Genetic structuring of Anatolian Bombus lapidarius L. (Apidae: Hymenoptera) populations
Yıl 2018,
Cilt: 7 Sayı: 2, 180 - 195, 17.08.2018
Burcu Temel Altun
,
Ertan Mahir Korkmaz
,
Hasan Hüseyin Başıbüyük
Öz
Anatolia is one of the
important regions which have contributed to current biodiversity of Europe. It
is suggested that some of the current central and northern populations of
Europe have been originated from populations took refuge during glacial ages. Cold
preferring animals are accepted as model organisms because they exhibit range
expansion and range contraction patterns during glacial and interglacial
periods, respectively. In order to improve our knowledge on biogeography and genetic
diversity of Anatolia, the distribution pattern of Bombus lapidarius were investigated in the Black Sea region using
COI and nCTB genes from 14
populations. High numbers of unique and diverse haplotypes were observed
in both markers, suggesting genetic differentiations among populations.
East-West differentiation is particularly supported throughout the Black Sea
region. All analyses indicate that the East 4 and East 5 populations exhibit significantly
differentiation from other populations. This differentiation is directly
related to the geographical distribution patterns of populations. These
populations constitute a separate lineage at the same time. In addition,
Western populations can be accepted as recently derived populations.
Kaynakça
- [1] Hewitt GM. Post–glacial re–colonization of European biota. Biological Journal of the Linnean Society, 1999; 68, 87–112.
- [2] Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology, 2007; 4, 1.
- [3] Ansell S, Stenøien HK., Grundmann M, et al. The importance of Anatolian mountains as the cradle of global diversity in Arabis alpina, a key arctic–alpine species. Annals of Botany, 2011; 108, 241–252.
- [4] Atkinson RJ, Rokas A, Stone GN. Longitudinal patterns in species richness and genetic diversity in European oaks and oak gallwasps. pp. 127–151, Eds. Weiss S. and Ferrand N., Phylogeography of Southern European Refugia. Springer, Dordrecht, The Netherlands. 2007.
- [5] Çıplak B. Biogeography of Anatolia: the marker group Orthoptera. Memorie della Società Entomologica Italiana, 82, 2004; 357–372.
- [6] Çıplak B. The analogy between interglacial and global warming for the glacial relicts in a refugium, pp. 135–163. Ed. Fattorini S., Insect Ecology and Conservation, Research Signpost. 2008.
- [7] Çıplak B, Kaya S, Gündüz İ. Phylogeography of Anterastes serbicus species group (Orthoptera, Tettigoniidae): phylogroups correlate with mountain belts, but not with the morphospecies. Journal of Orthoptera Research, 2010; 19, 29–40.
- [8] Hewitt GM. Some genetic consequence of ice ages, and their role in diverging and speciation. Biological Journal of the Linnean Society, 1996; 58, 247–276.
- [9] Kaya S, Çıplak B, Gündüz I. Estimating effects of global warming from past range changes for cold demanding refugial taxa: a case study on South-west Anatolian species Poecilimon birandi. Biologia, 67, 2012; 1152–1164.
- [10] Korkmaz EM, Lunt DH, Çıplak B, et al. The contribution of Anatolia to European phylogeography: the centre of origin of the meadow grasshopper, Chorthippus parallelus. Journal of Biogeograph, 2014; 41, 1793–1805.
- [11] Rokas A, Atkinson RJ, Webster LM. Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum–Mediterranean oak gallwasp Andricus quercustozae. Molecular Ecology, 2003; 12, 2153–2174.
- [12] Husemann M, Schmitt T, Zachos FE, et al. Palaearctic biogeography revisited: evidence for the existence of a North African refugium for Western Palaearctic biota. Journal of Biogeography, 2014; 41, 81–94.
- [13] Yılmaz Y, Tüysüz O, Yiğitbaş E, et al. Geology and tectonic evolution of the Pontides, pp. 183–226, Ed. Robinson A.G., Regional and Petroleum Geology of the Black Sea and Surrounding Region. AAPG Memoir, Tulsa, 1997.
- [14] Şekercioğlu Ç.H, Anderson S, Akcay E, et al. Turkey’s globally important biodiversity in crisis. Biological Conservation, 2011; 144, 2752–2769.
- [15] Ahmadzadeh F, Flecks M, Rödder D, et al. Multiple dispersal out of Anatolia: biogeography and evolution of oriental green lizards. Biological Journal of the Linnean Society, 2013; 110, 398–408.
- [16] Ambarlı D, Zeydanlı US, Balkız Ö, et al. An overview of biodiversity and conservation status of steppes of the Anatolian biogeographical region. Biodiversity and Conservation, 2016; s10531-016-1172-0,.
- [17] Kryštufek B, Vohralik V, Obuch J. Endemism, vulnerability and conservation issues for small terrestrial mammals from the Balkans and Anatolia. Folia Zoologica, 2009; 58, 291–302.
- [18] Mutun S. Review of oak gall wasps phylogeographic patterns in Turkey suggests a main role of the Anatolian diagonal. Turkish Journal of Forestry, 2016; 17, 1–6.
- [19] Williams PH. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of the British Museum (Natural History) Entomology, 1998; 67, 79–152.
- [20] Kim MJ, Yoon HJ, Im HH, et al. Mitochondrial DNA sequence variation of the bumblebee, Bombus ardens (Hymenoptera: Apidae). Journal of Asia-Pacific Entomology, 2009; 12, 133–139.
- [21] Lecocq T, Gérard M, Michez D, et al. Conservation genetics of European bees: new insights from the continental scale. Conservation Genetics, 2017; 18, 585–596.
- [22] Lopez‑Uribe MM, Soro A, Jha S. Conservation genetics of bees: advances in the application of molecular tools to guide bee pollinator conservation. Conservation Genetics, 2017; 18, 501–506.
- [23] Hines HM. Historical biogeography, divergence times and diversification patterns of Bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology, 2008; 57, 58–75.
- [24] Lecocq T, Dellicour S, Michez D, et al. Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BioMed Central Evolutionary Biology, 2013; 13, 263.
- [25] Rasmont P, Flagothier D. Biogeographie et choix florauxdes bourdons (Hymenoptera, Apidae) de la Turquie, NATO 8, 1996.
- [26] Özbek H. Doğu Anadolu’nun bazı yörelerindeki Bombinae (Hymoneptera: Apoidae, Bombidae) türleri üzerindeki taksonomik ve bazı biyolojik çalışmalar, Atatürk Üniversitesi Yayınları, No: 621, Atatürk Üniv. Basımevi, Erzurum, pp: 70., 1983.
- [27] Williams PH, Cameron SA, Hines HM, et al. A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, 2008; 39, 46–74.
- [28] Pedersen BV. European bumblebees (Hymenoptera: Bombini) – phylogenetic relationships inferred from DNA sequences. Insect Systematics and Evolution, 2002; 33, 1399-560.
- [29] Ewing B, Hillier L, Wendl MC, et al. Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730, USA., 1998.
- [30] Tamura K, Stecher G, Peterson D, et al. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 2013; 30, 2725–2729.
- [31] Librado P, Rozas J. DnaSP v5.0, A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009; 25, 1451–1452.
- [32] Nei M. Molecular Evolutionary Genetics. Columbia University Press, New York, 1987.
- [33] Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics, 1983; 105, 437–460.
- [34] Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 2005; 1, 47–50.
- [35] Tajima F. The effect of change in population size on DNA polymorphism. Genetics, 1989; 123, 597–601.
- [36] Fu Y-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 1997; 147, 915–925.
- [37] Dupanloup I, Schneider S, Excoffier L. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 2002; 11, 2571–81.
- [38] Weir BS, Cockherham CC. Estimating F–statistics for the analysis of population structure. Evolution, 1984; 38, 1358–1370.
- [39] Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 2006; 6, 288–295.
- [40] Hutchison DW, Templeton AR. Correlation of ikili genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 1999; 53, 1898–1914.
- [41] Kimura MA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 1980; 16, 111–20.
- [42] Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 1999; 16, 37–48.
- [43] D’Errico I, Gadaleta G, Saccone C. Pseudogenes in Metazoa: origin and features. Briefings in Functional Genomics & Proteomics, 2004; 3, 157–167.
- [44] Lopez JV, Yuhki N, Masuda R, et al. Numt, a recent transfer and tandem amplifications of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution, 1994; 39, 174–190.
- [45] Nugent JM, Palmer JD. RNA-mediated transfer of the gene COXII from the mitochondrion to the nucleus during flowering plant evolution. Cell, 1991; 66, 473–481.
- [46] Ermakov OA, Simonov E, Surin VL, et al. Implications of hybridization, NUMTs, and overlooked diversity for DNA barcoding of Eurasian ground squirrels. PLoS One, 2015; 10, e0117201.
- [47] Perez T, Rodríguez F, Fernández M, et al. Ancient mitochondrial pseudogenes reveal hybridization between distant lineages in the evolution of the Rupicapra genus. Gene, 2017; 628, 63–71.
- [48] Du Buy HG, Riley FL. Hybridization between the nuclear and kinetoplast DNA’s of Leishmania enriettii and between nuclear and mitochondrial DNA’s of mouse liver. Proceedings of the National Academy of Sciences USA, 1967; 57, 790–797.
- [49] Bensasson D, Zhang D.X, Hartl D L, et al. Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology & Evolution, 2001; 16, 314–321.
- [50] Richly E, Leister D. NUMTs in sequenced eukaryotic genomes. Molecular Biology and Evolution, 2004; 21, 1081–1084.
- [51] Martins JJr, Solomon SE, Mikheyev AS, et al. Nuclear mitochondrial-like sequences in ants: evidence from Atta cephalotes (Formicidae: Attini). Insect Molecular Biology, 2007; 16, 777–784.
- [52] Gaziev AI, Shaikhaev GO. Nuclear mitochondrial pseudogenes. Molecular Biology, 2010; 44, 358–368.
- [53] Magnacca KN, Brown MJ. Mitochondrial heteroplasmy and DNA barcoding in Hawaiian Hylaeus (Nesoprosopis) bees (Hymenoptera: Colletidae). BMC Evolutionary Biology, 2010; 10, 174.
- [54] Cristiano MP, Fernandes-Salomao TM, Yotoko KSC. Nuclear mitochondrial DNA: an Achilles’ heel of molecular systematics, phylogenetics, and phylogeographic studies of stingless bees. Apidologie, 2012; 43, 527.
- [55] Pamilo P, Viljakainen L, Vihavainen A. Exceptionally high density of NUMTs in the honeybee genome. Molecular Biology and Evolution, 2007; 24, 1340–1346.
- [56] Vijakainen L, Oliveira DC, Werren JH, et al. Transfers of mitochondrial DNA to the nuclear genome in the wasp Nasonia vitripennis. Insect Molecular Biology, 2010; 19, 27–35.
- [57] Ruiz C, William De JM, J. Javier GQ, et al. Presence of nuclear copies of mitochondrial origin (NUMTs) in two related species of stingless bee genus Melipona (Hymenoptera: Meliponini). Journal of Zoological Systematics and Evolutionary Research, 2013; 51, 107–113.
- [58] Ko YJ, Yang EC, Lee JH, et al. Characterization of cetacean Numt and its application into cetacean phylogeny. Genes & Genomics, 2015; 37, 1061–1071.
- [59] Miraldo A, Hewitt GM, Dear PH, et al. Numts help to reconstruct the demographic history of the ocellated lizard (Lacerta lepida) in a secondary contact zone. Molecular Ecology, 2012; 21, 1005–1018.
- [60] Gündüz I, Jaarola M, Tez C. Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Sciuridae, Rodentia) in Turkey. Molecular Phylogenetics and Evolution, 2007; 43, 916–935.
- [61] Hampe A, Arroyo J, Jordano P. Rangewide phylogeography of a bird–dispersed Eurasian shrub: contrasting Mediterranean and temperate glacial refugia. Molecular Ecology, 2003; 12, 3415–3426.
- [62] Naydenov K, Senneville S, Beaulieu J. Glacial vicariance in Eurasia: mitochondrial DNA evidence from Scots pine for a complex heritage involving genetically distinct refugia at mid-northern latitudes and in Asia Minor. BMC Evolutionary Biology, 2007; 7, 233–244.
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Anadolu Bombus lapidarius L. (Apidae: Hymenoptera) populasyonlarının genetik yapılanması
Yıl 2018,
Cilt: 7 Sayı: 2, 180 - 195, 17.08.2018
Burcu Temel Altun
,
Ertan Mahir Korkmaz
,
Hasan Hüseyin Başıbüyük
Öz
Anadolu,
Avrupa’nın günümüz biyoçeşitliliğine önemli derecede katkı sağlayan bölgelerden
birisidir. Bazı günümüz orta ve kuzey Avrupa populasyonlarının buzul dönemlerinde
Anadolu’da barınmış populasyonlardan giden öncülerce oluşturulduğu
savunulmaktadır. Soğuk tercih eden hayvanlar yayılış örüntülerinde buzul
dönemlerinde genişleme buzullar arası dönemlerde ise daralma sergiledikleri
için model organizmalar olarak kabul edilmektedir. Bu kapsamda Anadolu’nun tarihsel
biyocoğrafyası ve genetik çeşitliliği konusunda bilgi edinmek amacıyla
Karadeniz bölgesinde yayılış gösteren Bombus
lapidarius’un 14 kadar populasyonundan COI
ve nCTB gen bölgeleri çalışılmıştır. Her iki belirteç açısından da haplotip
çeşitliliği ve özgün haplotip sayısı yüksek olup, populasyonlar arasında
anlamlı bir genetik farklılaşma saptanmıştır. Özellikle Doğu-Batı farklılaşması
Karadeniz boyunca desteklenmektedir. Tüm analizlerde Doğu 4 ve Doğu 5 populasyonlarının
diğer populasyonlardan belirgin olarak farklı olduğu görülmektedir. Bu
farklılaşma populasyonların coğrafik yayılış örüntüleri ile doğrudan
ilişkilidir. Aynı zamanda bu populasyonlar ayrı bir soy hattı oluşturmaktadır. Ayrıca
Batı populasyonları son türemiş populasyonlar olarak görülmektedir.
Kaynakça
- [1] Hewitt GM. Post–glacial re–colonization of European biota. Biological Journal of the Linnean Society, 1999; 68, 87–112.
- [2] Schmitt T. Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in Zoology, 2007; 4, 1.
- [3] Ansell S, Stenøien HK., Grundmann M, et al. The importance of Anatolian mountains as the cradle of global diversity in Arabis alpina, a key arctic–alpine species. Annals of Botany, 2011; 108, 241–252.
- [4] Atkinson RJ, Rokas A, Stone GN. Longitudinal patterns in species richness and genetic diversity in European oaks and oak gallwasps. pp. 127–151, Eds. Weiss S. and Ferrand N., Phylogeography of Southern European Refugia. Springer, Dordrecht, The Netherlands. 2007.
- [5] Çıplak B. Biogeography of Anatolia: the marker group Orthoptera. Memorie della Società Entomologica Italiana, 82, 2004; 357–372.
- [6] Çıplak B. The analogy between interglacial and global warming for the glacial relicts in a refugium, pp. 135–163. Ed. Fattorini S., Insect Ecology and Conservation, Research Signpost. 2008.
- [7] Çıplak B, Kaya S, Gündüz İ. Phylogeography of Anterastes serbicus species group (Orthoptera, Tettigoniidae): phylogroups correlate with mountain belts, but not with the morphospecies. Journal of Orthoptera Research, 2010; 19, 29–40.
- [8] Hewitt GM. Some genetic consequence of ice ages, and their role in diverging and speciation. Biological Journal of the Linnean Society, 1996; 58, 247–276.
- [9] Kaya S, Çıplak B, Gündüz I. Estimating effects of global warming from past range changes for cold demanding refugial taxa: a case study on South-west Anatolian species Poecilimon birandi. Biologia, 67, 2012; 1152–1164.
- [10] Korkmaz EM, Lunt DH, Çıplak B, et al. The contribution of Anatolia to European phylogeography: the centre of origin of the meadow grasshopper, Chorthippus parallelus. Journal of Biogeograph, 2014; 41, 1793–1805.
- [11] Rokas A, Atkinson RJ, Webster LM. Out of Anatolia: longitudinal gradients in genetic diversity support an eastern origin for a circum–Mediterranean oak gallwasp Andricus quercustozae. Molecular Ecology, 2003; 12, 2153–2174.
- [12] Husemann M, Schmitt T, Zachos FE, et al. Palaearctic biogeography revisited: evidence for the existence of a North African refugium for Western Palaearctic biota. Journal of Biogeography, 2014; 41, 81–94.
- [13] Yılmaz Y, Tüysüz O, Yiğitbaş E, et al. Geology and tectonic evolution of the Pontides, pp. 183–226, Ed. Robinson A.G., Regional and Petroleum Geology of the Black Sea and Surrounding Region. AAPG Memoir, Tulsa, 1997.
- [14] Şekercioğlu Ç.H, Anderson S, Akcay E, et al. Turkey’s globally important biodiversity in crisis. Biological Conservation, 2011; 144, 2752–2769.
- [15] Ahmadzadeh F, Flecks M, Rödder D, et al. Multiple dispersal out of Anatolia: biogeography and evolution of oriental green lizards. Biological Journal of the Linnean Society, 2013; 110, 398–408.
- [16] Ambarlı D, Zeydanlı US, Balkız Ö, et al. An overview of biodiversity and conservation status of steppes of the Anatolian biogeographical region. Biodiversity and Conservation, 2016; s10531-016-1172-0,.
- [17] Kryštufek B, Vohralik V, Obuch J. Endemism, vulnerability and conservation issues for small terrestrial mammals from the Balkans and Anatolia. Folia Zoologica, 2009; 58, 291–302.
- [18] Mutun S. Review of oak gall wasps phylogeographic patterns in Turkey suggests a main role of the Anatolian diagonal. Turkish Journal of Forestry, 2016; 17, 1–6.
- [19] Williams PH. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of the British Museum (Natural History) Entomology, 1998; 67, 79–152.
- [20] Kim MJ, Yoon HJ, Im HH, et al. Mitochondrial DNA sequence variation of the bumblebee, Bombus ardens (Hymenoptera: Apidae). Journal of Asia-Pacific Entomology, 2009; 12, 133–139.
- [21] Lecocq T, Gérard M, Michez D, et al. Conservation genetics of European bees: new insights from the continental scale. Conservation Genetics, 2017; 18, 585–596.
- [22] Lopez‑Uribe MM, Soro A, Jha S. Conservation genetics of bees: advances in the application of molecular tools to guide bee pollinator conservation. Conservation Genetics, 2017; 18, 501–506.
- [23] Hines HM. Historical biogeography, divergence times and diversification patterns of Bumble bees (Hymenoptera: Apidae: Bombus). Systematic Biology, 2008; 57, 58–75.
- [24] Lecocq T, Dellicour S, Michez D, et al. Scent of a break-up: phylogeography and reproductive trait divergences in the red-tailed bumblebee (Bombus lapidarius). BioMed Central Evolutionary Biology, 2013; 13, 263.
- [25] Rasmont P, Flagothier D. Biogeographie et choix florauxdes bourdons (Hymenoptera, Apidae) de la Turquie, NATO 8, 1996.
- [26] Özbek H. Doğu Anadolu’nun bazı yörelerindeki Bombinae (Hymoneptera: Apoidae, Bombidae) türleri üzerindeki taksonomik ve bazı biyolojik çalışmalar, Atatürk Üniversitesi Yayınları, No: 621, Atatürk Üniv. Basımevi, Erzurum, pp: 70., 1983.
- [27] Williams PH, Cameron SA, Hines HM, et al. A simplified subgeneric classification of the bumblebees (genus Bombus). Apidologie, 2008; 39, 46–74.
- [28] Pedersen BV. European bumblebees (Hymenoptera: Bombini) – phylogenetic relationships inferred from DNA sequences. Insect Systematics and Evolution, 2002; 33, 1399-560.
- [29] Ewing B, Hillier L, Wendl MC, et al. Department of Molecular Biotechnology, University of Washington, Seattle, Washington 98195-7730, USA., 1998.
- [30] Tamura K, Stecher G, Peterson D, et al. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 2013; 30, 2725–2729.
- [31] Librado P, Rozas J. DnaSP v5.0, A software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 2009; 25, 1451–1452.
- [32] Nei M. Molecular Evolutionary Genetics. Columbia University Press, New York, 1987.
- [33] Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics, 1983; 105, 437–460.
- [34] Excoffier L, Laval G, Schneider S. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online, 2005; 1, 47–50.
- [35] Tajima F. The effect of change in population size on DNA polymorphism. Genetics, 1989; 123, 597–601.
- [36] Fu Y-X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics, 1997; 147, 915–925.
- [37] Dupanloup I, Schneider S, Excoffier L. A simulated annealing approach to define the genetic structure of populations. Molecular Ecology, 2002; 11, 2571–81.
- [38] Weir BS, Cockherham CC. Estimating F–statistics for the analysis of population structure. Evolution, 1984; 38, 1358–1370.
- [39] Peakall R, Smouse PE. GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes, 2006; 6, 288–295.
- [40] Hutchison DW, Templeton AR. Correlation of ikili genetic and geographic distance measures: inferring the relative influences of gene flow and drift on the distribution of genetic variability. Evolution, 1999; 53, 1898–1914.
- [41] Kimura MA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 1980; 16, 111–20.
- [42] Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 1999; 16, 37–48.
- [43] D’Errico I, Gadaleta G, Saccone C. Pseudogenes in Metazoa: origin and features. Briefings in Functional Genomics & Proteomics, 2004; 3, 157–167.
- [44] Lopez JV, Yuhki N, Masuda R, et al. Numt, a recent transfer and tandem amplifications of mitochondrial DNA to the nuclear genome of the domestic cat. Journal of Molecular Evolution, 1994; 39, 174–190.
- [45] Nugent JM, Palmer JD. RNA-mediated transfer of the gene COXII from the mitochondrion to the nucleus during flowering plant evolution. Cell, 1991; 66, 473–481.
- [46] Ermakov OA, Simonov E, Surin VL, et al. Implications of hybridization, NUMTs, and overlooked diversity for DNA barcoding of Eurasian ground squirrels. PLoS One, 2015; 10, e0117201.
- [47] Perez T, Rodríguez F, Fernández M, et al. Ancient mitochondrial pseudogenes reveal hybridization between distant lineages in the evolution of the Rupicapra genus. Gene, 2017; 628, 63–71.
- [48] Du Buy HG, Riley FL. Hybridization between the nuclear and kinetoplast DNA’s of Leishmania enriettii and between nuclear and mitochondrial DNA’s of mouse liver. Proceedings of the National Academy of Sciences USA, 1967; 57, 790–797.
- [49] Bensasson D, Zhang D.X, Hartl D L, et al. Mitochondrial pseudogenes: evolution’s misplaced witnesses. Trends in Ecology & Evolution, 2001; 16, 314–321.
- [50] Richly E, Leister D. NUMTs in sequenced eukaryotic genomes. Molecular Biology and Evolution, 2004; 21, 1081–1084.
- [51] Martins JJr, Solomon SE, Mikheyev AS, et al. Nuclear mitochondrial-like sequences in ants: evidence from Atta cephalotes (Formicidae: Attini). Insect Molecular Biology, 2007; 16, 777–784.
- [52] Gaziev AI, Shaikhaev GO. Nuclear mitochondrial pseudogenes. Molecular Biology, 2010; 44, 358–368.
- [53] Magnacca KN, Brown MJ. Mitochondrial heteroplasmy and DNA barcoding in Hawaiian Hylaeus (Nesoprosopis) bees (Hymenoptera: Colletidae). BMC Evolutionary Biology, 2010; 10, 174.
- [54] Cristiano MP, Fernandes-Salomao TM, Yotoko KSC. Nuclear mitochondrial DNA: an Achilles’ heel of molecular systematics, phylogenetics, and phylogeographic studies of stingless bees. Apidologie, 2012; 43, 527.
- [55] Pamilo P, Viljakainen L, Vihavainen A. Exceptionally high density of NUMTs in the honeybee genome. Molecular Biology and Evolution, 2007; 24, 1340–1346.
- [56] Vijakainen L, Oliveira DC, Werren JH, et al. Transfers of mitochondrial DNA to the nuclear genome in the wasp Nasonia vitripennis. Insect Molecular Biology, 2010; 19, 27–35.
- [57] Ruiz C, William De JM, J. Javier GQ, et al. Presence of nuclear copies of mitochondrial origin (NUMTs) in two related species of stingless bee genus Melipona (Hymenoptera: Meliponini). Journal of Zoological Systematics and Evolutionary Research, 2013; 51, 107–113.
- [58] Ko YJ, Yang EC, Lee JH, et al. Characterization of cetacean Numt and its application into cetacean phylogeny. Genes & Genomics, 2015; 37, 1061–1071.
- [59] Miraldo A, Hewitt GM, Dear PH, et al. Numts help to reconstruct the demographic history of the ocellated lizard (Lacerta lepida) in a secondary contact zone. Molecular Ecology, 2012; 21, 1005–1018.
- [60] Gündüz I, Jaarola M, Tez C. Multigenic and morphometric differentiation of ground squirrels (Spermophilus, Sciuridae, Rodentia) in Turkey. Molecular Phylogenetics and Evolution, 2007; 43, 916–935.
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