Breeding success of the interspecies hybrids: Reduced fertility in the hybridogeneous magpie population (Pica pica × Pica serica, Aves)

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Abstract

Data on the breeding success of hybrids, collected during direct field observations, are principally important for understanding nature of the species isolating factors and future fate of the hybridogeneous populations. In the zone of secondary contact between Eurasian magpie Pica pica and Oriental magpie Pica serica, emerging right now, limited hybridization occurs, what has been shown in our reported data on nuclear single nucleotide polymorphisms (SNP). In the present work, we have analyzed composition of 119 nesting pairs and content of 89 nests in the hybridogeneous population of P. pica leucoptera × P. serica jankowskii in Eastern Mongolia, then in the recent contact zone in Eastern Transbaikalia (South Siberia) and the relatively pure populations of P. p. leucoptera in Central Transbaikalia and P. s. jankowskii in Northeast China. In the hybridogeneous population of Mongolia, significantly increased portion of nonviable clutches with all dead eggs was recorded, as well as a portion of partly dead clutches, compared with the data on the pure population of Central Transbaikalia. The egg mortality was found to be much less dramatic in the population of the Eastern Transbaikalia, where hybridization is less pronounced than in Mongolia. Several possible mechanisms of genetic incompatibilities breaking the reproductive barriers are discussed. The future fate of this magpie contact zone is considered, taking in account selection against hybridization which was revealed in this study. Among possible scenarios, reinforcement of prezygotic isolation may occur, i. e., in the species-specific calls. It is possible that a kind of mosaic hybrid zone with some features of tension zone will appear. Monitoring of the unique situation with the emerging zone of contact and hybridization of two young magpie species is needed, as a necessary addition to genomic studies.

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A. P. Kryukov

Federal Scientific Center of the East Asia Terrestrial Biodiversity, RAS

Author for correspondence.
Email: alex.p.kryukov@gmail.com
Russian Federation, 690022, Vladivostok, Stoletiya Ave., 159

O. A. Goroshko

Daursky State Nature Biosphere Reserve; Chita Institute of Nature Resources, Ecology and Cryology, Siberian Branch of RAS

Email: oleggoroshko@mail.ru
Russian Federation, 674480, Zabaikalsky Krai, Nizhny Tsasuchey Settl., Komsomol’skaya St., 76; 672014, Chita, Nedorezov St., 16A

References

  1. Горошко О.А., 2018. Экспансия сороки Pica pica (Linnaeus, 1758) в Забайкалье и Амурской области // Современные проблемы орнитологии Сибири и Центральной Азии: Мат-лы 6-й Междунар. орнитол. конф. Иркутск: ИНЦХТ. С. 62–64.
  2. Горошко О.А., Крюков А.П., Лю Сонтао, Доу Хуашань, Базыр-оол Б.К., 2018. О распространении, подвидовой принадлежности и таксономическом статусе сорок (Pica pica) в бассейне реки Хайлар-Аргунь (северо-восточный Китай и Забайкалье, Россия) // Байкальский зоол. журн. № 2 (23). С. 38–45.
  3. Майр Э., 1968. Зоологический вид и эволюция. М.: Мир. 597 с.
  4. Рубцов А.С., 2021. Состав пар, биотопические предпочтения и относительная продолжительность жизни птиц в гибридной популяции обыкновенной (Emberiza citrinella) и белошапочной (Emberiza leucocephalos) овсянок (Passeriformes, Emberizidae) на Алтае // Зоол. журн. Т. 100. № 11. С. 1276–1287. https://doi.org/10.31857/S0044513421090075
  5. Рустамов А.К., 1954. Семейство вороновые // Птицы Советского Союза. Т. 5 / Под ред. Дементьева Г.П., Гладкова Н.А. М.: Советская наука. С. 13–105.
  6. Соколов В.Е., Васильева Н.Ю., 1993. Гибридологический анализ подтверждает видовую самостоятельность Phodopus sungorus (Pallas, 1773) и Phodopus campbelli (Thomas, 1905) // ДАН. Т. 332. № 1. С. 120–123.
  7. Штегман Б.К., 1932. Вороновые птицы. Птицы СССР. Определители по фауне СССР, издаваемые Зоол. ин-том АН. Т. 6. Л.: Изд-во АН СССР. 32 с.
  8. Abbott R., Albach D., Ansell S., Arntzen J.W., Baird S.J.E., et al., 2013. Hybridization and speciation // J. Evol. Biol. V. 26. № 2. P. 229–246. https://doi.org/10.1111/j.1420-9101.2012.02599.x
  9. Abbott R.J., Barton N.H., Good J.M., 2016. Genomics of hybridization and its evolutionary consequences // Mol. Ecol. V. 25. № 11. P. 2325–2332. https://doi.org/10.1111/mec.13685
  10. Anderson B.W., Daugherty R.J., 1974. Characteristics and reproductive biology of grosbeaks (Pheucticus) in the hybrid zone in South Dakota // Wilson Bull. V. 86. № 1. P. 1–11.
  11. Baker M.C., Boylan J.T., 1999. Singing behavior, mating associations and reproductive success in a population of hybridizing Lazuli and Indigo Buntings // Condor. V. 101. № 3. P. 493–504.
  12. Barton N.H., Hewitt G.M., 1985. Analysis of hybrid zones // Ann. Rev. Ecol. Syst. V. 16. P. 113–148.
  13. Bronson C.L., Grubb T.C., Jr, Sattler G.D., Braun M.J., 2005. Reproductive success across the Black-capped Chickadee (Poecile atricapillus) and Carolina Chickadee (P. carolinensis) hybrid zone in Ohio // Auk. V. 122. № 3. P. 759–772.
  14. Campagna L., Rodriguez P., Mazzulla J.C., 2018. Transgressive phenotypes and evidence of weak postzygotic isolation in F1 hybrids between closely related capuchino seedeaters // PLoS One. V. 13. № 6. Art. e0199113. https://doi.org/10.1371/journal.pone.0199113
  15. Currat M., Ruedi M., Petit R.J., Excoffier L., 2008. The hidden side of invasions: Massive introgression by local genes // Evolution. V. 62. № 8. P. 1908–1920. https://doi.org/10.1111/j.1558-5646.2008.00413.x
  16. Delport W., Kemp A.C., Ferguson J.W.H., 2004. Structure of an African red-billed hornbill (Tockus erythrorhynchus rufirostris and T. e. damarensis) hybrid zone as revealed by morphology, behavior, and breeding biology // Auk. V. 121. № 2. P. 565–586.
  17. Dobzhansky T., 1940. Speciation as a stage in evolutionary divergence // Am. Nat. V. 74. № 753. P. 312–321.
  18. Edwards S.V., Kingan S.B., Calkins J.D., Balakrishnan C.N., Jennings W.B., et al., 2005. Speciation in birds: genes, geography, and sexual selection // Proc. Natl Acad. Sci. V. 102. № 1. P. 6550–6557. https://doi.org/10.1073/pnas.0501846102
  19. Ellegren H., Smeds L., Burri R., Olason P.I., Backstrom N., et al., 2012. The genomic landscape of species divergence in Ficedula flycatchers // Nature. V. 491. P. 756–760. https://doi.org/10.1038/nature11584
  20. Gill F., Donsker D., Rasmussen P. (eds.), 2021. IOC World Bird List (v. 11.2). https://doi.org/10.14344/IOC.ML.11.2
  21. Goodwin D., 1986. Crows of the World. Seattle: Univ. Washington Press. 299 p.
  22. Grant P.R., Grant B.R., 1992. Hybridization of bird species // Science. V. 256. P. 193–197.
  23. Haldane J.B.S., 1922. Sex ratio and unisexual sterility in hybrid animals // J. Genetics. V. 12. P. 101–109.
  24. Harrison R.G., 1986. Pattern and process in a narrow hybrid zone // Heredity. V. 56. P. 337–349.
  25. Hedrick P.W., 2013. Adaptive introgression in animals: Examples and comparison to new mutation and standing variation as sources of adaptive variation // Mol. Ecol. V. 22. № 18. P. 4606–4618. https://doi.org/10.1111/mec.12415
  26. Irwin D., 2020. Assortative mating in hybrid zones is remarkably ineffective in promoting speciation // Am. Nat. V. 195. № 6. P. E150–E167. https://doi.org/10.1086/708529
  27. Kryukov A.P., Goroshko O.A., Arkhipov V.Y., Red’kin Y.A., Lee S.I., et al., 2022. Introgression at the emerging secondary contact zone of magpie Pica pica subspecies (Aves: Corvidae): Integrating data on nuclear and mitochondrial markers, vocalizations and field observations // Org. Diver. Evol. V. 22. P. 1037–1064. https://doi.org/10.1007/s13127-022-00568-6
  28. Kryukov A., Iwasa M.A., Kakizawa R., Suzuki H., Pinsker W., Haring E., 2004. Synchronic east-west divergence in azure-winged magpies (Cyanopica cyanus) and magpies (Pica pica) // J. Zool. Syst. Evol. Res. V. 42. № 4. P. 342–351. https://doi.org/10.1111/j.1439-0469.2004.00287.x
  29. Kryukov A.P., Spiridonova L.N., Mori S., Arkhipov V. Yu., Red’kin Y.A., et al., 2017. Deep phylogeographic breaks in magpie Pica pica across the Holarctic: Concordance with bioacoustics and phenotypes // Zool. Sci. V. 34. № 3. P. 185–200. https://doi.org/10.2108/zs160119
  30. Kryukov A.P., Spiridonova L.N., Tyunin A.P., Kryukov K.A., Dorda B.A., 2020. Complete mitochondrial genomes of five subspecies of the Eurasian magpie Pica pica, obtained with Oxford Nanopore MinION, and their interpretation regarding intraspecific taxonomy // Mitochondrial DNA B. V. 5. № 3. P. 3792–3793. https://doi.org/10.1080/23802359.2020.1838354
  31. Larson E.L., Vanderpool D., Sarver B.A., Callahan C., Keeble S., et al., 2018. The evolution of polymorphic hybrid incompatibilities in house mice // Genetics. V. 209. № 3. P. 845–859. https://doi.org/10.1534/genetics.118.300840
  32. Lijtmaer D.A., Mahler B., Tubaro P.L., 2003. Hybridization and postzygotic isolation patterns in pigeons and doves // Evolution. V. 57. № 6. P. 1411–1418.
  33. Liou L.W., Price T.D., 1994. Speciation by reinforcement of premating isolation // Evolution. V. 48. P. 1451–1459.
  34. Madge S., Burn H., 1999. Crows and Jays: A Guide to the Crows, Jays and Magpies of the World. L.: C. Helm. 192 p.
  35. Madge S., Christie D.A., Kirwan G.M., 2020. Oriental Magpie (Pica serica), version 1.0 // Birds of the World / Eds Billerman S.M., Keeney B.K., Rodewald P.G., Schulenberg T.S. Ithaca: Cornell Lab of Ornithology. https://doi.org/10.2173/bow.orimag1.01
  36. Maheshwari S., Barbash D.A., 2011. The genetics of hybrid incompatibilities // Annu. Rev. Genet. V. 45. P. 331–355. https://doi.org/10.1146/annurev-genet-110410-132514
  37. Mallet J., 2005. Hybridization as an invasion of the genome // Trends Ecol. Evol. V. 20. № 5. P. 229–237. https://doi.org/10.1016/j.tree.2005.02.010
  38. Mořkovský L., Janoušek V., Reif J., Rídl J., Pačes J., et al., 2018. Genomic islands of differentiation in two songbird species reveal candidate genes for hybrid female sterility // Mol. Ecol. V. 27. № 4. P. 949–958. https://doi.org/10.1111/mec.14479
  39. Mott C.L., Lockhart L.H., Rigdon R.H., 2004. Chromosomes of the sterile hybrid duck // Cytogen. Genome Res. V. 7. № 5. P. 403–412.
  40. Orr H.A., 1996. Dobzhansky, Bateson, and the genetics of speciation // Genetics. V. 144. № 4. P. 1331–1335.
  41. Osipova O.V., Soktin A.A., 2006. Bank and red vole hybridizatioin under experimental conditions // Dokl. Biol. Sci. V. 410. P. 381–383. https://doi.org/10.1134/S0012496606050103
  42. Ottenburghs J., 2023. How common is hybridization in birds? // J. Ornithol. V. 164. P. 913–920. https://doi.org/10.1007/s10336-023-02080-w
  43. Ottenburghs J., Kraus R.H., Hooft P., van, Wieren S.E., van, Ydenberg R.C., Prins H.H., 2017. Avian introgression in the genomic era // Avian Res. V. 8. № 1. P. 1–11. https://doi.org/10.1186/s40657-017-0088-z
  44. Price T.D., Bouvier M.M., 2002. The evolution of F1 postzygotic incompatibilities in birds // Evolution. V. 56. № 10. P. 2083–2089.
  45. Sætre G.P., Král K., Bures S., Ims R.A., 1999. Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficedula hypoleuca and F. albicollis) // J. Zool. V. 247. № 1. P. 53–64.
  46. Sætre G.P., Moum T., Bureš S., Krá M., Adamjan M., Moreno J., 1997. A sexually selected character displacement in flycatchers reinforces premating isolation // Nature. V. 387. № 6633. P. 589–592.
  47. Servedio M.R., Noor M.A., 2003. The role of reinforcement in speciation: theory and data // Ann. Rev. Ecol. Evol. Syst. V. 34. № 1. P. 339–364. https://doi.org/10.1146/annurev.ecolsys.34.011802.132412
  48. Song G., Zhang R., Alström P., Irestedt M., Cai T., et al., 2018. Complete taxon sampling of the avian genus Pica (magpies) reveals ancient relictual populations and synchronous Late-Pleistocene demographic expansion across the Northern Hemisphere // J. Avian Biol. V. 49. № 2. Art. e01612. https://doi.org/10.1111/jav.01612
  49. Torgasheva A.A., Borodin P.M., 2016. Cytological basis of sterility in male and female hybrids between sibling species of grey voles Microtus arvalis and M. levis // Sci. Rep. V. 6. Art. 36564. https://doi.org/10.1038/srep36564
  50. Turner T.L., Hahn M.W., Nuzhdin S.V., 2005. Genomic islands of speciation in Anopheles gambiae // PLOS Biol. V. 3. № 9. Art. e285. https://doi.org/10.1371/journal.pbio.0030285
  51. Walsh J., Billerman S.M., Rohwer V.G., Butcher B.G., Lovette I.J., 2020. Genomic and plumage variation across the controversial Baltimore and Bullock’s oriole hybrid zone // Auk. V. 137. № 4. Art. ukaa044.
  52. Zhang R., Song G., Qu Y., Alstrom P., Ramos R., et al., 2012. Comparative phylogeography of two widespread magpies: Importance of habitat preference and breeding behavior on genetic structure in China // Mol. Phylogenet. Evol. V. 65. P. 562–572. https://doi.org/10.1016/j.ympev.2012.07.011

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