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Natural and Experimental Sex Reversal in Birds and Other Groups of Vertebrates, with the Exception of Mammals

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Abstract

The review is focused on the current problem of sex determination. Many research papers were devoted to this issue, but all the details of its mechanisms have not yet been disclosed, since they are very diverse. The article summarizes new data obtained in the studies of natural and experimental sex reversal cases in vertebrates. Representatives of cold-blooded (fish, amphibians, reptiles) and warm-blooded (birds) vertebrates are considered. Sex reversal, which occurs in both natural and experimental conditions, may result from genetic disorders that appear at the early stages of embryonic development, as well as from normal changes that occur in mature animals under the control of neuroendocrine system. It is suggested that sex reversal and sex determination can be interrelated phenomena. Special emphasis is put on sex reversal and determination in birds. The studies on experimental sex reversal in these animals are considered in detail. For these purposes, the results of research studies on the relationship between the phenotypic sex manifestation at the cellular, tissue, and organ levels and its chromosomal and hormonal determination, as well as genetic and epigenetic control, are summarized. Finally, promising directions in the study of natural and experimental sex reversal in vertebrates are suggested.

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REFERENCES

  1. Smirnov, A.F. and Trukhina, A.V., Specific features of sex determination in birds on the example of Gallus gallus domesticus, in Gene Expression and Phenotypic Traits, UK: IntechOpen, 2020, pp. 338—481. https://doi.org/10.5772/intechopen.91178

    Book  Google Scholar 

  2. Cox, R.M., Sex steroids as mediators of phenotypic integration, genetic correlations, and evolutionary transitions, Mol. Cell. Endocrinol., 2019, vol. 502, p. 110668. https://doi.org/10.1016/j.mce.2019.110668

    Article  CAS  PubMed  Google Scholar 

  3. Weber, C. and Capel, B., Sex reversal, Curr. Biol., 2018, vol. 28, no. 21, pp. R1234—R1236. https://doi.org/10.1016/j.cub.2018.09.04

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Wilhelm, D., Palmer, S.J., and Koopman, P., Sex determination and gonadal development in mammals, Physiol. Rev., 2007, vol. 87, no. 1, pp. 1—28. https://doi.org/10.1152/physrev.00009.2006

  5. Wilhelm, D. and Pask, A.J., Genetic mechanisms of sex determination, in Encyclopedia of Reproduction, Elsevier, 2018, vol. 3, pp. 245—248. https://doi.org/10.1016/B978-0-12-801238-3.64460-4

    Book  Google Scholar 

  6. Ni, M., Feretzaki, M., Sun, S., et al., Sex in fungi, Annu. Rev. Genet., 2011, vol. 45, pp. 405—430. https://doi.org/10.1146/annurev-genet-110410-132536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Smirnov, A.F. and Trukhina, A.V., Comparison of sex determination in vertebrates (nonmammals), chapter 3 of Molecular-Genetic Mechanisms of Sex Determination in Animals, Yuan-Chuan Chen and Shiu-Jau Chen, Eds., Sci. Res. Publ., 2017, р. 162. ISBN: 978-1-61896-390-1.

  8. Tagirov, M.T., Sex determination and control mechanisms in birds, Biotechnol. Acta., 2013, vol. 6, no. 1, pp. 62—72. https://doi.org/10.15407/biotech6.01.062

    Article  Google Scholar 

  9. Bull, J.J., Evolution of environmental sex determination from genotypic sex determination, Heredity, 1981, vol. 47, no. 2, pp. 173—184.

    Article  Google Scholar 

  10. Holleley, C.E., O’Meally, D., Sarre, S.D., et al., Sex reversal triggers the rapid transition from genetic to temperature-dependent sex, Nature, 2015, vol. 523, no. 7558, pp. 79—82. https://doi.org/10.1038/nature14574

    Article  CAS  PubMed  Google Scholar 

  11. Pennell, M.W., Mank, J.E., and Peichel, C.L., Transitions in sex determination and sex chromosomes across vertebrate species, Mol. Ecol., 2018, vol. 27, no. 19, pp. 3950—3963. https://doi.org/10.1111/mec.14540

    Article  PubMed  PubMed Central  Google Scholar 

  12. Nakamura, M., Is a sex-determining gene(s) necessary for sex-determination in amphibians? Steroid hormones may be the key factor, Sex. Dev., 2013, vol. 7, nos. 1–3, pp. 104–114. https://doi.org/10.1159/000339661

    Article  CAS  PubMed  Google Scholar 

  13. Ma, W.-J. and Veltsos, P., The diversity and evolution of sex chromosomes in frogs, Genes, 2021, vol. 12, p. 483. https://doi.org/10.3390/genes12040483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Miura, I., Sex determination and sex chromosomes in amphibian, Sex. Dev., 2017, vol. 11, nos. 5—6, pp. 298—306. https://doi.org/10.1159/000485270

    Article  CAS  PubMed  Google Scholar 

  15. Wallace, H., Badawy, G.M.I., and Wallace, B.M.N., Amphibian sex determination and sex reversal, Cell. Mol. Life Sci., 1999, vol. 55, pp. 901—909. https://doi.org/10.1007/s000180050343

  16. Eggert, C., Sex determination: the amphibian models, Reprod. Nutr. Dev., 2004, vol. 44, pp. 539—549. https://doi.org/10.1051/rnd:2004062

    Article  PubMed  Google Scholar 

  17. Keating, S.E., Blumer, M., Grismer, L.L., et al., Sex chromosome turnover in bent-toed geckos (Cyrtodactylus), Genes, 2021, vol. 12, p. 116. https://doi.org/10.3390/genes12010116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Rovatsos, M., Vukić, J., Mrugała, A., et al., Little evidence for switches to environmental sex determination and turnover of sex chromosomes in lacertid lizards, Sci. Rep., 2019, vol. 9, p. 7832. https://doi.org/10.1038/s41598-019-44192-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Prokop’ev, Ya.V., Antropova, E.Yu., Mazitova, M.I., and Klyucharov, I.V., XX testicular disorder of sex development: rare variant of male infertility (case history), Russ. Med. Zh., 2019, no. 11, pp. 26—28.

  20. Ogino, Y., Tohyama, S., Kohno, S., et al., Functional distinctions associated with the diversity of sex steroid hormone receptors ESR and AR, J. Steroid Biochem. Mol. Biol., 2018, vol. 184, pp. 38—46. https://doi.org/10.1016/j.jsbmb.2018.06.002

  21. Rajendiran, P., Jaafar, F., Kar, S., et al., Sex determination and differentiation in teleost: roles of genetics, environment, and brain, Biology (Basel), 2021, vol. 10, p. 973. https://doi.org/10.3390/biology10100973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Nakamura, M., Kobayashi, T., Chang, X.-T., and Nagahama, Y., Gonadal sex differentiation in teleost fish, J. Exp. Zool., 1998, vol. 281, pp. 362—372. https://doi.org/10.1002/(SICI)1097-010X(19980801)-281:5<362::AID-JEZ3>3.0.CO;2-M

    Article  Google Scholar 

  23. Yamamoto, Y., Hattori, R.S., Patiño, R., and Strüssmann, C.A., Environmental regulation of sex determination in fishes: insights from Atheriniformes, Curr. Top. Dev. Biol., 2019, vol. 134, pp. 49—69. https://doi.org/10.1016/bs.ctdb.2019.02.003

    Article  CAS  PubMed  Google Scholar 

  24. Camerino, G., Parma, P., Radi, O., and Valentini, S., Sex determination and sex reversal, Curr. Opin. Genet. Dev., 2006, vol. 16, no. 3, pp. 289—292. https://doi.org/10.1016/j.gde.2006.04.014

    Article  CAS  PubMed  Google Scholar 

  25. Guerrero-Estévez, S. and Moreno-Mendoza, N., Sexual determination and differentiation in teleost fish, Rev. Fish Biol. Fish., 2009, vol. 20, no. 1, pp. 101—121. https://doi.org/10.1007/s11160-009-9123-4

    Article  Google Scholar 

  26. Hattori, R.S., Strüssmann, C.A., Fernandino, J., et al., Genotypic sex determination in teleosts: insights from the testis-determining amhy gene, Gen. Comp. Endocrinol., 2013, vol. 192, pp. 55—59. https://doi.org/10.1016/j.ygcen.2013.03.019

    Article  CAS  PubMed  Google Scholar 

  27. Kobayashi, Y., Nagahama, Y., and Nakamura, M., Diversity and plasticity of sex determination and differentiation in fishes, Sex. Dev., 2012, vol. 7, nos. 1—3, pp. 115—125. https://doi.org/10.1159/000342009

    Article  CAS  PubMed  Google Scholar 

  28. Baroiller, J.F., D’Cotta, H., and Saillant, E., Environmental effects on fish sex determination and differentiation, Sex. Dev., 2009, vol. 3, nos. 2—3, pp. 118—135. https://doi.org/10.1159/000223077

    Article  CAS  PubMed  Google Scholar 

  29. Devlin, R.H. and Nagahama, Y., Sex determination and sex differentiation in fish: an over-view of genetic, physiological, and environmental influences, Aquaculture, 2002, vol. 208, nos. 3—4, pp. 191—364. https://doi.org/10.1016/S0044-8486(02)00057-1

    Article  CAS  Google Scholar 

  30. Strüssmann, C.A. and Nakamura, M., Morphology, endocrinology, and environmental modulation of gonadal sex differentiation in teleost fishes, Fish Physiol. Biochem., 2002, vol. 26, pp. 13—29. https://doi.org/10.1023/A:1023343023556

    Article  Google Scholar 

  31. Mustapha, U.F., Huang, Y., Huang, Y.-Q., et al., Gonadal development and molecular analysis revealed the critical window for sex differentiation, and E2 reversibility of XY-male spotted scat, Scatophagus argus, Aquaculture, 2021, vol. 544, article 737147. https://doi.org/10.1016/j.aquaculture.2021.737147

    Article  CAS  Google Scholar 

  32. Hsiao, C.-D. and Tsai, H.-J., Transgenic zebrafish with fluorescent germ cell: a useful tool to visualize germ cell proliferation and juvenile hermaphroditism in vivo, Dev. Biol., 2003, vol. 262, pp. 313—323. https://doi.org/10.1016/S0012-1606(03)00402-0

    Article  CAS  PubMed  Google Scholar 

  33. Wu, G.-C. and Chang, C.-F., Primary males guide the femaleness through the regulation of testicular Dmrt1 and ovarian Cyp19a1a in protandrous black porgy, Gen. Comp. Endocrinol., 2018, vol. 261, pp. 198—202. https://doi.org/10.1016/j.ygcen.2017.01.033

    Article  CAS  PubMed  Google Scholar 

  34. Tang, Y., Chen, J.-Y., Ding, G.-H., and Lin, Z.-H., Analyzing the gonadal transcriptome of the frog Hoplobatrachus rugulosus to identify genes involved in sex development, BMC Genomics, 2021, vol. 22, p. 552. https://doi.org/10.1186/s12864-021-07879-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Mendoza-Cruz, E., Moreno-Mendoza, N., Zambrano, L., and Villagrán-Santa Cruz, M., Development and gonadal sex differentiation in the neotenic urodele: Ambystoma mexicanum, Zoomorphology, 2017, vol. 136, pp. 497—509. https://doi.org/10.1007/s00435-017-0361-z

    Article  Google Scholar 

  36. Lambert, M.R., Tran, T., Kilian, A., et al., Molecular evidence for sex reversal in wild populations of green frogs (Rana clamitans), Peer J., 2019, vol. 7. e6449. https://doi.org/10.7717/peerj.6449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Flament, S., Sex reversal in amphibians, Sex. Dev., 2016, vol. 10, nos. 5—6, pp. 267—278. https://doi.org/10.1159/000448797

    Article  CAS  PubMed  Google Scholar 

  38. Oike, A., Kodama, M., Yasumasu, S., et al., Participation of androgen and its receptor in sex determination of an amphibian species, PLoS One, 2017, vol. 12, no. 6. e0178067. https://doi.org/10.1371/journal.pone.0178067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Roco, Á.S., Ruiz-García, A., and Bullejos, M., Testis development and differentiation in amphibians, Genes, 2021, vol. 12, p. 578. https://doi.org/10.3390/genes12040578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Valenzuela, N., Badenhorst, D., Montiel, E.E., and Literman, R., Molecular cytogenetic search for cryptic sex chromosomes in painted turtles Chrysemys picta, Cytogenet. Genome Res., 2014, vol. 144, no. 1, pp. 39—46. https://doi.org/10.1159/000366076

    Article  PubMed  Google Scholar 

  41. Pieau, C., Dorizzi, M., Richard-Mercier, N., Temperature-dependent sex determination and gonadal differentiation in reptiles, in Genes and Mechanisms in Vertebrate Sex Determination, Scherer, G. and Schmid, M., Eds., Basel: Switzerland: Birkhäuser, 2001, pp. 117—141

    Google Scholar 

  42. Merchant-Larios, H. and Díaz-Hernández, V., Environmental sex determination mechanisms in reptiles, Sex. Dev., 2012, vol. 7, nos. 1—3, pp. 95—103. https://doi.org/10.1159/000341936

    Article  CAS  PubMed  Google Scholar 

  43. Georges, A. and Holleley, C.E., How does temperature determine sex?, Science, 2018, vol. 360, no. 6389, pp. 601—602. https://doi.org/10.1126/science.aat5993

    Article  CAS  PubMed  Google Scholar 

  44. Glersberg, M.F. and Kemper, N., Rearing male layer chickens: a German perspective, Agriculture, 2018, vol. 8, p. 176. https://doi.org/10.3390/agriculture8110176

    Article  Google Scholar 

  45. Singh, L., Wadhwa, R., Naidu, S., et al., Sex- and tissue specific Bkm (GATA)-binding protein in the germ cells of heterogametic sex, J. Biol. Chem., 1994, vol. 269, no. 41, pp. 25321—25327.

    Article  CAS  Google Scholar 

  46. Smirnov, A.F. and Trukhina, A.V., Molekulyarno-geneticheskie mekhanizmy determinatsii pola u zhivotnykh (Molecular Genetic Mechanisms of Sex Determination in Animals), St. Petersburg: Nestor-Istoriya, 2016.

  47. Elbrecht, A. and Smith, R.G., Aromatase enzyme activity and sex determination in chickens, Science, 1992, vol. 255, no. 5043, pp. 467—470. https://doi.org/10.1126/science.1734525

    Article  CAS  PubMed  Google Scholar 

  48. Vaillant, S., Guémené, D., Dorizzi, M., et al., Degree of sex reversal as related to plasma steroid levels in genetic female chickens (Gallus domesticus) treated with Fadrozole, Mol. Rep. Dev., 2003, vol. 65, no. 4, pp. 420—428. https://doi.org/10.1002/mrd.10318

    Article  CAS  Google Scholar 

  49. Fazli, N., Hassanabadi, A., Mottaghitalab, M., and Hajati, H., Manipulation of broiler chickens sex differentiation by in ovo injection of aromatase inhibitors, and garlic and tomato extracts, Poult. Sci., 2015, vol. 94, no. 11, pp. 2778—2783. https://doi.org/10.3382/ps/pev236

    Article  CAS  PubMed  Google Scholar 

  50. Yang, X., Zheng, J., Na, R., et al., Degree of sex differentiation of genetic female chicken treated with different doses of an aromatase inhibitor, Sex. Dev., 2008, vol. 2, no. 6, pp. 309—315. https://doi.org/10.1159/000195680

    Article  CAS  PubMed  Google Scholar 

  51. Yang, X., Zheng, J., Qu, L., et al., Methylation status of cMHM and expression of sex-specific genes in adult sex-reversed female chickens, Sex. Dev., 2011, vol. 5, no. 3, pp. 147—154. https://doi.org/10.1159/000327712

    Article  CAS  PubMed  Google Scholar 

  52. Yang, X., Deng, J., Zheng, J., et al., A Window of MHM demethylation correlates with key events in gonadal differentiation in the chicken, Sex. Dev., 2016, vol. 10, no. 3, pp. 152—158. https://doi.org/10.1159/000447659

    Article  CAS  PubMed  Google Scholar 

  53. Mohammadrezaei, M., Toghyani, M., Gheisari, A., et al., Synergistic effect of fadrozole and insulin-like growth factor-I on female-to-male sex reversal and body weight of broiler chicks, PLoS One, 2014, vol. 9, no. 7. e103570. https://doi.org/10.1371/journal.pone.0103570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Trukhina, A.V., Lukina, N.A., and Smirnov, A.F., Hormonal sex inversion and some aspects of its genetic determination in chicken, Russ. J. Genet., 2018, vol. 54, no. 9, pp. 1069—1077. https://doi.org/10.1134/S1022795418090144

    Article  CAS  Google Scholar 

  55. Estermann, M.A., Major, A.T., Smith, C.A., Gonadal sex differentiation: supporting versus steroidogenic cell lineage specification in mammals and birds, Front. Cell Dev. Biol., 2020, vol. 8, article 616387, pp. 1—10. https://doi.org/10.3389/fcell.2020.616387

  56. Abinawanto, A, Zhang, C., Saito, N., et al., Identification of sperm-bearing female-specific chromosome in the sex-reversed chicken, J. Exp. Zool., 1998, vol. 280, no. 2, pp. 65—72. https://doi.org/10.1002/(sici)1097-010x(19980101)280:1<65::aid-jez8>3.0.co;2-f

    Article  CAS  PubMed  Google Scholar 

  57. Takagi, S., Ono, T., Tsukada, A., et al., Fertilization and blastoderm development of quail oocytes after intracytoplasmic injection of chicken sperm bearing the W chromosome, Poult. Sci., 2007, vol. 86, no. 5, pp. 937—943. https://doi.org/10.1093/ps/86.5.937

    Article  CAS  PubMed  Google Scholar 

  58. Ellis, H.L., Shioda, K., Rosenthal, N.F., et al., Masculine epigenetic sex marks of the cyp19a1/aromatase promoter in genetically male chicken embryonic gonads are resistant to estrogen-induced phenotypic sex conversion, Biol. Reprod., 2012, vol. 87, no. 1, pp. 1—12. https://doi.org/10.1095/biolreprod.112.099747

    Article  CAS  Google Scholar 

  59. Major, A.T. and Smith, C.A., Sex reversal in birds, Sex. Dev., 2016, vol. 10, pp. 288—300. https://doi.org/10.1159/000448365

    Article  CAS  PubMed  Google Scholar 

  60. Morris, K.R., Hirst, C.E., Major, A.T., et al., Gonadal and endocrine analysis of a gynandromorphic chicken, Endocrinology, 2018, vol. 159, no. 10, pp. 3492—3502. https://doi.org/10.1210/en.2018-00553

    Article  CAS  PubMed  Google Scholar 

  61. Estermann, M.A., Major, A.T., Smith, C.A., Genetic regulation of avian testis development, Genes, 2021, vol. 12, p. 1459. https://doi.org/10.3390/genes12091459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Lambeth, L.S., Cummins, D.M., Doran, T.J., et al., Overexpression of aromatase alone is sufficient for ovarian development in genetically male chicken embryos, PLoS One, 2013, vol. 8, no. 6, p. e68362. https://doi.org/10.1371/journal.pone.0068362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Vining, B., Ming, Z., Bagheri-Fam, S., et al., Diverse regulation but conserved function: SOX9 in vertebrate sex determination, Genes, 2021, vol. 12, p. 486. https://doi.org/10.3390/genes12040486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Smith, C.A., Roeszler, K.N., Ohnesorg, T., et al., The avian Z-linked gene DMRT1 is required for male sex determination in the chicken, Nature, 2009, vol. 461, no. 7261, pp. 267—271. https://doi.org/10.1038/nature08298

    Article  CAS  PubMed  Google Scholar 

  65. Lambeth, L.S., Morris, K.R., Wise, T.G., et al., Transgenic chickens overexpressing aromatase have high estrogen levels but maintain a predominantly male phenotype, Endocrinology, 2016, vol. 157, no. 1, pp. 83—90. https://doi.org/10.1210/en.2015-1697

    Article  CAS  PubMed  Google Scholar 

  66. Wang, J. and Gong, Y., Transcription of CYP19A1 is directly regulated by SF-1 in the theca cells of ovary follicles in chicken, Gen. Comp. Endocrinol., 2017, vol. 247, pp. 1—7. https://doi.org/10.1016/j.ygcen.2017.03.013

    Article  CAS  PubMed  Google Scholar 

  67. Jin, K., Zuo, Q., Song, J., et al., CYP19A1 (aromatase) dominates female gonadal differentiation in chicken (Gallus gallus) embryos sexual differentiation, Biosci. Rep., 2020, vol. 40, no. 10, p. BSR20201576. https://doi.org/10.1042/BSR20201576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Hung, T. and Chang, H.Y., Long noncoding RNA in genome regulation: prospects and mechanisms, RNA Biol., 2010, vol. 7, no. 5, pp. 582—585. https://doi.org/10.4161/rna.7.5.13216

  69. Yoon, J.-H., Abdelmohsen, K., and Gorospe, M., Posttranscriptional gene regulation by long noncoding RNA, J. Mol. Biol., 2013, vol. 425, no. 19, pp. 3723—3730. https://doi.org/10.1016/j.jmb.2012.11.024

    Article  CAS  PubMed  Google Scholar 

  70. Huang, Sh., Ye, L., and Chen, H., Sex determination and maintenance: the role of DMRT1 and FOXL2, Asian J. Androl., 2017, vol. 19, no. 6, pp. 619—624. https://doi.org/10.4103/1008-682X.194420

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Ioannidis, J., Taylor, G., Zhao, D., et al., Primary sex determination in birds depends on DMRT1 dosage, but gonadal sex does not determine adult secondary sex characteristics, Proc. Natl. Acad. Sci. U.S.A., 2021, vol. 118, no. 10, p. e2020909118. https://doi.org/10.1073/pnas.2020909118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Clinton, M., Zhao, D., Nandi, S., and McBride, D., Evidence for avian cell autonomous sex identity (CASI) and implications for the sex-determination process?, Chromosome Res., 2012, vol. 20, no. 1, pp. 177—190. https://doi.org/10.1007/s10577-011-9257-9

    Article  CAS  PubMed  Google Scholar 

  73. Piferrer, F. and Anastasiadi, D., Do the offspring of sex reversals have higher sensitivity to environmental perturbations?, Sex. Dev., 2021, no. 15, pp. 134—147. https://doi.org/10.1159/000515192

  74. Smith, C.A., Major, A.T., and Esterman, M.A., The curious case of avian sex determination, Trends Genet., 2021, vol. 37, no. 6, pp. 496—497.

    Article  CAS  Google Scholar 

  75. Smith, C.A., Major, A.T., and Estermann, M.A., Chicken, sex and revisiting an old paradigm, Endocrinology, 2021, vol. 162, no. 7, p. bqab106. https://doi.org/10.1210/endocr/bqab106

  76. Shioda, K., Odajima, J., Kobayashi, M., et al., Transcriptomic and epigenetic preservation of genetic sex identity in estrogen–feminized male chicken embryonic gonads, Endocrinology, 2021, vol. 162, no. 1, p. bqaa208. https://doi.org/10.1210/endocr/bqaa208

  77. Aslam, M.L. and Woelders, H., Steroid hormones and female energy balance: relation to offspring primary sex ratio, in Egg Innovations and Strategies for Improvements, Acad. Press, 2017, pp. 47—54. https://doi.org/10.1016/B978-0-12-800879-9.00005-6

    Book  Google Scholar 

  78. Wrobel, E.R., Molina, E., Khan, N., et al., Androgen and mineralocorticoid receptors are present on the germinal disc region in laying hens: potential mediators of sex ratio adjustment in birds?, Gen. Comp. Endocrinol., 2019, vol. 287, no. 2, p. 113353. https://doi.org/10.1016/j.ygcen.2019.113353

    Article  CAS  PubMed  Google Scholar 

  79. Pinson, S.E., Wilson, J.L., and Navara, K.J., Timing matters: corticosterone injections 4 h before ovulation bias sex ratios towards females in chickens, J. Comp. Physiol. B, 2015, vol. 185, no. 5, pp. 539—546. https://doi.org/10.1007/s00360-015-0897-5

    Article  CAS  PubMed  Google Scholar 

  80. Bruggeman, V., As, P.V., and Decuypere, E., Developmental endocrinology of the reproductive axis in the chicken embryo, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2002, vol. 131, no. 4, pp. 839—846. https://doi.org/10.1016/S1095-6433(02)00022-3

    Article  Google Scholar 

  81. Teranishi, M., Shimada, Y., Hori, T., et al., Transcripts of the MHM region on the chicken Z chromosome accumulate as non-coding RNA in the nucleus of female cells adjacent to the DMRT1 locus, Chromosome Res., 2001, vol. 9, no. 2, pp. 147—165. https://doi.org/10.1023/a:1009235120741

    Article  CAS  PubMed  Google Scholar 

  82. Geffroy, B. and Douhard, M., The adaptive sex in stressful environment, Trends Ecol. Evol., 2019, vol. 34, no. 7, pp. 628—640. https://doi.org/10.1016/j.tree.2019.02.012

  83. Sánchez, L. and Chaouiya, C., Logical modelling uncovers developmental constraints for primary sex determination of chicken gonads, J. R. Soc. Interface, 2018, vol. 15, p. 20180165. https://doi.org/10.1098/rsif.2018.0165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kuroiwa, A., Sex-determining mechanism in avians, Adv. Exp. Med. Biol., 2017, vol. 1001, pp. 19—31. https://doi.org/10.1007/978-981-10-3975-1_2

    Article  CAS  PubMed  Google Scholar 

  85. Hirst, C.E., Major, A.T., and Smith, C.A., Sex determination and gonadal sex differentiation in the chicken model, Int. J. Dev. Biol., 2018, vol. 62, nos. 1—3, pp. 153–166. https://doi.org/10.1387/ijdb.170319cs

    Article  CAS  PubMed  Google Scholar 

  86. Bellott, D.W., Skaletsky, H., Cho, T.J., et al., Avian W and mammalian Y chromosomes convergently retained dosage-sensitive regulators, Nat. Genet., 2017, vol. 49, no. 3, pp. 387—394. https://doi.org/10.1038/ng.3778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Komissarov, A.S., Galkina, S.A., Koshel, E.I., et al., New high copy tandem repeat in the content of the chicken W chromosome, Chromosoma, 2018, vol. 127, no. 1, pp. 73—83. https://doi.org/10.1007/s00412-017-0646-5

    Article  CAS  PubMed  Google Scholar 

  88. Liu, L., Fan, Y., Zhao, D., et al., Expression profile of chicken sex chromosome gene BTF3 is linked to gonadal phenotype, Sex. Dev., 2019, vol. 13, no. 4, pp. 212—220. https://doi.org/10.1159/000506344

    Article  CAS  PubMed  Google Scholar 

  89. Xu, L. and Zhou, Q., The female-specific W chromosomes of birds have conserved gene contents but are not feminized, Genes, 2020, vol. 11, p. 1126. https://doi.org/10.3390/genes11101126

    Article  CAS  PubMed Central  Google Scholar 

  90. Rogers, T.F., Pizzari, T., and Wright, A.E., Multi-copy gene family evolution on the avian W chromosome, Heredity, 2021, vol. 112, no. 3, pp. 250—259. https://doi.org/10.1093/jhered/esab016

    Article  Google Scholar 

  91. Sun, C., Jin K., Zhou J. et al. Role and function of the HintW in early sex differentiation in chicken (Gallus gallus) embryo, Anim. Biotechnol., 2021, pp. 1–11. https://doi.org/10.1080/10495398.2021.1935981

  92. Jin K., Zhou, J., Zuo Q., et al., UBE2I stimulates female gonadal differentiation in chicken (Gallus gallus) embryos, J. Integr. Agric., 2021, vol. 20, pp. 2—10. https://doi.org/10.1016/S2095-3119(20)63486-4

    Article  Google Scholar 

  93. Kinsella, C.M., Ruiz-Ruano, F.J., Dion-Côté, A.M., et al., Programmed DNA elimination of germline development genes in songbirds, Nat. Commun., 2019, vol. 10, p. 5468. https://doi.org/10.1038/s41467-019-13427-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Ezaz, T. and Deakin, J.E., Repetitive sequence and sex chromosome evolution in vertebrates, Adv. Evol. Biol., 2014, article ID 104683. https://doi.org/10.1155/2014/104683

  95. Nagahama, Y., Chakraborty, T., Paul-Prasanth, B., et al., Sex determination, gonadal sex differentiation and plasticity in vertebrate species, J. Physiol. Rev., 2020, p. 213. https://doi.org/10.1152/physrev.00044.2019

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This study was supported by the Russian Foundation for Basic Research (grant no. 20-14-50268, “Expansion”).

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Correspondence to A. V. Trukhina.

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The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by N. Maleeva

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Smirnov, A.F., Leoke, D.Y. & Trukhina, A.V. Natural and Experimental Sex Reversal in Birds and Other Groups of Vertebrates, with the Exception of Mammals. Russ J Genet 58, 613–625 (2022). https://doi.org/10.1134/S1022795422060114

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