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A New Case of Recombination between Nuclear and Mitochondrial Genomes in the Genus Calliope Gould, 1836 (Muscicapidae, Aves): The Hypothesis of Origin Calliope pectoralis Gould, 1837

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Abstract

For the first time we propose a hypothesis of hybrid origin of Calliope pectoralis from two species, C. calliope and C. obscura, based on the new molecular genetic data and phenotypic characters. We examined 80 samples of C. calliope and one sample of С. pectoralis tschebaiewi. We discovered that products of the cytochrome b gene, as well as three transport RNAs, ND6, and a control region (3.2 kb) were heterogeneous in 22 specimens of C. calliope. The result of cloning of these amplicons produced two clone variants: the cytochrome b gene of C. calliope and the nuclear pseudogene homologous to the cytochrome b gene of C. pectoralis (96% match). Computer assisted phylogenetic analysis of the connections between the cloned sequences for the mtDNA cytochrome b gene and its nuclear copies revealed a distribution into two clades: C. calliope and C. pectoralis. This can be explained by an intergenomic recombination event, namely, a transfer of C. calliope’s nuclear copy of the cytochrome b gene into a mitochondrial genome of a hybrid female that later became the founder of the C. pectoralis species. According to morphological features, the second species involved in hybridization with C. calliope was probably C. obscura, since it is the only species of the Calliope genus that has a black breast and black outer tail feathers with white bases similar to those of C. pectoralis.

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REFERENCES

  1. Song, H., Buhay, J.E., Whiting, M.F., and Crandall, K.A., Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified, Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, pp. 13486—13491. https://doi.org/10.1073/pnas.0803076105

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bensasson, D., Zhang, D.-X., Hartl, D.L., and Hewitt, G.M., Mitochondrial pseudogenes: evolution’s misplaced witnesses, Trends Ecol. Evol., 2001, vol. 16, pp. 314—321.

    Article  CAS  PubMed  Google Scholar 

  3. Andrianov, B.V., Romanov, D.A., Gorelova, T.V., et al., Transfer of mitochondrial DNA to nuclear genome of cells of passaged cell line of Drosophila virilis, Russ. J. Genet., 2013, vol. 49, no. 6, pp. 685—689. https://doi.org/10.1134/S1022795413060021.

    Article  CAS  Google Scholar 

  4. Bernt, M., Braband, A., Schierwater, B., and Stadler, P.F., Genetic aspects of mitochondrial genome evolution, Mol. Phyl. Evol., 2013, vol. 69, pp. 328—338. https://doi.org/10.1016/j.ympev.2012.10.020

    Article  CAS  Google Scholar 

  5. Arctander, P., Comparison of a mitochondrial gene and a corresponding nuclear pseudogene, Proc. R. Soc. London, Ser. B, 1995, vol. B 262, pp. 13—19.

  6. Zhang, D.-X. and Hewitt, G.M., Nuclear integrations: challenges for mitochondrial DNA markers, Trends Evol. Ecol., 1996, vol. 11, pp. 247—251.

    Article  CAS  Google Scholar 

  7. Triant, D.A. and DeWoody, J.A., The occurrence, detection, and avoidance of mitochondrial DNA translocations in mammalian systematics and phylogeography, J. Mamm., 2007, vol. 88, pp. 908—920.

    Article  Google Scholar 

  8. Grechko, V.V., The problems of molecular phylogenetics with the example of squamate reptiles: mitochondrial DNA markers, Mol. Biol. (Moscow), 2013, vol. 47, no. 1, pp. 55—74.

    Article  CAS  Google Scholar 

  9. Grzybowski, T., Malyarchuk, B.A., Czarny, J., et al., High level of mitochondrial DNA heteroplasmy in single hair roots: reanalysis and revision, Electrophoresis, 2003, vol. 24, pp. 1159—1165.

    Article  CAS  PubMed  Google Scholar 

  10. Kraytsberg, Y., Schwartz, M., Brown, T.A., et al., Recombination of human mitochondrial DNA, Science, 2004, vol. 304, p. 981.

    Article  CAS  PubMed  Google Scholar 

  11. Spiridonova, L.N., Red’kin, Ya.A., Valchuk, O.P., and Kryukov, A.P., Nuclear mtDNA pseudogenes as a source of new variants of the mtDNA cytochrome b haplotypes: a case study of Siberian rubythroat Luscinia calliope (Muscicapidae, Aves), Russ. J. Genet., 2016, vol. 52, no. 9, pp. 952—962. https://doi.org/10.1134/S1022795416090131.

    Article  CAS  Google Scholar 

  12. Sangster, G., Alstrom, P., Forsmark, E., and Olsson, U., Multilocus phylogenetic analysis of Old World chats and flycatchers reveals extensive paraphyly at family, subfamily and genus level (Aves: Muscicapidae), Mol. Phylogenet. Evol., 2010, vol. 57, pp. 380—392. https://doi.org/10.1016/j.ympev.2010.07.008

    Article  PubMed  Google Scholar 

  13. Alstrom, P., Song, G., Zhang, R., et al., Taxonomic status of blackthroat Calliope obscura and firethroat C. pectardens, Forktail, 2013, vol. 29, pp. 94—99.

    Google Scholar 

  14. Dickinson, E.C. and Christidis, L., The Howard and Moore Complete Checklist of the Birds of the World: Passerines, vol. 2, Eastbourne: Aves Press, 2014, 4th ed.

    Google Scholar 

  15. del Hoyo, J. and Collar, N.J., HBW and BirdLife International Illustrated Checklist of the Birds of the World, vol. 2: Passerines, Barcelona: Lynx, 2016.

    Google Scholar 

  16. Loskot, V.M. and Daletskaya, K.K., Plumages and size variation of the Himalayan rubythroat, Luscinia pectoralis (Gould, 1837) (Aves: Muscicapidae), Zoosyst. Ross., 2001, vol. 9, pp. 463—486.

    Google Scholar 

  17. Spiridonova, L.N., Valchuk, O.P., Red’kin, Ya.A., et al., Phylogeography and demographic history of Siberian rubythroat Luscinia calliope, Russ. J. Genet., 2017, vol. 53, no. 8, pp. 885—902. https://doi.org/10.1134/S1022795417080105.

    Article  CAS  Google Scholar 

  18. Vaurie, Ch., The Birds of the Palearctic Fauna: A Systematic Reference. Order Passeriformes, London: Witherby, 1959.

    Google Scholar 

  19. Collar, N., Family Turdidae: Handbook of the Birds of the World, Cuckoo-Shrikes to Thrushes, Del Hoyo, J., Elliott, A., and Christie, D., Eds., Barcelona: Lynx, 2005, vol. 10, pp. 514—807.

    Google Scholar 

  20. Rasmussen, P.C. and Anderton, J.C., Birds of South Asia, in The Ripley Guide: 2. Attributes and Status, Washington D.C.: The Smithsonian Institution, 2012, 2nd ed.

    Google Scholar 

  21. Liu, Y., Chen, G., Huang, Q., et al., Species delimitation of the white-tailed rubythroat Calliope pectoralis complex (Aves, Turdidae) using an integrative taxonomic approach, J. Avian Biol., 2016, vol. 47, pp. 001—012.

  22. Bonfield, J.K., Smith, K.F., and Staden, R., A new DNA sequence assembly program, Nucleic Acids Res., 1995, vol. 23, pp. 4992—4999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: molecular evolutionary genetics analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725—2729. https://doi.org/10.1093/molbev/mst197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Librado, P. and Rozas, J., DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, 2009, vol. 25, pp. 1451—1452.

    Article  CAS  PubMed  Google Scholar 

  25. Martin, D.P., Williamson, C., and Posada, D., RDP2: recombination detection and analysis from sequence alignments, Bioinformatics, 2005, vol. 21, no. 2, pp. 260—262.

    Article  CAS  PubMed  Google Scholar 

  26. Pavlova, A., Rohwer, S., Drovetski, S.V., and Zink, R.M., Different post-Pleistocene histories of Eurasian parids, J. Hered., 2006, vol. 97, pp. 389—402.

    Article  CAS  PubMed  Google Scholar 

  27. Haring, E., Gamauf, A., and Kryukov, A., Phylogeographic patterns in widespread corvid birds, Mol. Phyl. Evol., 2007, vol. 45, pp. 840—862.

    Article  CAS  Google Scholar 

  28. Dohms, K.M. and Burg, T.M., Molecular markers reveal limited population genetic structure in a North American corvid, Clark’s nutcracker (Nucifraga columbiana), PLoS One, 2013, vol. 8. e79621.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zink, R.M., Drovetski, S.V., Questiau, S., et al., Recent evolutionary history of the bluethroat (Luscinia svecica) across Eurasia, Mol. Ecol., 2003, vol. 12, pp. 3069—3075.

    Article  PubMed  Google Scholar 

  30. Pavlova, A., Zink, R.M., Drovetski, S.V., et al., Phylogeographic patterns in Motacilla flava and M. citreola: species limits and population history, Auk, 2003, vol. 120, pp. 744—758.

    Article  Google Scholar 

  31. Zink, R.M., Pavlova, A., Drovetski, S., and Rohwer, S., Mitochondrial phylogeographies of five widespread Eurasian bird species, J. Ornithol., 2008, vol. 149, pp. 399—413.

    Article  Google Scholar 

  32. Drovetski, S.V., Zink, R.M., Ericson, P.G.P., and Fadeev, I.V., A multilocus study of pine grosbeak phylogeography supports the pattern of greater intercontinental divergence in Holarctic boreal forest birds than in birds inhabiting other high-latitude habitats, J. Biogeogr., 2010, vol. 37, pp. 696—706.

    Article  Google Scholar 

  33. Weber-Lotfi, F., Koulintchenko, M.V., Ibrahim, N., et al., Nucleic acid import into mitochondria: new insights into the translocation pathways, Biochim. Biophys. Acta, 2015, vol. 1853, pp. 3165—3181. https://doi.org/10.1016/j.bbamcr.2015.09.011

    Article  CAS  PubMed  Google Scholar 

  34. Konstantinov, Yu.M., Ditrish, A., Veber-Lotfi, F., et al., DNA import into mitochondria, Biochemistry (Moscow), 2016, vol. 81, no. 10, pp. 1044—1056. https://doi.org/10.1134/S0006297916100035.

    Article  CAS  PubMed  Google Scholar 

  35. Lopez, J.V., Yuhki, N., Masuda, R., et al., Numt, a recent transfer and tandem amplification of mitochondrial DNA to the nuclear genome of the domestic cat, J. Mol. Evol., 1994, vol. 39, pp. 174—190.

    CAS  PubMed  Google Scholar 

  36. Randler, C., Avian hybridization, mixed pairing and female choice, Anim. Behav., 2002, vol. 63, no. 1, pp. 103—119.

    Article  Google Scholar 

  37. Lamichhaney, S., Han, F., Webster, M.T., et al., Rapid hybrid speciation in Darwin’s finches, Science, 2017. https://doi.org/10.1126/science.aao4593

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Authors and Affiliations

  1. Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch, Russian Academy of Sciences, 690022 , Vladivostok, Russia

    L. N. Spiridonova & O. P. Valchuk

  2. Zoological Museum, Moscow State University, 125009, Moscow, Russia

    Ya. A. Red’kin

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  1. L. N. Spiridonova
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  2. O. P. Valchuk
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  3. Ya. A. Red’kin
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Correspondence to L. N. Spiridonova.

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Translated by I. Grishina

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Spiridonova, L.N., Valchuk, O.P. & Red’kin, Y.A. A New Case of Recombination between Nuclear and Mitochondrial Genomes in the Genus Calliope Gould, 1836 (Muscicapidae, Aves): The Hypothesis of Origin Calliope pectoralis Gould, 1837. Russ J Genet 55, 89–99 (2019). https://doi.org/10.1134/S1022795419010137

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