1932

Abstract

In vertebrates, sex organs are generally specialized to perform a male or female reproductive role. Acquisition of the Müllerian duct, which gives rise to the oviduct, together with emergence of the Amh/Amhr2 system favored evolution of viviparity in jawed vertebrates. Species with high sex-specific reproductive adaptations have less potential to sex reverse, making intersex a nonfunctional condition. Teleosts, the only vertebrate group in which hermaphroditism evolved as a natural reproductive strategy, lost the Müllerian duct during evolution. They developed for gamete release complete independence from the urinary system, creating optimal anatomic and developmental preconditions for physiological sex change. The common and probably ancestral role of Amh is related to survival and proliferation of germ cells in early and adult gonads of both sexes rather than induction of Müllerian duct regression. The relationship between germ cell maintenance and sex differentiation is most evident in species in which Amh became the master male sex–determining gene.

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2019-02-15
2024-03-29
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Literature Cited

  1. 1.  Mittwoch U 2005. Sex determination in mythology and history. Arq. Bras. Endocrinol. Metabol. 49:7–13
    [Google Scholar]
  2. 2.  Avise JC, Mank JE 2009. Evolutionary perspectives on hermaphroditism in fishes. Sex. Dev. 3:152–63
    [Google Scholar]
  3. 3.  Capel B 2017. Vertebrate sex determination: evolutionary plasticity of a fundamental switch. Nat. Rev. Genet. 18:675–89
    [Google Scholar]
  4. 4.  Raz E 2003. Primordial germ-cell development: the zebrafish perspective. Nat. Rev. Genet. 4:690–700
    [Google Scholar]
  5. 5.  Raz E 2005. Germ cells: sex and repression in mice. Curr. Biol. 15:R600–3
    [Google Scholar]
  6. 6.  Lombardi J 1998. Comparative Vertebrate Reproduction New York: Springer US
  7. 7.  Gilbert SF 2006. Developmental Biology Sunderland, MA: Sinauer
  8. 8.  Rey R, Lukas-Croisier C, Lasala C, Bedecarras P 2003. AMH/MIS: what we know already about the gene, the protein and its regulation. Mol. Cell. Endocrinol. 211:21–31
    [Google Scholar]
  9. 9.  Josso N, di Clemente N, Gouedard L 2001. Anti-Müllerian hormone and its receptors. Mol. Cell. Endocrinol. 179:25–32
    [Google Scholar]
  10. 10.  Mullen RD, Behringer RR 2014. Molecular genetics of Müllerian duct formation, regression and differentiation. Sex. Dev. 8:281–96
    [Google Scholar]
  11. 11.  Wood R 1998. Trends in Genetics: Genetic Nomenclature Guide with Information on Websites Cambridge, UK: Elsevier
  12. 12.  Nelson JS, Grande TC, Wilson MVH 2016. Fishes of the World New York: John Wiley & Sons
  13. 13.  Hardisty MW 1971. Gonadogenesis, sex differentiation, and gametogenesis. The Biology of Lampreys 1 MW Hardisty, IC Potter 295–360 New York: Academic
    [Google Scholar]
  14. 14.  Gorbman A 1990. Sex differentiation in the hagfish Eptatretus stouti. Gen. Comp. . Endocrinol 77:309–23
    [Google Scholar]
  15. 15.  Jørgensen JM, Lomholt JP, Weber RE, Malte H 1998. The Biology of Hagfishes Dordrecht, Neth: Springer
  16. 16.  Clemens BJ, Sower SA, van de Wetering S, Schreck CB 2012. Incidence of male intersex in adult Pacific lamprey (Entosphenus tridentatus), with a brief discussion of intersex versus hermaphroditism in lampreys (Petromyzontiformes). Can. J. Zool. 90:1201–6
    [Google Scholar]
  17. 17.  Musick JA, Ellis J 2005. Reproductive evolution of Chondrichthyans. Reproductive Biology and Phylogeny of Chondrichthyans WC Hamlett 45–79 Enfield, NH: Sci. Publ
    [Google Scholar]
  18. 18.  Wourms JP 1981. Viviparity: the maternal-fetal relationship in fishes. Am. Zool. 21:473–515
    [Google Scholar]
  19. 19.  Wourms JP 1977. Reproduction and development in chondrichthyan fishes. Am. Zool. 17:379–410
    [Google Scholar]
  20. 20.  Norris DO 1987. Regulation of male gonaducts and sex accessory structures. Hormones and Reproduction in Fishes, Amphibians, and Reptiles DO Norris, RE Jones 327–54 Boston: Springer
    [Google Scholar]
  21. 21.  Hamlett WC 2005. Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids, and Chimaeras Boca Raton, FL: CRC Press
  22. 22.  Galíndez EJ, Díaz-Andrade MC, Avaca MS, Estecondo S 2010. Morphological study of the oviductal gland in the smallnose fanskate Sympterygia bonapartii (Muller and Henle, 1841) (Chondrichthyes, Rajidae). Braz. J. Biol. 70:325–33
    [Google Scholar]
  23. 23.  Smith RM, Walker TI, Hamlett WC 2004. Microscopic organization of the oviducal gland of the holocephalan elephant fish. Callorhynchus milii. Freshw. Res. 55:155–64
    [Google Scholar]
  24. 24.  Capapé C, El Kamel-Moutalibi O, Mnasri N, Boumaïza M, Reynaud C 2012. A case of hermaphroditism in tortonese's stingray, Dasyatis tortonesei (Elasmobranchii: Rajiformes: Dasyatidae) from the Lagoon of Bizerte, Tunisia. Acta Ichthyol. Piscat. 42:141–49
    [Google Scholar]
  25. 25.  Santander-Neto J, Lessa R 2013. Hermaphroditic smalleyed roundray (Urotrygon microphthalmum) from north-eastern Brazil. Mar. Biodivers. Rec. 6:e60
    [Google Scholar]
  26. 26.  Matta ME 2015. Reproductive biology of the Alaska skate Bathyraja parmifera, with comments on an intersexual individual. J. Fish Biol. 87:664–78
    [Google Scholar]
  27. 27.  Hendon JM, Koester DM, Hoffmayer ER, Driggers WBI, Cicia AM 2013. Occurrence of an intersexual blacktip shark in the northern Gulf of Mexico, with notes on the standardization of classifications for this condition in elasmobranchs. Mar. Coast. Fish. Dyn. Manag. Ecosyst. Sci. 5:174–80
    [Google Scholar]
  28. 28.  Iglésias SP, Sellos DY, Nakaya K 2005. Discovery of a normal hermaphroditic chondrichthyan species: Apristurus longicephalus. J. Fish Biol 66:417–28
    [Google Scholar]
  29. 29.  Betancur RR, Broughton RE, Wiley EO, Carpenter K, López JA et al. 2013. The tree of life and a new classification of bony fishes. PLOS Curr 5. https://doi.org/10.1371/currents.tol.53ba26640df0ccaee75bb165c8c26288
    [Crossref]
  30. 30.  Budgett JS 1901. On some points in the anatomy of Polypterus. . Trans. Zool. Soc. Lond 15:323–38
    [Google Scholar]
  31. 31.  Budgett JS 1902. On the structure of the larval Polypterus. . Trans. Zool. Soc. Lond 16:315–46
    [Google Scholar]
  32. 32.  Ferrara AM, Irwin ER 2001. A standardized procedure for internal sex identification in Lepisosteidae. N. Am. J. Fish. Manag. 21:956–61
    [Google Scholar]
  33. 33.  Wrobel KH 2003. The genus Acipenser as a model for vertebrate urogenital development: the Müllerian duct. Anat. Embryol. 206:255–71
    [Google Scholar]
  34. 34.  Rzepkowska M, Ostaszewska T, Gibala M, Roszko ML 2014. Intersex gonad differentiation in cultured Russian (Acipenser gueldenstaedtii) and Siberian (Acipenser baerii) sturgeon. Biol. Reprod. 90:31
    [Google Scholar]
  35. 35.  Williot P, Brun R, Rouault T, Pelard M, Mercier D, Ludwig A 2005. Artificial spawning in cultured sterlet sturgeon, Acipenser ruthenus L., with special emphasis on hermaphrodites. Aquaculture 246:263–73
    [Google Scholar]
  36. 36.  Henne JP, Ware KM, Wayman WR, Bakal RS, Horváth Á 2006. Synchronous hermaphroditism and self-fertilization in a captive shortnose sturgeon. Trans. Am. Fish. Soc 135:55–60
    [Google Scholar]
  37. 37.  Pfennig F, Standke A, Gutzeit HO 2015. The role of Amh signaling in teleost fish—multiple functions not restricted to the gonads. Gen. Comp. Endocrinol. 223:87–107
    [Google Scholar]
  38. 38.  Hagihara S, Yamashita R, Yamamoto S, Ijiri S, Adachi S 2014. Identification of genes involved in gonadal sex differentiation and the dimorphic expression pattern in undifferentiated gonads of Russian sturgeon Acipenser gueldenstaedtii. J. Appl. Ichthyol 30:1557–64
    [Google Scholar]
  39. 39.  Yue H, Li C, Du H, Zhang S, Wei Q 2015. Sequencing and de novo assembly of the gonadal transcriptome of the endangered Chinese sturgeon (Acipenser sinensis). PLOS ONE 10:e0127332
    [Google Scholar]
  40. 40.  Wang W, Zhu H, Dong Y, Tian Z, Dong T et al. 2017. Dimorphic expression of sex-related genes in different gonadal development stages of sterlet, Acipenser ruthenus, a primitive fish species. Fish. Physiol. Biochem. 43:1557–69
    [Google Scholar]
  41. 41.  Cole KS 2010. Reproduction and Sexuality in Marine Fishes: Patterns and Processes Oakland: Univ. Calif. Press
  42. 42.  Wootton RJ, Smith C 2014. Reproductive Biology of Teleost Fishes Hoboken, NJ: John Wiley & Sons
  43. 43.  Costa FG, Adolfi MC, Gomes CC, Jesus LWO, Batlouni SR, Borella MI 2014. Testes of Astyanax altiparanae: the Sertoli cell functions in a semicystic spermatogenesis. Micron 61:20–27
    [Google Scholar]
  44. 44.  Campuzano-Caballero JC, Uribe MC 2017. Functional morphology of the gonoduct of the viviparous teleost Poeciliopsis gracilis (Heckel, 1848) (Poeciliidae). J. Morphol. 278:1647–55
    [Google Scholar]
  45. 45.  Uribe MC, Grier HJ 2005. Viviparous Fishes Homestead, FL: New Life
  46. 46.  Sadovy de Mitcheson Y, Liu M 2008. Functional hermaphroditism in teleosts. Fish Fish 9:1–43
    [Google Scholar]
  47. 47.  Rodríguez-Mari A, Cañestro C, BreMiller RA, Nguyen-Johnson A, Asakawa K et al. 2010. Sex reversal in zebrafish fancl mutants is caused by Tp53-mediated germ cell apoptosis. PLOS Genet 6:e1001034
    [Google Scholar]
  48. 48.  Mazzoni TS, Grier HJ, Quagio-Grassiotto I 2015. The basement membrane and the sex establishment in the juvenile hermaphroditism during gonadal differentiation of the Gymnocorymbus ternetzi (Teleostei: Characiformes: Characidae). Anat. Rec. 298:1984–2010
    [Google Scholar]
  49. 49.  Warner RR 1984. Mating behavior and hermaphroditism in coral reef fishes. Am. Sci. 72:128–36
    [Google Scholar]
  50. 50.  Chan STH, Yeung WSB 1983. Sex control and sex reversal in fish under natural conditions. Fish Physiology WS Hoar, DJ Randall, EM Donaldson 171–222 Amsterdam: Elsevier
    [Google Scholar]
  51. 51.  Smith CL 1975. The evolution of hermaphroditism in fishes. Intersexuality in the Animal Kingdom R Reinboth, 295–310 Berlin/New York: Springer-Verlag
    [Google Scholar]
  52. 52.  Atz JW 1964. Intersexuality in fishes. Intersexuality in Vertebrates including Man CN Armstrong, AJ Marshall 145–232 New York: Academic
    [Google Scholar]
  53. 53.  Abd-el-Aziz SH, Ramadan AA 1990. Sexuality and hermaphroditism in fishes. I. Synchronous functional hermaphroditism in the serranid fish Serranus scriba L. Folia Morphol 38:86–100
    [Google Scholar]
  54. 54.  Soto CG, Leatherland JF, Noakes DLG 1992. Gonadal histology in the self-fertilizing hermaphroditic fish Rivulus marmoratus (Pisces, Cyprinodontidae). Can. J. Zool. 70:2338–47
    [Google Scholar]
  55. 55.  Capel B 2000. The battle of the sexes. Mech. Dev. 92:89–103
    [Google Scholar]
  56. 56.  Nakamura S, Kobayashi D, Aoki Y, Yokoi H, Ebe Y et al. 2006. Identification and lineage tracing of two populations of somatic gonadal precursors in medaka embryos. Dev. Biol. 295:678–88
    [Google Scholar]
  57. 57.  Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S et al. 2007. The hotei mutation of medaka in the anti-Müllerian hormone receptor causes the dysregulation of germ cell and sexual development. PNAS 104:9691–96
    [Google Scholar]
  58. 58.  Nakamura S, Watakabe I, Nishimura T, Picard JY, Toyoda A et al. 2012. Hyperproliferation of mitotically active germ cells due to defective anti-Müllerian hormone signaling mediates sex reversal in medaka. Development 139:2283–87
    [Google Scholar]
  59. 59.  Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK et al. 2012. A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. PNAS 109:2955–59
    [Google Scholar]
  60. 60.  Yamamoto Y, Zhang Y, Sarida M, Hattori RS, Strussmann CA 2014. Coexistence of genotypic and temperature-dependent sex determination in pejerrey Odontesthes bonariensis. . PLOS ONE 9:e102574
    [Google Scholar]
  61. 61.  Li M, Sun Y, Zhao J, Shi H, Zeng S et al. 2015. A tandem duplicate of anti-Müllerian hormone with a missense SNP on the Y chromosome is essential for male sex determination in Nile tilapia. Oreochromis niloticus. PLOS Genet. 11:e1005678
    [Google Scholar]
  62. 62.  Skaar KS, Nobrega RH, Magaraki A, Olsen LC, Schulz RW, Male R 2011. Proteolytically activated, recombinant anti-Müllerian hormone inhibits androgen secretion, proliferation, and differentiation of spermatogonia in adult zebrafish testis organ cultures. Endocrinology 152:3527–40
    [Google Scholar]
  63. 63.  Nobrega RH, Morais RD, Crespo D, de Waal PP, de Franca LR et al. 2015. Fsh stimulates spermatogonial proliferation and differentiation in zebrafish via Igf3. Endocrinology 156:3804–17
    [Google Scholar]
  64. 64.  Morais R, Crespo D, Nobrega RH, Lemos MS, van de Kant HJG et al. 2017. Antagonistic regulation of spermatogonial differentiation in zebrafish (Danio rerio) by Igf3 and Amh. Mol. Cell. Endocrinol. 454:112–24
    [Google Scholar]
  65. 65.  Lin Q, Mei J, Li Z, Zhang X, Zhou L, Gui JF 2017. Distinct and cooperative roles of amh and dmrt1 in self-renewal and differentiation of male germ cells in zebrafish. Genetics 207:1007–22
    [Google Scholar]
  66. 66.  Miura T, Miura C, Konda Y, Yamauchi K 2002. Spermatogenesis-preventing substance in Japanese eel. Development 129:2689–97
    [Google Scholar]
  67. 67.  Herpin A, Schartl M 2015. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep 16:1260–74
    [Google Scholar]
  68. 68.  Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T et al. 2012. Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosome Res 20:163–76
    [Google Scholar]
  69. 69.  Balch GC, Mackenzie CA, Metcalfe CD 2004. Alterations to gonadal development and reproductive success in Japanese medaka (Oryzias latipes) exposed to 17α-ethinylestradiol. Environ. Toxicol. Chem. 23:782–91
    [Google Scholar]
  70. 70.  Dietrich DR, Krieger HO 2009. Histological Analysis of Endocrine Disruptive Effects in Small Laboratory Fish Hoboken, NJ: John Wiley & Sons
  71. 71.  Wu GC, Chiu PC, Lyu YS, Chang CF 2010. The expression of amh and amhr2 is associated with the development of gonadal tissue and sex change in the protandrous black porgy. Acanthopagrus schlegeli. Biol. Reprod. 83:443–53
    [Google Scholar]
  72. 72.  Wu G-C, Li H-W, Luo J-W, Chen C, Chang C-F 2015. The potential role of Amh to prevent ectopic female development in testicular tissue of the protandrous black porgy. Acanthopagrus schlegelii. Biol. Reprod 92:158
    [Google Scholar]
  73. 73.  Wu G-C, Li H-W, Tey W-G, Lin C-J, Chang C-F 2017. Expression profile of amh/Amh during bi-directional sex change in the protogynous orange-spotted grouper Epinephelus coioides. . PLOS ONE 12:e0185864
    [Google Scholar]
  74. 74.  Wake MH 1986. Urogenital morphology of dipnoans, with comparisons to other fishes and to amphibians. J. Morphol. Suppl. 1:199–216
    [Google Scholar]
  75. 75.  Grafe TU, Linsenmair KE 1989. Protogynous sex change in the reed frog (Hyperolius viridiflavus). Copeia 4:1024–29
    [Google Scholar]
  76. 76.  Eggert C 2004. Sex determination: the amphibian models. Reprod. Nutr. Dev. 44:539–49
    [Google Scholar]
  77. 77.  Gallien LG 1965. Genetic control of sexual differentiation. Organogenesis RL DeHaan, H Ursprung 583–610 New York: Holt, Reinhardt & Winston
    [Google Scholar]
  78. 78.  Witschi E 1929. Studies on the sex differentiation and sex determination in amphibians. III. Rudimentary hermaphroditism and Y chromosome in Rana temporaria. J. Exp. Zool 54:157–223
    [Google Scholar]
  79. 79.  Blackburn DG 1998. Structure, function, and evolution of the oviducts of squamate reptiles, with special reference to viviparity and placentation. J. Exp. Zool. 282:560–617
    [Google Scholar]
  80. 80.  Bull JJ 1980. Sex determination in reptiles. Q. Rev. Biol. 55:3–21
    [Google Scholar]
  81. 81.  Sasanami T, Matsuzaki M, Mizushima S, Hiyama G 2013. Sperm storage in the female reproductive tract in birds. J. Reprod. Dev. 59:334–38
    [Google Scholar]
  82. 82.  Raymond CS, Kettlewell JR, Hirsch B, Bardwell VJ, Zarkower D 1999. Expression of Dmrt1 in the genital ridge of mouse and chicken embryos suggests a role in vertebrate sexual development. Dev. Biol. 215:208–20
    [Google Scholar]
  83. 83.  Teranishi M, Shimada Y, Hori T, Nakabayashi O, Kikuchi T et al. 2001. 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 9:147–65
    [Google Scholar]
  84. 84.  Frankenhuis MT, van Walsum J, de Boer LE, Dieleman SJ, Misdorp W et al. 1990. Triploidy and intersexuality in adult commercial layers. Avian Pathol 19:3–14
    [Google Scholar]
  85. 85.  Lewis PD, Long SE 1992. Incidence of non‐laying in domestic hens. Br. Poultry Sci. 33:289–95
    [Google Scholar]
  86. 86.  Zhao D, McBride D, Nandi S, McQueen HA, McGrew MJ et al. 2010. Somatic sex identity is cell autonomous in the chicken. Nature 464:237–42
    [Google Scholar]
  87. 87.  Renfree MB 1993. Ontogeny, genetic control, and phylogeny of female reproduction in monotreme and therian mammals. Mammal Phylogeny FS Szalay, MJ Novacek, MC McKenna 4–20 New York: Springer
    [Google Scholar]
  88. 88.  Sharman GB, Robinson ES, Walton SM, Berger RJ 1970. Sex chromosomes and reproductive anatomy of some intersexual marsupials. J. Reprod. Fertil. 21:57–68
    [Google Scholar]
  89. 89.  Greene RR, Burrill MW, Ivy AC 1938. Experimental intersexuality: the production of feminized male rats by antenatal treatment with estrogens. Science 88:130–31
    [Google Scholar]
  90. 90.  Koopman P 1999. Sry and Sox9: mammalian testis-determining genes. Cell. Mol. Life Sci. 55:839–56
    [Google Scholar]
  91. 91.  Zhao L, Svingen T, Ng ET, Koopman P 2015. Female-to-male sex reversal in mice caused by transgenic overexpression of Dmrt1. . Development 142:1083–88
    [Google Scholar]
  92. 92.  Jost A 1953. Problems of fetal endocrinology: the gonadal and hypophyseal hormones. Recent Prog. Horm. Res. 8:379–418
    [Google Scholar]
  93. 93.  Jost A 1972. A new look at the mechanisms controlling sex differentiation in mammals. Johns Hopkins Med. J. 130:38–53
    [Google Scholar]
  94. 94.  Biscotti MA, Adolfi MC, Barucca M, Forconi M, Pallavicini A et al. 2018. A comparative view on sex differentiation and gametogenesis genes in lungfish and coelacanths. Genome Biol. Evol. 10:61430–44
    [Google Scholar]
  95. 95.  Piprek RP, Pecio A, Laskowska-Kaszub K, Kubiak JZ, Szymura JM 2013. Sexual dimorphism of AMH, DMRT1 and RSPO1 localization in the developing gonads of six anuran species. Int. J. Dev. Biol. 57:891–95
    [Google Scholar]
  96. 96.  Jansson E, Mattsson A, Goldstone J, Berg C 2016. Sex-dependent expression of anti-Müllerian hormone (amh) and amh receptor 2 during sex organ differentiation and characterization of the Müllerian duct development in Xenopus tropicalis. Gen. Comp. . Endocrinol 229:132–44
    [Google Scholar]
  97. 97.  Al-Asaad I, Chardard D, di Clemente N, Picard JY, Dumond H et al. 2013. Müllerian inhibiting substance in the caudate amphibian Pleurodeles waltl. . Endocrinology 154:3931–36
    [Google Scholar]
  98. 98.  Radhakrishnan S, Literman R, Neuwald J, Severin A, Valenzuela N 2017. Transcriptomic responses to environmental temperature by turtles with temperature-dependent and genotypic sex determination assessed by RNAseq inform the genetic architecture of embryonic gonadal development. PLOS ONE 12:e0172044
    [Google Scholar]
  99. 99.  Western PS, Harry JL, Graves JA, Sinclair AH 1999. Temperature-dependent sex determination in the American alligator: AMH precedes SOX9 expression. Dev. Dyn. 216:411–19
    [Google Scholar]
  100. 100.  Urushitani H, Katsu Y, Miyagawa S, Kohno S, Ohta Y et al. 2011. Molecular cloning of anti-Müllerian hormone from the American alligator, Alligator mississippiensis. Mol. Cell. Endocrinol. 333:190–99
    [Google Scholar]
  101. 101.  Durando M, Cocito L, Rodríguez HA, Varayoud J, Ramos JG et al. 2013. Neonatal expression of amh, sox9 and sf-1 mRNA in Caiman latirostris and effects of in ovo exposure to endocrine disrupting chemicals. Gen. Comp. Endocrinol. 191:31–38
    [Google Scholar]
  102. 102.  Oreal E, Pieau C, Mattei MG, Josso N, Picard JY et al. 1998. Early expression of AMH in chicken embryonic gonads precedes testicular SOX9 expression. Dev. Dyn. 212:522–32
    [Google Scholar]
  103. 103.  Lambeth LS, Ayers K, Cutting AD, Doran TJ, Sinclair AH, Smith CA 2015. Anti-Müllerian hormone is required for chicken embryonic urogenital system growth but not sexual differentiation. Biol. Reprod. 93:138
    [Google Scholar]
  104. 104.  Lambeth LS, Morris K, Ayers KL, Wise TG, O'Neil T et al. 2016. Overexpression of anti-Müllerian hormone disrupts gonadal sex differentiation, blocks sex hormone synthesis, and supports cell autonomous sex development in the chicken. Endocrinology 157:1258–75
    [Google Scholar]
  105. 105.  Cutting AD, Ayers K, Davidson N, Oshlack A, Doran T et al. 2014. Identification, expression, and regulation of anti-Müllerian hormone type-II receptor in the embryonic chicken gonad. Biol. Reprod. 90:106
    [Google Scholar]
  106. 106.  Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A et al. 2014. Origins and functional evolution of Y chromosomes across mammals. Nature 508:488–93
    [Google Scholar]
  107. 107.  Pask AJ, Calatayud NE, Shaw G, Wood WM, Renfree MB 2010. Oestrogen blocks the nuclear entry of SOX9 in the developing gonad of a marsupial mammal. BMC Biol 8:113
    [Google Scholar]
  108. 108.  Juengel JL, Whale LJ, Wylde KA, Greenwood P, McNatty KP, Eckery DC 2002. Expression of anti-Müllerian hormone mRNA during gonadal and follicular development in the brushtail possum (Trichosurus vulpecula). Reprod. Fertil Dev. 14:345–53
    [Google Scholar]
  109. 109.  Tran D, Muesy-Dessole N, Josso N 1977. Anti-Müllerian hormone is a functional marker of foetal Sertoli cells. Nature 269:411–12
    [Google Scholar]
  110. 110.  Tran D, Meusy-Dessolle N, Josso N 1981. Waning of anti-Müllerian activity: an early sign of Sertoli cell maturation in the developing pig. Biol. Reprod. 24:923–31
    [Google Scholar]
  111. 111.  Josso N, Legeai L, Forest MG, Chaussain JL, Brauner R 1990. An enzyme linked immunoassay for anti-Müllerian hormone: a new tool for the evaluation of testicular function in infants and children. J. Clin. Endocrinol. Metab. 70:23–27
    [Google Scholar]
  112. 112.  Rey R, Lordereau-Richard I, Carel JC, Barbet P, Cate RL et al. 1993. Anti-Müllerian hormone and testosterone serum levels are inversely during normal and precocious pubertal development. J. Clin. Endocrinol. Metab. 77:1220–26
    [Google Scholar]
  113. 113.  Rey R, Mebarki F, Forest MG, Mowszowicz I, Cate RL et al. 1994. Anti-Müllerian hormone in children with androgen insensitivity. J. Clin. Endocrinol. Metab. 79:960–64
    [Google Scholar]
  114. 114.  Rey R, al-Attar L, Louis F, Jaubert F, Barbet P et al. 1996. Testicular dysgenesis does not affect expression of anti-Müllerian hormone by Sertoli cells in premeiotic seminiferous tubules. Am. J. Pathol. 148:1689–98
    [Google Scholar]
  115. 115.  Vigier B, Picard JY, Tran D, Legeai L, Josso N 1984. Production of anti-Müllerian hormone: another homology between Sertoli and granulosa cells. Endocrinology 114:1315–20
    [Google Scholar]
  116. 116.  Ueno S, Takahashi M, Manganaro TF, Ragin RC, Donahoe PK 1989. Cellular localization of Müllerian inhibiting substance in the developing rat ovary. Endocrinology 124:1000–6
    [Google Scholar]
  117. 117.  Hirobe S, He WW, Lee MM, Donahoe PK 1992. Müllerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity. Endocrinology 131:854–62
    [Google Scholar]
  118. 118.  Hoegg S, Brinkmann H, Taylor JS, Meyer A 2004. Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish. J. Mol. Evol. 59:190–203
    [Google Scholar]
  119. 119.  Clarke JT, Lloyd GT, Friedman M 2016. Little evidence for enhanced phenotypic evolution in early teleosts relative to their living fossil sister group. PNAS 113:11531–36
    [Google Scholar]
  120. 120.  Devlin R, Nagahama Y 2002. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208:191–364
    [Google Scholar]
  121. 121.  Davies JA 2002. Morphogenesis of the metanephric kidney. ScientificWorldJournal 2:1937–50
    [Google Scholar]
  122. 122.  Klekamp M, Prahlad KV, Hampel AE 1983. Amphibian egg jelly coat and fertilization envelope: involvement in sodium-dependent amino acid transport. Comp. Biochem. Physiol. 76:357–62
    [Google Scholar]
  123. 123.  Jamieson BGM 2011. Fish Evolution and Systematics: Evidence from Spermatozoa Cambridge, UK: Cambridge Univ. Press
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