco: Freeman, Cooper & Co., 1972;82-115Ferreira S., Lorenzo-Carballa M.O., Torres-Cambas Y., Cordero-Rivera A., Thompson D.J., Watts P.C. New EPIC nuclear DNA sequence markers to improve the resolution of phylogeographic studies of coenagrionids and other odonates. Int J Odonatol. 2014;17(2-3): 135-147. doi 10.1080/13887890.2014.950698Ferreira S., Lorenzo-Carballa M.O., Torres-Cambas Y., Cordero-Rivera A., Thompson D.J., Watts P.C. New EPIC nuclear DNA sequence markers to improve the resolution of phylogeographic studies of coenagrionids and other odonates. Int J Odonatol. 2014;17(2-3): 135-147. doi 10.1080/13887890.2014.950698Ferreira S., Boudot J.-P., El Haissoufi M., Alves P.C., Thompson D.J., Watts P.C. Genetic distinctiveness of the damselfly Coenagrion puella in North Africa: an overlooked and endangered taxon. Conserv Genet. 2016;17:985-991. doi 10.1007/s10592-016-0826-5Ferreira S., Boudot J.-P., El Haissoufi M., Alves P.C., Thompson D.J., Watts P.C. Genetic distinctiveness of the damselfly Coenagrion puella in North Africa: an overlooked and endangered taxon. Conserv Genet. 2016;17:985-991. doi 10.1007/s10592-016-0826-5Futahashi R., Kawahara-Miki R., Kinoshita M., Yoshitake K., Yajima S., Arikawa K., Fukatsu T. Extraordinary diversity of visual opsin genes in dragonflies. Proc Natl Acad Sci USA. 2015;112(11): E1247-E1256. doi 10.1073/pnas.1424670112Futahashi R., Kawahara-Miki R., Kinoshita M., Yoshitake K., Yajima S., Arikawa K., Fukatsu T. Extraordinary diversity of visual opsin genes in dragonflies. Proc Natl Acad Sci USA. 2015;112(11): E1247-E1256. doi 10.1073/pnas.1424670112Galimberti A., Assandri G., Maggioni D., Ramazotti F., Baroni D., Bazzi G., Chiandetti I., … Ramellini S., Santinelli R., Soldato G., Surdo S., Casiraghi M. Italian odonates in the Pandora’s box: a comprehensive DNA barcoding inventory shows taxonomic warnings at the Holarctic scale. Mol Ecol Resour. 2021;21(1):183-200. doi 10.1111/1755-0998.13235Galimberti A., Assandri G., Maggioni D., Ramazotti F., Baroni D., Bazzi G., Chiandetti I., … Ramellini S., Santinelli R., Soldato G., Surdo S., Casiraghi M. Italian odonates in the Pandora’s box: a comprehensive DNA barcoding inventory shows taxonomic warnings at the Holarctic scale. Mol Ecol Resour. 2021;21(1):183-200. doi 10.1111/1755-0998.13235Geiger M., Koblmüller S., Assandri G., Chovanec A., Ekrem T., Fischer I., Galimberti A., … Sittenthaler M., Stur E., Tończyk G., Zangl L., Moriniere J. Coverage and quality of DNA barcode references for Central and Northern European Odonata. PeerJ. 2021; 9:e11192. doi 10.7717/peerj.11192Geiger M., Koblmüller S., Assandri G., Chovanec A., Ekrem T., Fischer I., Galimberti A., … Sittenthaler M., Stur E., Tończyk G., Zangl L., Moriniere J. Coverage and quality of DNA barcode references for Central and Northern European Odonata. PeerJ. 2021; 9:e11192. doi 10.7717/peerj.11192Goodenough U. Genetics. Hong Kong: CBS College Publishing, 1984 Gurdon C., Svab Z., Feng Y., Kumar D., Maliga P. Cell-to-cell movement of mitochondria in plants. Proc Natl Acad Sci USA. 2016; 113(12):3395-3400. doi 10.1073/pnas.1518644113Goodenough U. Genetics. Hong Kong: CBS College Publishing, 1984 Gurdon C., Svab Z., Feng Y., Kumar D., Maliga P. Cell-to-cell movement of mitochondria in plants. Proc Natl Acad Sci USA. 2016; 113(12):3395-3400. doi 10.1073/pnas.1518644113Hovmöller R., Johansson F. A phylogenetic perspective on larval spine morphology in Leucorrhinia (Odonata: Libellulidae) based on ITS1, 5.8s and ITS2 rDNA sequences. Mol Phyl Evol. 2004;30(3): 653-662. doi 10.1016/S1055-7903(03)00226-4Hovmöller R., Johansson F. A phylogenetic perspective on larval spine morphology in Leucorrhinia (Odonata: Libellulidae) based on ITS1, 5.8s and ITS2 rDNA sequences. Mol Phyl Evol. 2004;30(3): 653-662. doi 10.1016/S1055-7903(03)00226-4Karube H., Futahashi R., Sasamoto A., Kawashima I. Taxonomic revision of Japanese Odonata species, based on nuclear and and mitochondrial gene genealogies and morphological comparison with allied species. Part I. Tombo. 2012;54:75-106Karube H., Futahashi R., Sasamoto A., Kawashima I. Taxonomic revision of Japanese Odonata species, based on nuclear and and mitochondrial gene genealogies and morphological comparison with allied species. Part I. Tombo. 2012;54:75-106Kohli M., Letsch H., Greve C., Bethoux O., Deregnaucourt I., Liu S., Zhou X., … Rust J., Wappler T., Yu X., Misof B., Ware J. Evolutionary history and divergence times of Odonata (dragonflies and damselflies) revealed through transcriptomics. iScience 2021;24(11): 103324. doi 10.1016/j.isci.2021.103324Kohli M., Letsch H., Greve C., Bethoux O., Deregnaucourt I., Liu S., Zhou X., … Rust J., Wappler T., Yu X., Misof B., Ware J. Evolutionary history and divergence times of Odonata (dragonflies and damselflies) revealed through transcriptomics. iScience 2021;24(11): 103324. doi 10.1016/j.isci.2021.103324Kosterin O.E. Discovery of East-Asiatic dragonfly (Odonata, Libellulidae) at the Manzherock Lake (Altay). In: Cherepanov A.I. (Ed.). Nasekomye, kleshchi i gel’minty. Novye i maloizvestnye vidy fauny Sibiri. Novosibirsk: Nauka, 1987;57-63 [in Russian]Kosterin O.E. Discovery of East-Asiatic dragonfly (Odonata, Libellulidae) at the Manzherock Lake (Altay). In: Cherepanov A.I. (Ed.). Nasekomye, kleshchi i gel’minty. Novye i maloizvestnye vidy fauny Sibiri. Novosibirsk: Nauka, 1987;57-63 [in Russian]Kosterin O.E. Western range limits and isolates of eastern odonate species in Siberia and their putative origins. Odonatologica. 2002; 34(3):219-242Kosterin O.E. Western range limits and isolates of eastern odonate species in Siberia and their putative origins. Odonatologica. 2002; 34(3):219-242Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947-2948. doi 10.1093/bioinformatics/btm404Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics. 2007;23(21):2947-2948. doi 10.1093/bioinformatics/btm404Lorenzo-Carballa M.O., Sanmartín-Villar I., Cordero-Rivera A. Molecular and morphological analyses support different taxonomic units for Asian and Australo-Pacific forms of Ischnura aurora (Odonata, Coenagrionidae). Diversity. 2022;14(8):606. doi 10.3390/d14080606Lorenzo-Carballa M.O., Sanmartín-Villar I., Cordero-Rivera A. Molecular and morphological analyses support different taxonomic units for Asian and Australo-Pacific forms of Ischnura aurora (Odonata, Coenagrionidae). Diversity. 2022;14(8):606. doi 10.3390/d14080606Lowe C.D., Harvey I.F., Thompson D.J., Watts P.C. Strong genetic divergence indicates that congeneric damselflies Coenagrion puella and C. pulchellum (Odonata: Zygoptera: Coenagrionidae) do not hybridise. Hydrobiologia. 2008;605:55-63. doi 10.1007/s10750-008-9300-9Lowe C.D., Harvey I.F., Thompson D.J., Watts P.C. Strong genetic divergence indicates that congeneric damselflies Coenagrion puella and C. pulchellum (Odonata: Zygoptera: Coenagrionidae) do not hybridise. Hydrobiologia. 2008;605:55-63. doi 10.1007/s10750-008-9300-9Mayr E. Zoological species and evolution. Cambridge, Massachusetts: The Belknap Press of Harward University Press, 1963 Needham J.G., Fischer E. The nymphs of North American libelluline dragonflies. Trans Am Entomol Soc. 1936;62(2):107-116Mayr E. Zoological species and evolution. Cambridge, Massachusetts: The Belknap Press of Harward University Press, 1963 Needham J.G., Fischer E. The nymphs of North American libelluline dragonflies. Trans Am Entomol Soc. 1936;62(2):107-116Onishko V., Kosterin O. Dragonflies of Russia. Illustrated Photo Guide. Moscow: Phyton XXI, 2021 [in Russian] Ožana S., Dolný A., Pánek T. Nuclear copies of mitochondrial DNA as a potential problem for phylogenetic and population genetic studies of Odonata. Syst Entomol. 2022;47(4):591-602. doi 10.1111/syen. 12550Onishko V., Kosterin O. Dragonflies of Russia. Illustrated Photo Guide. Moscow: Phyton XXI, 2021 [in Russian] Ožana S., Dolný A., Pánek T. Nuclear copies of mitochondrial DNA as a potential problem for phylogenetic and population genetic studies of Odonata. Syst Entomol. 2022;47(4):591-602. doi 10.1111/syen. 12550Pilgrim E.M., von Dohlen C.D. Phylogeny of the dragonfly genus Sympetrum (Odonata: Libellulidae). Org Divers Evol. 2012;12:281- 295. doi 10.1007/s13127-012-0081-7Pilgrim E.M., von Dohlen C.D. Phylogeny of the dragonfly genus Sympetrum (Odonata: Libellulidae). Org Divers Evol. 2012;12:281- 295. doi 10.1007/s13127-012-0081-7Popova O.N., Haritonov A.Y. On the distribution of Sympetrum croceolum in the Russian part of its range (Odonata: Libellulidae). Odonatologica. 2020;49(1/2):29-49. doi 10.5281/zenodo.3823325Popova O.N., Haritonov A.Y. On the distribution of Sympetrum croceolum in the Russian part of its range (Odonata: Libellulidae). Odonatologica. 2020;49(1/2):29-49. doi 10.5281/zenodo.3823325Schmidt E. Generic reclassification of some Westpalearctic Odonata taxa in view of their Nearctic affinities. Adv Odonatol. 1987;3(1): 135-145Schmidt E. Generic reclassification of some Westpalearctic Odonata taxa in view of their Nearctic affinities. Adv Odonatol. 1987;3(1): 135-145Schneider T., Vierstraete A., Kosterin O.E, Ikemeyer D., Hu F.-S., Snegovaya N., Dumont H.J. Molecular phylogeny of Holarctic Aeshnidae with a focus on the West Palaearctic and some remarks on its genera worldwide (Aeshnidae, Odonata). Diversity. 2023;15(9): 950. doi 10.3390/d15090950Schneider T., Vierstraete A., Kosterin O.E, Ikemeyer D., Hu F.-S., Snegovaya N., Dumont H.J. Molecular phylogeny of Holarctic Aeshnidae with a focus on the West Palaearctic and some remarks on its genera worldwide (Aeshnidae, Odonata). Diversity. 2023;15(9): 950. doi 10.3390/d15090950Solovyev V.I., Bogdanova V.S., Dubatolov V.V., Kosterin O.E. Range of a Palearctic uraniid moth Eversmannia exornata (Lepidoptera: Uraniidae: Epipleminae) was split in the Holocene, as evaluated using histone H1 and COI genes with reference to the Beringian disjunction in the genus Oreta (Lepidoptera: Drepanidae). Org Divers Evol. 2015;15(2):285-300. doi 10.1007/s13127-014-0195-1Solovyev V.I., Bogdanova V.S., Dubatolov V.V., Kosterin O.E. Range of a Palearctic uraniid moth Eversmannia exornata (Lepidoptera: Uraniidae: Epipleminae) was split in the Holocene, as evaluated using histone H1 and COI genes with reference to the Beringian disjunction in the genus Oreta (Lepidoptera: Drepanidae). Org Divers Evol. 2015;15(2):285-300. doi 10.1007/s13127-014-0195-1Solovyev V.I., Dubatolov V.V., Vavilova V.Y., Kosterin O.E. Estimating range disjunction time of the Palaearctic Admirals (Limenitis L.) with COI and histone H1 genes. Org Divers Evol. 2022;22:975- 1002. doi 10.1007/s13127-022-00565-9Solovyev V.I., Dubatolov V.V., Vavilova V.Y., Kosterin O.E. Estimating range disjunction time of the Palaearctic Admirals (Limenitis L.) with COI and histone H1 genes. Org Divers Evol. 2022;22:975- 1002. doi 10.1007/s13127-022-00565-9Staden R., Judge D.P., Bonfield J.K. Managing sequencing projects in the GAP4 environment. In: Krawetz S.A., Womble D.D. (Eds). Introduction to Bioinformatics. Human Press Inc., 2023;327-224. doi 10.1007/978-1-59259-335-4_20Staden R., Judge D.P., Bonfield J.K. Managing sequencing projects in the GAP4 environment. In: Krawetz S.A., Womble D.D. (Eds). Introduction to Bioinformatics. Human Press Inc., 2023;327-224. doi 10.1007/978-1-59259-335-4_20Stein G.S., Stein J.L., Marzluff W.F. (Eds). Histone Genes: Structure, Organization, and Regulation. New York: Willey, 1984 Tamura K., Stecher G., Peterson D., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725-2729. doi 10.1093/molbev/mst197Stein G.S., Stein J.L., Marzluff W.F. (Eds). Histone Genes: Structure, Organization, and Regulation. New York: Willey, 1984 Tamura K., Stecher G., Peterson D., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30: 2725-2729. doi 10.1093/molbev/mst197

The authors declare that there are no conflicts of interest present.