Sex reversal is a biological process whereby the pathway directed towards the already determined-sex fate is flipped towards the opposite sex, creating a discordance between the primary sex fate and the sex phenotype expressed.[1][2] The process of sex reversal occurs during embryonic development or before gonad differentiation. In GSD species sex reversal means that the sexual phenotype is discordant with the genetic/chromosomal sex. In TSD species sex reversal means that the temperature/conditions that usually trigger the differentiation towards one sexual phenotype are producing the opposite sexual phenotype.[1]

Sex reversal can occur naturally, by mutations, or can be induced artificially. Sex reversal can be genetically or hormonally induced in laboratory. It can also occur artificially by exposure to endocrine disruptors such as pollutants, including herbicides, which can act as estrogen promoters or inhibitors, for instance by altering aromatase expression.[3][4][5][6]

In vertebrates

In gonochoristic fishes

In gonochoristic fishes, the sex can be determined genetically, environmentally or by a combination of both. In fishes, primary sexual fate can be susceptible to alteration by hormones exposure and multiple environmental factors, such as population density, water pH, or temperature. Those conditions can affect the gonad development and differentiation, which can lead to sex reversal.[7][8] In medaka fish, where sex reversal has been documented show a shared gene related to normal male development, the dmy gene. In wild populations, genetically female fate can be phenotypically reversed to males if they carry the dmy gene or a mutated dmy gene and genetic males can be reversed to females if they lack the dmy gene.[9]

Induced reversal in aquaculture industry

In aquaculture, sex control is important due to the role of sex in growth and reproduction. In fishes, growth rates can be different between sexes. These differences can affect their economic value. Producing a monosex fish population can improve product quality and therefore generates higher financial profit.[10]

Hormone-induced sex reversal is the most frequent method used in aquaculture. It consists of exposing sexually undifferentiated fishes to sex steroids.[11][12] There are other methods to induced sex reversal in fishes such as chromosomal/genetic manipulation, hybridization, or treatments influencing sex determination or gonad differentiation (e.g. temperature, population density, pH, social factors).[10]

In amphibians

Sex is genetically determined in amphibians.[13][14] Temperature-induced sex reversal has been documented in some species of anuran and caudate amphibians. Temperature only can have an effect on sex differentiation during a window period called thermosensitive period (TSP) which varies among species.[15][16][17] Tadpoles or larvae exposed to specific higher or lower temperatures, depending on the temperature thresholds of the species, can differentiate gonads that do not align with their primary sexual fate.[18]

Amphibian sex reversal can be also induced by exposure to sex steroid and pollutants. Endocrine disruptors can affect gonad differentiation, and therefore induce sex reversal. Exposure to ethylnyl estradiol (EE2) and bisphenol A (BPA) induces feminizing effects.[19] Masculinizing effects can be induced by exposure to the drug trenbolone, used in cattle.[20]

Research [21] in wild populations of the North American green frog has demonstrated that sex reversal is common. This work shows that genetic females sex reverse into phenotypic males and that genetic males sex reverse into phenotypic females, providing evidence that sex reversal can be bidirectional in amphibians. While endocrine disrupting chemical contamination is known from laboratory experiments to cause sex reversal in amphibians,[22] sex reversal in green frogs occurs irrespective of contamination, suggesting sex reversal is a natural process in amphibians [23]

In reptiles

Sex in reptiles can be determined genetically (GSD), environmentally (ESD) or by an interaction of both.[24] Sex reversal has been documented in detail in wild populations of the central bearded dragon Pogona vitticeps, and in the eastern three-lined skink Bassiana duperreyi. In these species, their genetically determined sex is overridden by temperature influence.[25][24][26]

Sex reversal in reptiles can be induced by hormonal manipulation, treatments influencing sex determination (e.g. temperature) or by inhibition of the aromatase gene (CYP19A1) which causes sex reversal from female to male phenotype.[26]

In birds

In birds, sex reversal has been documented in natural and experimental conditions. Sex steroid manipulation can induced sex reversal in birds. Aromatase inhibitors injected into chicken eggs before the gonadal differentiation stage induce testis development in ZW embryos.[27]

In mammals

Sex reversal in mammals has been documented in domestic species such as cattle, water buffalo, horses, dogs, cats, pigs, goats, etc. Sex reversal in these species usually relates to genetic changes and the resulting phenotype is often associated with gonadal malformation.[28] Natural sex reversal without disruptive effects on fertility has been documented in several rodents, including Myopus schisticolor, Dicrostonyx torquatus, Akodon, Mus minutoides, Microtus cabrerae. In these species some individuals genetically determined as males develop typical ovarian structure.[29] In these rodents species, sex reversal mainly occurs after mutational events.[28]

See also

References

  1. 1 2 Weber C, Capel B (November 2018). "Sex reversal". Current Biology. 28 (21): R1234–R1236. doi:10.1016/j.cub.2018.09.043. PMC 8941919. PMID 30399341.
  2. ↑ Charnov EL, Bull J (April 1977). "When is sex environmentally determined?". Nature. 266 (5605): 828–30. Bibcode:1977Natur.266..828C. doi:10.1038/266828a0. PMID 865602. S2CID 4166753.
  3. ↑ Gilbert SF (2010-04-15). Developmental Biology. ISBN 978-0-87893-384-6.
  4. ↑ Nakamura M (August 2010). "The mechanism of sex determination in vertebrates-are sex steroids the key-factor?". Journal of Experimental Zoology A. 313 (7): 381–98. doi:10.1002/jez.616. PMID 20623803.
  5. ↑ Chew KY, Renfree MB (2016). "Inducing Sex Reversal in Marsupial Mammals". Sexual Development. 10 (5–6): 301–312. doi:10.1159/000450927. PMID 27794571. S2CID 749166.
  6. ↑ Chan ST (August 1970). "Natural sex reversal in vertebrates". Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences. 259 (828): 59–71. Bibcode:1970RSPTB.259...59C. doi:10.1098/rstb.1970.0046. PMID 4399069.
  7. ↑ Yamaguchi T, Kitano T (March 2012). "High temperature induces cyp26b1 mRNA expression and delays meiotic initiation of germ cells by increasing cortisol levels during gonadal sex differentiation in Japanese flounder". Biochemical and Biophysical Research Communications. 419 (2): 287–92. doi:10.1016/j.bbrc.2012.02.012. PMID 22342721.
  8. ↑ Baroiller JF, D'Cotta H (2016). "The Reversible Sex of Gonochoristic Fish: Insights and Consequences". Sexual Development. 10 (5–6): 242–266. doi:10.1159/000452362. PMID 27907925.
  9. ↑ Matsuda M, Shinomiya A, Kinoshita M, Suzuki A, Kobayashi T, Paul-Prasanth B, et al. (March 2007). "DMY gene induces male development in genetically female (XX) medaka fish". Proceedings of the National Academy of Sciences of the United States of America. 104 (10): 3865–70. Bibcode:2007PNAS..104.3865M. doi:10.1073/pnas.0611707104. PMC 1820675. PMID 17360444.
  10. 1 2 Budd AM, Banh QQ, Domingos JA, Jerry DR (2015-05-28). "Sex Control in Fish: Approaches, Challenges and Opportunities for Aquaculture". Journal of Marine Science and Engineering. 3 (2): 329–355. doi:10.3390/jmse3020329.
  11. ↑ Yamamoto T (1953). "Artificially induced sex-reversal in genotypic males of the medaka (Oryzias latipes)". Journal of Experimental Zoology. 123 (3): 571–594. doi:10.1002/jez.1401230309.
  12. ↑ Pandian TJ, Sheela SG (1995). "Hormonal induction of sex reversal in fish". Aquaculture. 138 (1–4): 1–22. doi:10.1016/0044-8486(95)01075-0. ISSN 0044-8486.
  13. ↑ Schmid M, Steinlein C (2001). Sex chromosomes, sex-linked genes, and sex determination in the vertebrate class Amphibia. Birkhäuser Basel. pp. 143–176. doi:10.1007/978-3-0348-7781-7_8. ISBN 978-3-0348-7783-1. PMID 11301597. {{cite book}}: |work= ignored (help)
  14. ↑ Hillis DM, Green DM (1990). "Evolutionary changes of heterogametic sex in the phylogenetic history of amphibians". Journal of Evolutionary Biology. 3 (1–2): 49–64. doi:10.1046/j.1420-9101.1990.3010049.x. ISSN 1010-061X. S2CID 83609311.
  15. ↑ Witschi E (1929). "Studies on sex differentiation and sex determination in amphibians. II. Sex reversal in female tadpoles of Rana sylvatica following the application of high temperature". Journal of Experimental Zoology. 52 (2): 267–291. doi:10.1002/jez.1400520203. ISSN 0022-104X.
  16. ↑ Flament S, Chardard D, Chesnel Ad, Dumond H (2011). Sex Determination and Sexual Differentiation in Amphibians. Elsevier. pp. 1–19. doi:10.1016/b978-0-12-374932-1.00014-7. ISBN 978-0-12-374932-1. {{cite book}}: |work= ignored (help)
  17. ↑ Sakata N, Tamori Y, Wakahara M (2005). "P450 aromatase expression in the temperature-sensitive sexual differentiation of salamander (Hynobius retardatus) gonads". The International Journal of Developmental Biology. 49 (4): 417–25. doi:10.1387/ijdb.041916ns. PMID 15968587.
  18. ↑ Flament S (2016). "Sex Reversal in Amphibians". Sexual Development. 10 (5–6): 267–278. doi:10.1159/000448797. PMID 27648840.
  19. ↑ Bhandari RK, Deem SL, Holliday DK, Jandegian CM, Kassotis CD, Nagel SC, et al. (April 2015). "Effects of the environmental estrogenic contaminants bisphenol A and 17α-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species". General and Comparative Endocrinology. 214: 195–219. doi:10.1016/j.ygcen.2014.09.014. PMID 25277515.
  20. ↑ Olmstead AW, Kosian PA, Johnson R, Blackshear PE, Haselman J, Blanksma C, et al. (October 2012). "Trenbolone causes mortality and altered sexual differentiation in Xenopus tropicalis during larval development". Environmental Toxicology and Chemistry. 31 (10): 2391–8. doi:10.1002/etc.1965. PMID 22847831. S2CID 22489522.
  21. ↑ Lambert MR, Tran T, Kilian A, Ezaz T, Skelly DK (2019-02-08). "Rana clamitans)". PeerJ. 7: e6449. doi:10.7717/peerj.6449. PMC 6369831. PMID 30775188.
  22. ↑ "Pollutants change 'he' frogs into 'she' frogs". Yahoo! News. 2007. Archived from the original on March 2, 2007. Retrieved 2007-03-01.
  23. ↑ "Healthy frogs can mysteriously reverse their sex". National Geographic. Archived from the original on February 20, 2021.
  24. 1 2 Holleley CE, O'Meally D, Sarre SD, Marshall Graves JA, Ezaz T, Matsubara K, et al. (July 2015). "Sex reversal triggers the rapid transition from genetic to temperature-dependent sex". Nature. 523 (7558): 79–82. Bibcode:2015Natur.523...79H. doi:10.1038/nature14574. PMID 26135451. S2CID 1741119.
  25. ↑ Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Marshall Graves JA (2005). "The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes". Chromosome Research. 13 (8): 763–76. doi:10.1007/s10577-005-1010-9. PMID 16331408. S2CID 4934610.
  26. 1 2 Holleley CE, Sarre SD, O'Meally D, Georges A (2016). "Sex Reversal in Reptiles: Reproductive Oddity or Powerful Driver of Evolutionary Change?". Sexual Development. 10 (5–6): 279–287. doi:10.1159/000450972. PMID 27794577. S2CID 27199048.
  27. ↑ Major AT, Smith CA (2016). "Sex Reversal in Birds". Sexual Development. 10 (5–6): 288–300. doi:10.1159/000448365. PMID 27529790. S2CID 5525642.
  28. 1 2 Parma P, Veyrunes F, Pailhoux E (2016). "Sex Reversal in Non-Human Placental Mammals". Sexual Development. 10 (5–6): 326–344. doi:10.1159/000448361. hdl:2434/429122. PMID 27529721. S2CID 21751654.
  29. ↑ Rahmoun M, Perez J, Saunders PA, Boizet-Bonhoure B, Wilhelm D, Poulat F, Veyrunes F (2014). "Anatomical and molecular analyses of XY ovaries from the African pygmy mouse Mus minutoides". Sexual Development. 8 (6): 356–63. doi:10.1159/000368664. PMID 25359508. S2CID 19650896.
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