Genome size variation in diploid and polyploid mountain lizards of the genus Darevskia (Lacertidae, Squamata)

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

The study of genome size variation in cells of vertebrates using the DNA flow cytometry makes it possible to precisely determine polyploid individuals, which is extremely important when studying the processes of reticulate speciation. In addition, in many groups of vertebrates, closely related species often differ in the nuclear DNA content. Therefore, the purpose of our study was to explore the variability of genome size and ploidy in populations of 29 species and subspecies of mountain lizards of the genus Darevskia, as well as their hybrids. As a result of the study, the range of variability in individuals of different ploidy (91% of diploid and 9% of triploid individuals) was established not to overlap. Among diploid species, no correlation was found between the nuclear DNA content and phylogenetic relationships, geographic coordinates, altitude, average annual temperatures and precipitation. Representatives of all studied species complexes (with the exception of D. adjarica) had approximately the same limits of variability. Two species (D. derjugini and D. saxicola) show significant intraspecific variability. Comparisons of the genome size of parthenogenetic and bisexual species generally revealed no noticeable differences between them. Studies of triploid hybrids have shown that their genome size as a whole roughly corresponds to the sum of the average size of the diploid genome of the maternal parthenogenetic species and the haploid genome of the paternal species. The variability of genome sizes within samples of triploid hybrids was on average slightly higher than in most parthenogenetic species, but some lower than in bisexual species. The paper discusses peculiarities of reticulate speciation in this group of animals.

Texto integral

Acesso é fechado

Sobre autores

S. Litvinchuk

Institute of Cytology, Russian Academy of Sciences; Dagestan State University

Autor responsável pela correspondência
Email: litvinchukspartak@yandex.ru
Rússia, St. Petersburg, 196064; Makhachkala, 367025 Republic of Dagestan

N. Aksyonov

Institute of Cytology, Russian Academy of Sciences

Email: litvinchukspartak@yandex.ru
Rússia, St. Petersburg, 196064

L. Borkin

Zoological Institute, Russian Academy of Sciences

Email: litvinchukspartak@yandex.ru
Rússia, St. Petersburg, 199034

I. Doronin

Zoological Institute, Russian Academy of Sciences

Email: litvinchukspartak@yandex.ru
Rússia, St. Petersburg, 199034

V. Erashkin

Russian State Agrarian University – K. A. Timiryazev Moscow Agricultural Academy

Email: litvinchukspartak@yandex.ru
Rússia, Moscow, 127550

A. Kidov

Russian State Agrarian University – K. A. Timiryazev Moscow Agricultural Academy

Email: litvinchukspartak@yandex.ru
Rússia, Moscow, 127550

Bibliografia

  1. Аззелл Т.М., Даревский И.С., 1974. Доказательства гибридного происхождения партеногенетических видов кавказских скальных ящериц рода Lacerta // Журнал общей биологии. Т. 35. № 4. С. 553–561.
  2. Боркин Л.Я., Даревский И.С., 1980. Сетчатое (гибридогенное) видообразование у позвоночных // Журнал общей биологии. Т. 16. № 4. С. 485–507.
  3. Боркин Л.Я., Литвинчук С.Н., 2013. Гибридизация, видообразование и систематика животных // Труды Зоологического института РАН. Приложение 2. С. 83–139.
  4. Боркин Л.Я., Литвинчук С.Н., 2022. Памяти Юрия Михайловича Розанова (1938–2021) // Современная герпетология. Т. 22. № 3/4. С. 166–182.
  5. Даревский И.С., Даниелян Ф.Д., Розанов Ю.М., Соколова Т.М., 1991. Внутриклональное спаривание и его вероятное эволюционное значение в группе партеногенетических видов скальных ящериц рода Archaeolacerta // Зоологический журнал. Т. 70. № 5. С. 63–74.
  6. Доронин И.В., 2015. Систематика, филогения и распространение скальных ящериц надвидовых комплексов Darevskia (praticola), Darevskia (caucasica) и Darevskia (saxicola). Дис. … канд. биол. наук. ЗИН РАН. 371 с.
  7. Литвинчук С.Н., 2021. Видообразование и гибридизация у амфибий Палеарктики. Дунаев Е.А., Поярков Н.А. (Ред.), Вопросы герпетологии. М.: КМК Scientific Press. С. 170–172.
  8. Литвинчук С.Н., Боркин Л.Я., Скоринов Д.В., Пасынкова Р.А., Розанов Ю.М., 2016. Природная полиплоидия у амфибий // Вестник Санкт-Петербургского государственного университета. Сер. 3. Биология. № 3. С. 77–86.
  9. Литвинчук С.Н., Боркин Л.Я., Мазепа Г.А., Розанов Ю.М., 2018. Размер генома и распространение диплоидных и полиплоидных зелёных жаб рода Bufotes в Узбекистане и Туркменистане // Герпетологические и орнитологические исследования: современные аспекты. Посвящается 100-летию А.К. Рустамова (1917–2005). М.: Товарищество научных изданий КМК. С. 88–101.
  10. Литвинчук С.Н., Скоринов Д.В., Пасынкова Р.А., Кидов А.А., Матушкина К.А., Боркин Л.Я., Розанов Ю.М., 2019. Полиплоидное видообразование у азиатских зеленых жаб рода Bufotes (Bufonidae) // Известия высших учебных заведений. Поволжский регион. Естественные науки. Пенза. № 1 (25). С. 80–93.
  11. Розанов Ю.М., Виноградов А.Е., 1998. Прецизионная ДНК-цитометрия: исследование индивидуальной вариабельности размера генома животных // Цитология. Т. 40. № 8/9. С. 792–799.
  12. Чилингарян А.А., Павлов Е.Ф., 1961. Количественные измерения содержания ДНК в ядрах эритроцитов крови у межвидовых гибридов птиц и рептилий // Доклады академии наук Армянской ССР. Т. 32. № 1. С. 55–60.
  13. Abdala C.S., Baldo D., Juárez R.A., Espinoza R.E., 2016. The first parthenogenetic pleurodont iguanian: a new all-female Liolaemus (Squamata: Liolaemidae) from Western Argentina // Copeia. V. 104. № 2. P. 487–497.
  14. Ahmadzadeh F., Flecks M., Carretero M.A., Mozaffari O., Böhme W., Harris D.J., Freitas S., Rödder D., 2013. Cryptic speciation patterns in Iranian rock lizards uncovered by integrative taxonomy // PLoS ONE. V. 8. № 12. P. e80563.
  15. Arakelyan M., Spangenberg V., Petrosyan V., Ryskov A., Kolomiets O., Galoyan E., 2023. Evolution of parthenogenetic reproduction in Caucasian rock lizards: A review // Current Zoology. V. 69. P. 128–135.
  16. Arribas O.J., 1999. Phylogeny and relationships of the mountain lizards of Europe and Near East (Archaeolacerta Mertens, 1921 sensu lato) and their relationships among the Eurasian lacertid radiation // Russian Journal of Herpetology. V. 6. № 1. P. 1–22.
  17. Bezy R.L., 1972. Karyotypic variation and evolution of the lizards in the family Xantusiidae // Contributions in Science. V. 227. P. 1–29.
  18. Bianchi N.O., Redi C., Garagna C., Capanna E., Manfredi-Romanini M.G., 1983. Evolution of the genome size in Akodon (Rodentia, Cricetidae) // Journal of Molecular Evolution. V. 19. P. 362–370.
  19. Bickham J.W., Hanks B.G., 2009. Diploid-triploid mosaicism and tissue ploidy diversity within Platemys platycephala from Suriname // Cytogenetic and Genome Research. V. 127. P. 280–286.
  20. Bickham J.W., Tucker P.K., Legler J.M., 1985. Diploid-triploid mosaicism: an unusual phenomenon in side-necked turtles (Platemys platycephala) // Science. V. 227. P. 1591–1593.
  21. Biriuk O.V., Shabanov D.A., Korshunov A.V., Borkin L.J., Lada G.A., Pasynkova R.A., Rosanov J.M., Litvinchuk S.N., 2016. Gamete production patterns and mating systems in water frogs of the hybridogenetic Pelophylax esculentus complex in north-eastern Ukraine // Journal of Zoological Systematics and Evolutionary Research. V. 54. № 3. P. 215–225.
  22. Bogart J.P., 1980. Evolutionary implications of polyploidy in amphibians and reptiles. Lewis W.H. (ed.). Polyploidy: Biological Relevance. New York and London: Plenum Press. P. 341–378.
  23. Borkin L.J., Litvinchuk S.N., Rosanov J.M., 1996. Spontaneous triploidy in the crested newt, Triturus cristatus (Salamandridae) // Russian Journal of Herpetology. V. 3. № 2. P. 152–156.
  24. Borkin L.J., Litvinchuk S.N., Rosanov J.M., Milto K.D., 2001. Cryptic speciation in Pelobates fuscus (Anura, Pelobatidae): evidence from DNA flow cytometry // Amphibia-Reptilia. V. 22. № 4. P. 387–396.
  25. Borkin L.J., Korshunov A.V., Lada G.A., Litvinchuk S.N., Rosanov J.M., Shabanov D.A., Zinenko A.I., 2004. Mass occurrence of polyploidy green frogs (Rana esculenta complex) in eastern Ukraine // Russian Journal of Herpetology. V. 11. № 3. P. 194–213.
  26. Canapa A., Biscotti M.A., Barucca M., Carducci F., Carotti E., Olmo E., 2020. Shedding light upon the complex net of genome size, genome composition and environment in chordates // The European Zoological Journal. V. 87. № 1. P. 192–202.
  27. Cole C.J., Taylor H.L., Baumann D.P., Baumann P., 2014. “Neaves’ whiptail lizard: the first known tetraploid parthenogenetic tetrapod (Reptilia: Squamata: Teiidae) // Breviora. V. 539. P. 1–19.
  28. Cole C.J., Taylor H.L., Neaves W.B., Baumann D.P., Newton A., Schnittker R., Baumann P., 2017. The second known tetraploid species of parthenogenetic tetrapod (Reptilia: Squamata: Teiidae): description, reproduction, comparisons with ancestral taxa, and origins of multiple clones // Bulletin of the Museum of Comparative Zoology. V. 161. № 8. P. 285–321.
  29. Danielyan F., Arakelyan M., Stepanyan I., 2008. Hybrids of Darevskia valentini, D. armeniaca and D. unisexualis from a sympatric population in Armenia // Amphibia-Reptilia. V. 29. P. 487–504.
  30. Dar T.-Ul.-H., Rehman R.-Ul. (eds.), 2017. Polyploidy: Recent Trends and Future Perspectives. Springer.
  31. Darevsky I.S., Danielyan F.D., 1968. Diploid and triploid progeny arising from natural mating of parthenogenetic Lacerta armeniaca and L. unisexualis with bisexual L. saxicola valentini // Journal of Herpetology. V. 2. № 3–4. P. 65– 69.
  32. Darevsky I.S., Kupriyanova L.A., 1982. Rare males in parthenogenetic lizard Lacerta armeniaca Méhely // Vertebrata Hungarica. V. 21. P. 69–75.
  33. Darevsky I.S., Kupriyanova L.A., Bakradze M.A., 1978. Occasional males and intersexes in parthenogenetic species of Caucasian Rock Lizards (genus Lacerta) // Copeia. № 2. P. 201–207.
  34. Darevsky I.S., Kupriyanova L.A., Uzzell T., 1985. Parthenogenesis in reptiles. Gans C., Billet F. (eds). Biology of Reptiles. V. 15. New York: Wiley J. and Sons. P. 411–526.
  35. Darevsky I.S., Danielyan F.D., Sokolova T.M., Rozanov Y.M., 1989. Intraclonal mating in the parthenogenetic lizard species Lacerta unisexualis. Dawley R.M., Bogart J.P. (eds). Evolution and Ecology of Unisexual Vertebrates. Bulletin of the NY State Museum, New York. P. 228–235.
  36. Disсhe Z., 1931. Nachweis und Bestimmung der Thymonukleinsaure. Abderhalden E., Handbuch der biologischen Arbeitsmethoden. Wien. Abt. 5. T. 2. Hf. 16. P. 18–29.
  37. Dolezel J., Bartos J., Voglmayr H., Greilhuber J., 2003. Nuclear DNA content and genome size of trout and human // Cytometry A.V. 51. № 2. P. 127–128.
  38. Dufresnes C., Mazepa G., Jablonski D., Oliveira R.C., Wenseleers T., Shabanov D.A., Auer M., Ernst R., Koch C., Ramírez-Chaves H.E. Mulder K.P., Simonov E., Tiutenko A., Kryvokhyzha D., Wennekes P.L., Zinenko O.I., Korshunov O.V., Al-Johany A.M., Peregontsev E.A., Masroor R., Betto-Colliard C., Denoël M., Borkin L.J., Skorinov D.V., Pasynkova R.A., Mazanaeva L.F., Rosanov J.M., Dubey S., Litvinchuk S., 2019. Fifteen shades of green: The evolution of Bufotes toads revisited // Molecular Phylogenetics and Evolution. V. 141. P. 106615.
  39. Dufresnes C., Strachinis I., Suriadna N., Mykytynets G., Cogălniceanu D., Székely P., Vukov T., Arntzen J.W., Wielstra B., Lymberakis P., Geffen E., Gafny S., Kumlutaş Y., Ilgaz Ç., Candan K., Mizsei E., Szabolcs M., Kolenda K., Smirnov N., Géniez P., Lukanov S., Crochet P.‐A., Sylvain D., Perrin N., Litvinchuk S.N., Denoël M., 2019а. Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads (Pelobates) // Molecular Ecology. V. 28. № 13. P. 3257– 3270.
  40. Dufresnes C., Brelsford A., Jeffries D.L., Mazepa G., Suchan T., Canestrelli D., Nicieza A., Fumagalli L., Dubey S., Martínez-Solano I., Litvinchuk S.N., Vences M., Perrin N., Crochet P.-A. 2021. Mass of genes rather than master genes underlie the genomic architecture of amphibian speciation // Proceedings of the National Academy of Sciences USA. V. 118. № 36. P. e2103963118.
  41. Feulgen R., Rossenbeck H., 1924. Mikroskopisch-chemischer Nachweis einer Nukleinsäure vom Typus der Thymonukleinsäure und die darauf beruhende elektive Färbung von Zellkernen in mikroskopischen Präparaten // Hoppe-Seyler’s Zeitschrift für Physiologische Chemie. V. 135. P. 203–248.
  42. Fick S.E., Hijmans R.J., 2017. WorldClim 2: new 1km spatial resolution climate surfaces for global land areas // International Journal of Climatology. V. 37. № 12. P. 4302–4315.
  43. Freitas S., Rocha S., Campos J., Ahmadzadeh F., Corti C., Sillero N., Ilgaz Ç., Kumlutaş Y., Arakelyan M., Harris D.J., Carretero M.A., 2016. Parthenogenesis through the ice ages: a biogeographic analysis of Caucasian rock lizards (genus Darevskia) // Molecular Phylogenetics and Evolution. V. 102. P. 117–127.
  44. Freitas S.N., Harris D.J., Sillero N., Arakelyan M., Butlin R.K., Carretero M.A., 2019. The role of hybridisation in the origin and evolutionary persistence of vertebrate parthenogens: a case study of Darevskia lizards // Heredity. V. 123. P. 795–808.
  45. Girnyk A.E., Vergun A.A., Semyenova S.K., Guliaev A.S., Arakelyan M.S., Danielyan F.D., Martirosyan I.A., Murphy R.W., Ryskov A.P., 2018. Multiple interspecific hybridization and microsatellite mutations provide clonal diversity in the parthenogenetic rock lizard Darevskia armeniaca // BMC Genomics. V. 19. № 1. P. 979.
  46. Gregory T.R., Nathwani P., Bonnett T.R., Huber D.P.W., 2013. Sizing up arthropod genomes: an evaluation of the impact of environmental variation on genome size estimates by flow cytometry and the use of qPCR as a method of estimation // Genome. V. 56. № 9. P. 505–510.
  47. Hardy L.M., Cole C.J., 1998. Morphology of a sterile, tetraploid, hybrid whiptail lizard (Squamata: Teiidae: Cnemidophorus) // American Museum Novitates. V. 3228. P. 1–16.
  48. Kearney M., Fujita M.K., Ridenour J., 2009. Lost sex in the reptiles: Constraints and correlations. I. Schön I., Martens K., Dijk P. (eds). Lost Sex. Springer. P. 447–474.
  49. Lamborot M.M., Manzur E., Alvarez-Sarret E., 2006. Triploidy and mosaicism in Liolaemus chiliensis (Sauria: Tropiduridae) // Genome. V. 49. P. 445–453.
  50. Litvinchuk S.N., 2018. Testicular anomalies in the hybridogenetic frog Pelophylax esculentus (Amphibia: Anura: Ranidae). Vershinin V.L., Vershinina S.D. (eds). The Second International Conference “Amphibians and Reptiles Anomalies and Pathology: Methodology, Evolutionary Significance, Monitoring and Enveronmental Helth”. KnE Life Science. P. 92–96.
  51. Litvinchuk S.N., Kazakov V.I., Pasynkova R.A., Borkin L.J., Kuranova V.N., Rosanov J.M., 2010. Tetraploid green toad species (Bufo pewzowi) from the Altay Mountains: The first record for Russia // Russian Journal of Herpetology. V. 17. № 4. P. 290–298.
  52. Litvinchuk S.N., Rosanov J.M., Borkin L.J., 2007. Correlations of geographic distribution and temperature of embryonic development with the nuclear DNA content in the Salamandridae (Urodela, Amphibia) // Genome. V. 50. № 4. P. 333–342.
  53. Lutes A.A., Baumann D.P., Neaves W.B., Baumann P., 2011. Laboratory synthesis of an independently reproducing vertebrate species // Proceedings of the National Academy of Sciences USA. V. 108. № 24. P. 9910–9915.
  54. Mason A.S., Pires J.C., 2015. Unreduced gametes: meiotic mishap or evolutionary mechanism? // Trends in Genetics. V. 31. № 1. P. 5–10.
  55. Moritz C., Uzzell T., Spolsky C., Hotz H., Darevsky I.S., Kupriyanova L.A., Danielyan F.D., 1992. The maternal ancestry and approximate age of parthenogenetic species of Caucasian rock lizards (Lacerta: Lacertidae) // Genetica. V. 87. № 1. P. 53–62.
  56. Muller H.J., 1932. Some genetic aspects of sex // American Naturalist. V. 66. № 703. P. 118–138.
  57. Murphy R.W., Fu J., Macculloch R.D., Darevsky I.S., Kupriyanova L.A., 2000. A fine line between sex and unisexuality: the phylogenetic constraints on parthenogenesis in lacertid lizards // Zoological Journal of Linnean Society. V. 130. P. 527–549.
  58. Ochkalova S., Korchagin V., Vergun A., Urin A., Zilov D., Ryakhovsky S., Girnyk A., Martirosyan I., Zhernakova D.V., Arakelyan M., Danielyan F., Kliver S., Brukhin V., Komissarov A., Ryskov A., 2022. First genome of rock lizard Darevskia valentini involved in formation of several parthenogenetic species // Genes. V. 13. P. 1569.
  59. Pensabene E., Augstenová B., Kratochvíl L., Rovatsos M., 2024. Differentiated sex chromosomes, karyotype evolution, and spontaneous triploidy in carphodactylid geckos // Journal of Heredity. V. 115. № 3. P. 262– 276.
  60. Stöck M., Dedukh D., Reifová R., Lamatsch D.K., Starostová Z., Janko K., 2021. Sex chromosomes in meiotic, hemiclonal, clonal and polyploid hybrid vertebrates: along the ‘extended speciation continuum’ // Philosophical Transactions of the Royal Society B.V. 376. P. 20200103.
  61. Tarkhnishvili D., Gabelaia M., Adriaens D., 2020. Phenotypic divergence, convergence and evolution of Caucasian rock lizards (Darevskia) // Biological Journal of the Linnean Society. V. 130. P. 142–155.
  62. Trifonov V.A., Paoletti A., Caputo Barucchi V., Kalinina T., O’Brien P.C.M., Ferguson-Smith M.A., Giovannotti M., 2015. Comparative chromosome painting and NOR distribution suggest a complex hybrid origin of triploid Lepidodactylus lugubris (Gekkonidae) // PLoS ONE. V. 10. № 7. P. e0132380.
  63. Uzzell T., Darevsky I.S., 1975. Biochemical evidence for the hybrid origin of the parthenogenetic species of the Lacerta saxicola complex (Sauria: Lacertidae), with a discussion of some ecological and evolutionary implications // Copeia. № 2. P. 204–222.
  64. Uetz P. (ed.), 2024. The Reptile Database. http://www.reptile-database.org. Accessed February 28, 2024.
  65. Yanchukov A., Tarkhnishvili D., Erdolu M., Şahin M.K., Candan K., Murtskhvaladze M., Gabelaia M., Iankoshvili G., Barateli N., Ilgaz Ç., Kumlutaş Y., Matur F., Çolak F., Arakelyan M., Galoyan E., 2022. Precise paternal ancestry of hybrid unisexual ZW lizards (genus Darevskia: Lacertidae: Squamata) revealed by Z-linked genomic markers // Biological Journal of the Linnean Society. V. 136. P. 293–305.

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
2. Fig. 1. Map of rock lizard collection sites of the genus Darevskia. The insert in the upper right corner (A) covers the territory of northern Armenia. In the lower right corner is a photograph of D. lindholmi from Cape Fiolent (Sevastopol).

Baixar (466KB)
3. Fig. 2. Variability (violin plots) of the amount of nuclear DNA in different species, subspecies and interspecific hybrids of rock lizards of the genus Darevskia.

Baixar (306KB)

Declaração de direitos autorais © Russian Academy of Sciences, 2024