Nuclear Cytoplasmic Conflict in Hybrids of Roach Rutilus rutilus and Bream Abramis brama as a Consequence of the Divergence Species in Body and Genome Sizes

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Abstract

Species divergence in body size is often associated with changes in genome size and the rate of evolution of mitochondrial DNA (mtDNA), which can lead to problems of nuclear-cytoplasmic compatibility and embryonic genome activation and reduce the fitness of hybrids. The bream Abramis brama (L.) is larger than the roach Rutilus rutilus (L.) in body and genome sizes. In the first generation of hybrids according to the ITS1 region of ribosomal DNA, a change in the donor genome of male to the level of the maternal species was previously established, which can affect the inheritance of traits from the male and, in particular, body size. Body length and height, a complex of diagnostic morphological characters, and genotyping (ITS1 rDNA and cyt b mtDNA) of underyearlings and mature individuals of bream, roach, F1 hybrids and underyearlings of backcrosses (Fb) were analyzed. Sexually mature hybrids of both directions of crossing are close in body length to R. rutilus, which indicates a violation of the paternal effect when inheriting the body length of a larger of species. Violation of the inheritance of bream body length in hybrids of cross R. rutilus × A. brama (♀ <♂, RA) is considered as a developmental deviation, which, obviously, can affect the adaptation of hybrids and determines the rarity of this variant in nature. At the same time, alloplasmic ARR backcrosses restore the body length of the bream even in the presence of the roach nuclear genome, which indicates the influence of mitochondrial genes on the development of this trait. The observed decrease in the fitness of first-generation hybrids with roach mtDNA may be associated with to an insufficient level of transcription of ribosomal genes due to a decrease in the number and variability of copies of the donor bream rDNA. Moreover, the high level of changes of mtDNA roach indicate a suboptimal mitochondrial-nuclear correspondence of respiratory a complexes in hybrids RA, which negatively affects key physiological processes, including growth and development of a large body size. Presumably, the development of large body size, as a complex trait with high aerobic fitness, is blocked in RA hybrids for energy reasons. The paper shows that differences families of repeated sequences rDNA and mtDNA in terms of the number and variability of copies in genome of R. rutilus and A. brama can lead to regulatory nuclear-cytoplasmic incompatibility of genomes and affect the fitness of hybrids already in the first generation.

About the authors

V. V. Stolbunova

Papanin Institute for Biology of Inland Waters Russian Academy of Sciences

Author for correspondence.
Email: vvsto@mail.ru
Russia, Nekouzskii raion, Yaroslavl oblast, Borok

Yu. V. Kodukhova

Papanin Institute for Biology of Inland Waters Russian Academy of Sciences

Email: vvsto@mail.ru
Russia, Nekouzskii raion, Yaroslavl oblast, Borok

References

  1. Атлас пресноводных рыб России. 2003. Москва: Наука.
  2. Беннетт M.Д. 1986. Нуклеотипическая основа пространственной упорядоченности хромосом эукариот и ее значение для эволюции генома и фенотипической изменчивости // Эволюция генома. Москва: Мир. С. 234.
  3. Бердников В.А. 1991. Эволюция и прогресс. Новосибирск: Наука.
  4. Геодакян В.А. 2012. Два пола. Зачем и почему? Эволюционная теория пола. Москва: эл. издание. ISBN: 978-0-9856620-0-4
  5. Гинатулин А.А. 1984. Структура, организация и эволюция генома позвоночных. Москва: Наука.
  6. Голубовский М.Д. 2000. Век генетики: эволюция идей и понятий. Санкт-Петербург: Борей Арт.
  7. Кирпичников В.С. 1987. Генетика и селекция рыб. Ленинград: Наука.
  8. Кодухова Ю.В. 2008. Морфологические и экологические особенности гибридов первого поколения леща Abramis brama L. и плотвы Rutilus rutilus L. (Cyprinidae): Автореф. дис…. канд. биол. наук. Борок: Ин-т биологии внутр. вод РАН.
  9. Кодухова Ю.В. 2010. Морфологическая характеристика потомства от гибридов первого поколения леща (Abramis brama L.) и плотвы (Rutilus rutilus L.) при бэккросссировании. Матер. IV шк.-конф. молодых ученых. Борок. С. 56.
  10. Крыжановский С.Г. 1968. Закономерности развития гибридов рыб различных систематических категорий. Москва: Наука.
  11. Лапушкина Е.Е. 2002. Эколого-генетический анализ раннего развития отдаленных гибридов F1 леща (Abramis brama L.), плотвы (Rutilus rutilus L.) и синца (Abramis ballerus L.): Дис. … канд. биол. наук. Борок: Ин-т биологии внутр. вод РАН.
  12. Луданный Р.И. 2008. Генетическая идентификация и дифференциация представителей семейства Карповых (Cyprinidae): Автореф. дис. … канд. биол. наук. Москва: Ин-т биологии гена РАН.
  13. Максимовский Л.Ф. 1988. Возможности направленного воздействия на формирование соотношения полов потомства млекопитающих // Сельскохозяйственная биология. Т. 1. С. 10.
  14. Озернюк Н.Д. 1985. Энергетический обмен в раннем онтогенезе рыб. Москва: Наука.
  15. Патрушев Л.И. 2004. Искусственные генетические системы. Т. 1. Москва: Наука.
  16. Правдин И.Ф. 1966. Руководство по изучению рыб (преимущественно пресноводных). Москва: Пищ. пром-сть.
  17. Рис Г., Дженкинс Д., Сил А.Д. и др. 1986. О фенотипических эффектах изменений количества ДНК // Эволюция генома. Москва: Мир. С. 281.
  18. Рябов И.Н. 1981. Методы гибридизации рыб на примере семейства карповых // Исследование размножения и развития рыб. Москва: Наука. С. 195.
  19. Слынько Е.Е., Слынько Ю.В. 2010. Жизнеспособность гибридов первого поколения плотвы (Rutilus rutilus L.), леща (Abramis brama L.) и синца (Abramis ballerus L.) на ранних стадиях развития // Биология внутр. вод. № 2. С. 57.
  20. Столбунова В.В. 2017. Межгеномный конфликт при отдаленной гибридизации плотвы (Rutilus rutilus L.) и леща (Abramis brama L.) // Успехи соврем. биологии. Т. 137. № 4. С. 361. https://doi.org/10.7868/S0042132417040044
  21. Столбунова В.В., Кодухова Ю.В. 2021. Наследование ITS1 рДНК у реципрокных гибридов плотвы Rutilus rutilus (L.) и леща Abramis brama (L.) в раннем онтогенезе // Успехи соврем. биологии. Т. 141. № 1. С. 66. https://doi.org/10.31857/S0042132421010233
  22. Формозов Н.А. 2007. Интрогресcия чужеродных митотипов как следствие гипотезы “передового края” Годфрея Хьюитта: влияние гетерогаметности самцов или самок и соотношения полов в расселяющих популяциях: Матер. конф. “Современные проблемы биологической эволюции”, к 100-летию Государственного Дарвинского музея. Москва, 17–20 сентября 2007. Москва: ГДМ. С. 155.
  23. Честков И.В. 2018. Исследование вариабельности числа копий рРНК-кодирующих генов и митохондриальной ДНК в геноме пациентов с шизофренией: Автореф. дис. … канд. биол. наук. Москва: Мед.-генетич. науч. центр.
  24. Allard M.W., Honeycutt R.L. 1991. Ribosomal DNA Variation Within and Between Species of Rodents, with Emphasis on the Genus Onychomys // Mol. Biol. Evol. V. 8. № 1. P. 71. https://doi.org/10.1093/oxfordjournals.molbev.a040637
  25. Baerwald M., May B. 2004. Characterization of microsatellite loci for five members of the minnow family Cyprinidae found in the Sacramento-San Joaquin Delta and its tributaries // Mol. Ecol. Notes. № 4. P. 385.
  26. Bateson W. 1909. Heredity and variation in modern lights // Danvin and Modmz Science. Cambridge: Cambridge Univ. Press. P. 85.
  27. Bianco P.G., Aprea G., Balletto E. et al. 2004. The karyology of the cyprinid genera Scardinius and Rutilus in southern Europe // Ichthyol. Res. V. 51. P. 274.
  28. Blankenhorn W.U. 2000. The evolution of body size: What keeps organisms small? // Q. Rev. Biol. V. 75. P. 385.
  29. Bolnick D.I., Near T.J., Wainwright P.C. 2006. Body size divergence promotes post-zygotic reproductive isolation in centrarchids // Evol. Ecol. Res. V. 8. P. 903.
  30. Bolnick D.I., Turelli M., López-Fernández H. et al. 2008. Accelerated Mitochondrial Evolution and “Darwin’s Corollary”: Asymmetric Viability of Reciprocal F1 Hybrids in Centrarchid Fishes // Genetics. V. 178. № 2. P. 1037. https://doi.org/10.1534
  31. Boughman J.W. 2001. Divergent sexual selection enhances reproductive isolation in sticklebacks // Nature. V. 411. P. 944. https://doi.org/10.1038/35082064
  32. Burke J.M., Arnold M.L. 2001. Genetics and the fitness of hybrids // Annu. Rev. Genet. V. 35. P. 31. https://doi.org/10.1146/annurev.genet.35.102401.085719
  33. Coelho P.S.R., Bryan A.C., Kumar A. et al. 2002. A novel mitochondrial protein, Tar1p, is encoded on the antisense strand of the nuclear 25S rDNA // Genes & Development. V. 16. P. 2755. https://doi.org/10.1101/gad.1035002
  34. Chan Kai M.A., Levin S.A. 2005. Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA // Evolution. V. 59. № 4. P. 720. https://www.jstor.org/stable/3449021
  35. Dobzhansky T. 1937. Studies on Hybrid Sterility. I. Spermatogenesis in pure and hybrid Drosophila pseudoobscura // Zeitschrift für Zellforschung und mikroskopische Anatomie. V. 21. № 2. P. 169. https://doi.org/10.1007/bf00374056
  36. Dowling T.E., DeMarais B.D. 1993. Evolutionary significance of introgressive hybridization in cyprinid fishes // Nature. V. 362. P. 444.
  37. Economidis P.S., Wheeler A. 1989. Hybrids of Abramis brama with Scardinius erythrophthalmus and Rutilus rutilus from Lake Volvi, Macedonia, Greece // J. Fish Biol. V. 35. № 2. P. 295. https://doi.org/10.1111/j.1095-8649.1989.tb02978.x
  38. Flavell R.B. 1982. Sequence amplification, deletion and rearrangement: major sources of variation during species divergence // Genome Evolution. L.: Acad. Press. P. 301.
  39. Ellison Ch.K., Burton R.S. 2006. Disruption of mitochondrial function in interpopulation hybrids of Tigriopus californicus // Evolution. V. 60. № 7. P. 1382.
  40. Fujii S., Toriyama K. 2008. Genome barriers between nuclei and mitochondria exemplified by cytoplasmic male sterility // Plant and Cell Physiology. V. 49. № 10. P. 1484. https://doi.org/10.1093/pcp/pcn102
  41. Fujiwara A., Abe S., Yamaha E. et al. 1997. Uniparental chromosome elimination in the early embryogenesis of the inviable salmonid hybrids between masu salmon female and rainbow trout male // Chromosoma. V. 106. P. 44.
  42. Gangloff S., Zou H., Rothstein R. 1996. Gene conversion plays the major role in controlling the stability of large tandem repeats in yeast // EMBO J. V. 15. P. 1715.
  43. Gibbons J.G., Branco A.T., Yu S., Lemos B. 2014. Ribosomal DNA copy number is coupled with gene expression variation and mitochondrial abundance in humans // Nat. Commun. V. 5. P. 4850. https://doi.org/10.1038/ncomms5850
  44. Gill B.S. 1991. Nucleocytoplasmic interactions (NCI) hypothesis of genome evolution and speciation in polyploid plants // Proceedings of the Kihara Memorial International Symposium on cytoplasmis engineering in wheat. Japan: Yokohama. P. 48.
  45. Gregory T.R. 2013. Animal genome size database. https://www.genomesize.com
  46. Hayden B., Pulcini D., Kelly-Quinn M. et al. 2010. Hybridisation between two cyprinid fishes in a novel habitat: genetics, morphology and life-history traits // Evol. Biol. V. 10. P. 169.
  47. Hayden B., Coscia I., Mariani S. 2011. Low cytochrome b variation in bream Abramis brama // J. Fish Biol. V. 78. P. 1579. https://doi.org/10.1111/j.1095-8649.2011.02941.x
  48. Hill G.E., Johnson J.D. 2013. The mitonuclear compatibility hypothesis of sexual selection // Proc. Biol. Sci. 2013280:20131314. https://doi.org/10.1098/rspb.2013.1314
  49. Hinegardner R. 1968. Evolution of Cellular DNA Content in Teleost Fishes // The American Naturalist. V. 102. № 928. P. 517. https://doi.org/10.1086/282564
  50. Hubbs C.L., Kuronuma K. 1942. Hybridization in nature between two genera of flounders in Japan // Papers Michigan Acad. Sci., Arts and Letters. V. 27. P. 267.
  51. Kopiejewska W., Terlecki J., Chybowski L. 2003. Varied somatic growth and sex cell development in reciprocal hybrids of roach Rutilus rutilus (L.) and ide Leuciscus idus (L.) // Arch. Polish Fisheries. V. 11. № 1. P. 33. https://doi.org/10.3750/AIP2004.34.1.05
  52. Konopinski M.K., Amirowicz A. 2018. Genetic composition of a population of natural common bream Abramis brama × roach Rutilus rutilus hybrids and their morphological characteristics in comparison with parent species // J. Fish Biol. V. 92. № 2. P. 365. https://doi.org/10.1111/jfb.13506
  53. Koonin E.V., Wolf Y.I. 2006. Evolutionary Systems Biology: Links Between Gene Evolution and Function // Curr. Opin. Biotechnol. V. 17. P. 481.
  54. Lane N. 2011. Mitonuclear match: optimizing fitness and fertility over generations drives ageing within generations // Bioessays. V. 33. P. 860. https://doi.org/10.1002/bies.201100051
  55. Lane N., Martin W. 2010. The energetics of genome complexity // Nature. V. 467. P. 929.
  56. Larson D.E., Zahradka P., Sells B.H. 1991. Control points in eucaryotic ribosome biogenesis // Biochem. Cell. Biol. V. 69. P. 5. https://doi.org/10.1139/o91-002
  57. López G.J., Chiaraviglio M., Cardozo G. 2018. Macroevolution of sexual size dimorphism and reproduction-related phenotypic traits in lizards of the Chaco Domain // Evol. Biology. V. 18. P. 186. https://doi.org/10.1186/s12862-018-1299-6
  58. Marckmann K. 1954. Is there any correlation between metabolism, and number of vertebrae (and other meristic characters) in the sea trout (Salmo trutta trutta L.) // Medd. Dan. fisk.-og havUnders. V. 1. № 3. P. 1.
  59. Matondo B.N., Ovidio M., Poncin P. et al. 2008. Morphological recognition of artificial F1 hybrids between three common European cyprinid species: Rutilus rutilus, Blicca bjoerkna and Abramis brama // Acta Zool. Sin. V. 54. № 1. P. 144.
  60. Mayr E. 1963. Animal species and evolution. Cambridge, MA: Harvard Univ. Press.
  61. McKinnon J.S., Mori S., Blackman B.K. et al. Evidence for ecology’s role in speciation // Nature. 2004. V. 429. P. 294. https://doi.org/10.1038/nature02556
  62. McLain D.K. 1993. Cope’s rules, sexual selection, and the loss of ecological plasticity // Oikos. V. 68. P. 490. https://doi.org/10.2307/3544917
  63. Olmo E. 2003. Reptiles: a group of transition in the evolution of genome size and of the nucleotypic effect // Cytogenet Genome Res. V. 101. P. 166. https://doi.org/10.1159/000074174
  64. Orr H.A., Turelli M. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities // Evolution. V. 55. P. 10854. https://doi.org/10.1111/j.0014-3820.2001.tb00628.x
  65. Muller H.J. 1942. Isolating mechanisms, evolution and temperature // Biol. Symp. V. 6. P. 71.
  66. Pierce B.A., Mitton J.B. 1980. The relationship between genome size and genetic variation // Am. Nat. V. 116. P. 850.
  67. Prokopowich C.D., Gregory T.R., Crease T.J. 2003. The correlation between rDNA copy number and genome size in eukaryotes // Genome. V. 46. P. 48.
  68. Purdom C.E. 1979. Genetics of growth and reproduction in teleosts. Fish phenology: anabolic adaptiveness in teleosts. London; New York: Acad. Press. P. 207.
  69. Rand D.M., Haney R.A., Fry A.J. 2004. Cytonuclear coevolution: the genomics of cooperation // Trends Ecol. Evol. V. 19. P. 645. https://doi.org/10.1016/j.tree.2004.10.003
  70. Reeder R.H. 1985. Mechanisms of nucleolar dominance in animals and plants // J. Cell Biol. V. 101. P. 2013.
  71. Rensch B. 1959. Evolution above the species level. New York: Columbia Univ. Press.
  72. Richard G.F., Kerrest A., Dujon B. 2008. Comparative genomics and molecular dynamics of DNA repeats in eukaryotes // Microbiol. Mol. Biol. Rev. V. 72. № 4. P. 686. https://doi.org/10.1128/MMBR.00011-08
  73. Rocher C., Taanman J.-W., Pierron D. et al. 2008. Influence of mitochondrial DNA level on cellular energy metabolism: implications for mitochondrial diseases // J. Bioenerg. Biomembr. V. 40. P. 59.
  74. Schrader M., Fuller R.C., Travis J. 2013. Differences in offspring size predict the direction of isolation asymmetry between populations of a placental fish // Biology Letters. V. 9. № 55. P. 20130327. https://doi.org/10.1098/rsbl.2013.0327
  75. Shipley J.R., Campbell P., Searle J.B., Pasch B. 2016. Asymmetric energetic costs in reciprocal-cross hybrids between carnivorous mice (Onychomys) // J. Exp. Biology. V. 219. P. 3803. https://doi.org/10.1242/jeb.148890
  76. Skaliská K., Lim K.Y., Matyásek R. et al. 2003. Rapid evolution of parental rDNA in a synthetic tobacco allotetraploid line // Am. J. Bot. V. 90. № 7. P. 988. https://doi.org/10.3732/ajb.90.7.988
  77. Stolbunova V.V., Pavlova V.V., Kodukhova Y.V. 2020. Asymmetric hybridization of roach Rutilus rutilus L. and common bream Abramis brama L. in controlled backcrosses: Genetic and morphological patterns // Biosyst. Divers. V. 28. № 4. P. 35. https://doi.org/10.15421/012048
  78. Vinogradov A. E., Anatskaya O.V. 2006. Genome size and metabolic intensity in tetrapods: a tale of two lines // Proc. R. Soc. B. V. 273. P. 27. https://doi.org/10.1098/rspb.2005.3266
  79. Wilson A.C., Maxson L.R., Sarish V.M. 1974. Two types of molecular evolution evidence from studies of interspecific hybridization // Proc. Nat. Acad. Sci. USA. V. 71. № 7. P. 2843. https://doi.org/10.1073/pnas.71.7.2843
  80. Wirtz P. 1999. Mother species-father species: unidirectional hybridization in animals with female choice // Anim. Behav. V. 58. № 1. P. 1. https://doi.org/10.1006/anbe.1999.1144
  81. Wyatt P.M.W., Pitts C.S., Butlin R.K. 2006. A molecular approach to detect hybridization between bream Abramis brama, roach Rutilus rutilus and rudd Scardinius erythrophthalmus // J. Fish Biol. V. 69. P. 52. https://doi.org/10.1111/j.1095-8649.2006.01104.x

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