Abstract
The sex of an individual is determined by the type of reproductive organs that they have, i.e., testes or ovaries. These reproductive organs originate from bipotential gonads. Therefore, sex is determined by the direction of gonadal development of a bipotential gonad, which can develop into either a testis or an ovary. Various strategies to determine the sex of a gonad are found in fish, and these strategies range from gonochorism, in which ovaries or testes are developed in different individuals, to sequential hermaphroditism including protogyny, protandry, and bidirectional sex change, and synchronous hermaphroditism. In gonochoristic species, the direction of gonadal development must be decided at a specific time. Regarding the timing, a cue establishes the bifurcation point, and the cue is either a genetic or an environmental factor. To describe how these cues control sex differentiation, this chapter focuses on gonochoristic fish. This chapter first describes the sex-determining genes (i.e., genetic cues) in fish and then summarizes gonadal development including sex reversals induced by non-genomic factors (environmental cues) and genomic factors.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Baker BS, Ridge KA (1980) Sex and the single cell. I. On the action of major loci affecting sex determination in Drosophila melanogaster. Genetics 94(2):383–423
Bellefroid EJ, Leclere L, Saulnier A, Keruzore M, Sirakov M, Vervoort M, De Clercq S (2013) Expanding roles for the evolutionarily conserved Dmrt sex transcriptional regulators during embryogenesis. Cell Mol Life Sci 70(20):3829–3845. https://doi.org/10.1007/s00018-013-1288-2
Bylund M, Andersson E, Novitch BG, Muhr J (2003) Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 6(11):1162–1168. https://doi.org/10.1038/nn1131
Conover DO, Fleisher MK (1986) Temperature-sensitive period of sex determination in the Atlantic silverside, Menidia menidia. Can J Fish Aquat Sci 43(3):514–520
Conover DO, Heins SW (1987) Adaptive variation in environmental and genetic sex determination in a fish. Nature 326(6112):496–498. https://doi.org/10.1038/326496a0
Dai X, Jin X, Chen X, He J, Yin Z (2015) Sufficient numbers of early germ cells are essential for female sex development in zebrafish. PLoS One 10(2):e0117824. https://doi.org/10.1371/journal.pone.0117824
Dee CT, Hirst CS, Shih YH, Tripathi VB, Patient RK, Scotting PJ (2008) Sox3 regulates both neural fate and differentiation in the zebrafish ectoderm. Dev Biol 320(1):289–301. https://doi.org/10.1016/j.ydbio.2008.05.542
Fernandino JI, Hattori RS, Moreno Acosta OD, Strussmann CA, Somoza GM (2013) Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen Comp Endocrinol 192:36–44. https://doi.org/10.1016/j.ygcen.2013.05.024
Guiguen Y, Fostier A, Piferrer F, Chang CF (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165(3):352–366. https://doi.org/10.1016/j.ygcen.2009.03.002
Hamaguchi S, Toyazaki Y, Shinomiya A, Sakaizumi M (2004) The XX-XY sex-determination system in Oryzias luzonensis and O. mekongensis revealed by the sex ratio of the progeny of sex-reversed fish. Zool Sci 21(10):1015–1018
Hattori RS, Gould RJ, Fujioka T, Saito T, Kurita J, Strussmann CA, Yokota M, Watanabe S (2007) Temperature-dependent sex determination in Hd-rR medaka Oryzias latipes: gender sensitivity, thermal threshold, critical period, and DMRT1 expression profile. Sex Dev 1(2):138–146. https://doi.org/10.1159/000100035
Hattori RS, Oura M, Sakamoto T, Yokota M, Watanabe S, Strussmann CA (2010) Establishment of a strain inheriting a sex-linked SNP marker in Patagonian pejerrey (Odontesthes hatcheri), a species with both genotypic and temperature-dependent sex determination. Anim Genet 41(1):81–84. https://doi.org/10.1111/j.1365-2052.2009.01948.x
Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strussmann CA (2012) A Y-linked anti-Mullerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci U S A 109(8):2955–2959. https://doi.org/10.1073/pnas.1018392109
Hayashi Y, Kobira H, Yamaguchi T, Shiraishi E, Yazawa T, Hirai T, Kamei Y, Kitano T (2010) High temperature causes masculinization of genetically female medaka by elevation of cortisol. Mol Reprod Dev 77(8):679–686. https://doi.org/10.1002/mrd.21203
Imai T, Saino K, Matsuda M (2015) Mutation of Gonadal soma-derived factor induces medaka XY gonads to undergo ovarian development. Biochem Biophys Res Commun 467:109–114. https://doi.org/10.1016/j.bbrc.2015.09.112
Jiang T, Hou CC, She ZY, Yang WX (2013) The SOX gene family: function and regulation in testis determination and male fertility maintenance. Mol Biol Rep 40(3):2187–2194. https://doi.org/10.1007/s11033-012-2279-3
Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N, Fujita M, Suetake H, Suzuki S, Hosoya S, Tohari S, Brenner S, Miyadai T, Venkatesh B, Suzuki Y, Kikuchi K (2012) A trans-species missense SNP in Amhr2 is associated with sex determination in the tiger pufferfish, Takifugu rubripes (fugu). PLoS Genet 8(7):e1002798. https://doi.org/10.1371/journal.pgen.1002798
Kitano T, Hayashi Y, Shiraishi E, Kamei Y (2012) Estrogen rescues masculinization of genetically female medaka by exposure to cortisol or high temperature. Mol Reprod Dev 79(10):719–726. https://doi.org/10.1002/mrd.22080
Kobayashi T, Nagahama Y (2009) Molecular aspects of gonadal differentiation in a teleost fish, the Nile tilapia. Sex Dev 3(2–3):108–117. https://doi.org/10.1159/000223076
Kobayashi T, Matsuda M, Kajiura-Kobayashi H, Suzuki A, Saito N, Nakamoto M, Shibata N, Nagahama Y (2004) Two DM domain genes, DMY and DMRT1, involved in testicular differentiation and development in the medaka, Oryzias latipes. Dev Dyn 231(3):518–526. https://doi.org/10.1002/dvdy.20158
Kobayashi T, Kajiura-Kobayashi H, Guan G, Nagahama Y (2008) Sexual dimorphic expression of DMRT1 and Sox9a during gonadal differentiation and hormone-induced sex reversal in the teleost fish Nile tilapia (Oreochromis niloticus). Dev Dyn 237(1):297–306. https://doi.org/10.1002/dvdy.21409
Kondo M, Nanda I, Hornung U, Asakawa S, Shimizu N, Mitani H, Schmid M, Shima A, Schartl M (2003) Absence of the candidate male sex-determining gene dmrt1b(Y) of medaka from other fish species. Curr Biol 13(5):416–420
Kondo M, Nanda I, Hornung U, Schmid M, Schartl M (2004) Evolutionary origin of the medaka Y chromosome. Curr Biol 14(18):1664–1669. https://doi.org/10.1016/j.cub.2004.09.026
Kondo M, Hornung U, Nanda I, Imai S, Sasaki T, Shimizu A, Asakawa S, Hori H, Schmid M, Shimizu N, Schartl M (2006) Genomic organization of the sex-determining and adjacent regions of the sex chromosomes of medaka. Genome Res 16(7):815–826. https://doi.org/10.1101/gr.5016106
Koopman P, Gubbay J, Vivian N, Goodfellow P, Lovell-Badge R (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351(6322):117–121. https://doi.org/10.1038/351117a0
Koshimizu E, Strussmann CA, Okamoto N, Fukuda H, Sakamoto T (2010) Construction of a genetic map and development of DNA markers linked to the sex-determining locus in the Patagonian pejerrey (Odontesthes hatcheri). Mar Biotechnol (NY) 12(1):8–13. https://doi.org/10.1007/s10126-009-9194-1
Koster RW, Kuhnlein RP, Wittbrodt J (2000) Ectopic Sox3 activity elicits sensory placode formation. Mech Dev 95(1–2):175–187
Kurokawa H, Aoki Y, Nakamura S, Ebe Y, Kobayashi D, Tanaka M (2006) Time-lapse analysis reveals different modes of primordial germ cell migration in the medaka Oryzias latipes. Develop Growth Differ 48(3):209–221. https://doi.org/10.1111/j.1440-169X.2006.00858.x
Kurokawa H, Saito D, Nakamura S, Katoh-Fukui Y, Ohta K, Baba T, Morohashi K, Tanaka M (2007) Germ cells are essential for sexual dimorphism in the medaka gonad. Proc Natl Acad Sci U S A 104(43):16958–16963. https://doi.org/10.1073/pnas.0609932104
Li MH, Yang HH, Li MR, Sun YL, Jiang XL, Xie QP, Wang TR, Shi HJ, Sun LN, Zhou LY, Wang DS (2013) Antagonistic roles of Dmrt1 and Foxl2 in sex differentiation via estrogen production in tilapia as demonstrated by TALENs. Endocrinology 154(12):4814–4825. https://doi.org/10.1210/en.2013-1451
Maack G, Segner H (2004) Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp Biochem Physiol C Toxicol Pharmacol 139(1–3):47–55. https://doi.org/10.1016/j.cca.2004.09.004
Mankiewicz JL, Godwin J, Holler BL, Turner PM, Murashige R, Shamey R, Daniels HV, Borski RJ (2013) Masculinizing effect of background color and cortisol in a flatfish with environmental sex-determination. Integr Comp Biol 53(4):755–765. https://doi.org/10.1093/icb/ict093
Martinez P, Vinas AM, Sanchez L, Diaz N, Ribas L, Piferrer F (2014) Genetic architecture of sex determination in fish: applications to sex ratio control in aquaculture. Front Genet 5:340. https://doi.org/10.3389/fgene.2014.00340
Masuyama H, Yamada M, Kamei Y, Fujiwara-Ishikawa T, Todo T, Nagahama Y, Matsuda M (2012) Dmrt1 mutation causes a male-to-female sex reversal after the sex determination by Dmy in the medaka. Chromosom Res 20(1):163–176. https://doi.org/10.1007/s10577-011-9264-x
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T, Morrey CE, Shibata N, Asakawa S, Shimizu N, Hori H, Hamaguchi S, Sakaizumi M (2002) DMY is a Y-specific DM-domain gene required for male development in the medaka fish. Nature 417(6888):559–563. https://doi.org/10.1038/nature751
Matsuda M, Sato T, Toyazaki Y, Nagahama Y, Hamaguchi S, Sakaizumi M (2003) Oryzias curvinotus has DMY, a gene that is required for male development in the medaka, O. latipes. Zool Sci 20(2):159–161
Morinaga C, Tomonaga T, Sasado T, Suwa H, Niwa K, Yasuoka A, Henrich T, Watanabe T, Deguchi T, Yoda H, Hirose Y, Iwanami N, Kunimatsu S, Okamoto Y, Yamanaka T, Shinomiya A, Tanaka M, Kondoh H, Furutani-Seiki M (2004) Mutations affecting gonadal development in Medaka, Oryzias latipes. Mech Dev 121(7–8):829–839. https://doi.org/10.1016/j.mod.2004.03.025
Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N, Mitani H, Furutani-Seiki M, Tanaka M, Kondoh H (2007) The hotei mutation of medaka in the anti-Mullerian hormone receptor causes the dysregulation of germ cell and sexual development. Proc Natl Acad Sci U S A 104(23):9691–9696. https://doi.org/10.1073/pnas.0611379104
Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A, Naruse K, Hamaguchi S, Sakaizumi M (2012) Tracing the emergence of a novel sex-determining gene in medaka, Oryzias luzonensis. Genetics 191(1):163–170. https://doi.org/10.1534/genetics.111.137497
Nakamoto M, Muramatsu S, Yoshida S, Matsuda M, Nagahama Y, Shibata N (2009) Gonadal sex differentiation and expression of Sox9a2, Dmrt1, and Foxl2 in Oryzias luzonensis. Genesis 47(5):289–299. https://doi.org/10.1002/dvg.20498
Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A, Shan Z, Haaf T, Shimizu N, Shima A, Schmid M, Schartl M (2002) A duplicated copy of DMRT1 in the sex-determining region of the Y chromosome of the medaka, Oryzias latipes. Proc Natl Acad Sci U S A 99(18):11778–11783. https://doi.org/10.1073/pnas.182314699
Nanda I, Hornung U, Kondo M, Schmid M, Schartl M (2003) Common spontaneous sex-reversed XX males of the medaka Oryzias latipes. Genetics 163(1):245–251
Ospina-Alvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS One 3(7):e2837. https://doi.org/10.1371/journal.pone.0002837
Otake H, Shinomiya A, Matsuda M, Hamaguchi S, Sakaizumi M (2006) Wild-derived XY sex-reversal mutants in the Medaka, Oryzias latipes. Genetics 173(4):2083–2090. https://doi.org/10.1534/genetics.106.058941
Otake H, Masuyama H, Mashima Y, Shinomiya A, Myosho T, Nagahama Y, Matsuda M, Hamaguchi S, Sakaizumi M (2010) Heritable artificial sex chromosomes in the medaka, Oryzias latipes. Heredity (Edinb) 105(3):247–256. https://doi.org/10.1038/hdy.2009.174
Phillips RB (2013) Evolution of the sex chromosomes in salmonid fishes. Cytogenet Genome Res 141(2–3):177–185. https://doi.org/10.1159/000355149
Phillips RB, Morasch MR, Park LK, Naish KA, Devlin RH (2005) Identification of the sex chromosome pair in coho salmon (Oncorhynchus kisutch): lack of conservation of the sex linkage group with chinook salmon (Oncorhynchus tshawytscha). Cytogenet Genome Res 111(2):166–170. https://doi.org/10.1159/000086387
Phillips RB, DeKoning J, Morasch MR, Park LK, Devlin RH (2007) Identification of the sex chromosome pair in chum salmon (Oncorhynchus keta) and pink salmon (Oncorhynchus gorbuscha). Cytogenet Genome Res 116(4):298–304. https://doi.org/10.1159/000100414
Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197:229–281
Rizzoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, Lovell-Badge R (2004) SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat Genet 36(3):247–255. https://doi.org/10.1038/ng1309
Saito D, Tanaka M (2009) Comparative aspects of gonadal sex differentiation in medaka: a conserved role of developing oocytes in sexual canalization. Sex Dev 3(2–3):99–107. https://doi.org/10.1159/000223075
Sato T, Endo T, Yamahira K, Hamaguchi S, Sakaizumi M (2005) Induction of female-to-male sex reversal by high temperature treatment in Medaka, Oryzias latipes. Zool Sci 22(9):985–988
Sato T, Suzuki A, Shibata N, Sakaizumi M, Hamaguchi S (2008) The novel mutant scl of the medaka fish, Oryzias latipes, shows no secondary sex characters. Zool Sci 25(3):299–306. https://doi.org/10.2108/zsj.25.299
Sawatari E, Shikina S, Takeuchi T, Yoshizaki G (2007) A novel transforming growth factor-beta superfamily member expressed in gonadal somatic cells enhances primordial germ cell and spermatogonial proliferation in rainbow trout (Oncorhynchus mykiss). Dev Biol 301(1):266–275. https://doi.org/10.1016/j.ydbio.2006.10.001
Shen MM, Hodgkin J (1988) mab-3, a gene required for sex-specific yolk protein expression and a male-specific lineage in C. elegans. Cell 54(7):1019–1031
Shibata Y, Paul-Prasanth B, Suzuki A, Usami T, Nakamoto M, Matsuda M, Nagahama Y (2010) Expression of gonadal soma derived factor (GSDF) is spatially and temporally correlated with early testicular differentiation in medaka. Gene Expr Patterns 10(6):283–289. https://doi.org/10.1016/j.gep.2010.06.005
Shinomiya A, Otake H, Togashi K, Hamaguchi S, Sakaizumi M (2004) Field survey of sex-reversals in the medaka, Oryzias latipes: genotypic sexing of wild populations. Zool Sci 21(6):613–619
Shinomiya A, Otake H, Hamaguchi S, Sakaizumi M (2010) Inherited XX sex reversal originating from wild medaka populations. Heredity (Edinb) 105(5):443–448. https://doi.org/10.1038/hdy.2010.51
Siegfried KR, Nusslein-Volhard C (2008) Germ line control of female sex determination in zebrafish. Dev Biol 324(2):277–287. https://doi.org/10.1016/j.ydbio.2008.09.025
Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ, Foster JW, Frischauf AM, Lovell-Badge R, Goodfellow PN (1990) A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346(6281):240–244. https://doi.org/10.1038/346240a0
Strüssmann CA, Moriyama S, Hanke EF, Calsina Cota JC, Takashima F (1996) Evidence of thermolabile sex determination in pejerrey. J Fish Biol 48:643–651
Takehana Y (2011) Frequent turnover of sex chromosomes in the medaka fishes. In: Naruse K, Tanaka M, Takeda H (eds) Medaka a model for organogenesis, human disease, and evolution. Springer, Tokyo, pp 229–240
Takehana Y, Naruse K, Sakaizumi M (2005) Molecular phylogeny of the medaka fishes genus Oryzias (Beloniformes: Adrianichthyidae) based on nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 36(2):417–428. https://doi.org/10.1016/j.ympev.2005.01.016
Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin IT, Kohara Y, Kuroki Y, Toyoda A, Fujiyama A, Hamaguchi S, Sakaizumi M, Naruse K (2014) Co-option of Sox3 as the male-determining factor on the Y chromosome in the fish Oryzias dancena. Nat Commun 5:4157. https://doi.org/10.1038/ncomms5157
Tanaka K, Takehana Y, Naruse K, Hamaguchi S, Sakaizumi M (2007) Evidence for different origins of sex chromosomes in closely related Oryzias fishes: substitution of the master sex-determining gene. Genetics 177(4):2075–2081. https://doi.org/10.1534/genetics.107.075598
Volff JN, Kondo M, Schartl M (2003) Medaka dmY/dmrt1Y is not the universal primary sex-determining gene in fish. Trends Genet 19(4):196–199. https://doi.org/10.1016/S0168-9525(03)00051-9
Woram RA, Gharbi K, Sakamoto T, Hoyheim B, Holm LE, Naish K, McGowan C, Ferguson MM, Phillips RB, Stein J, Guyomard R, Cairney M, Taggart JB, Powell R, Davidson W, Danzmann RG (2003) Comparative genome analysis of the primary sex-determining locus in salmonid fishes. Genome Res 13(2):272–280
Yamamoto T (1953) Artificially induced sex-reversal in genotypic males of the medaka (Oryzias latipes). J Exp Zool A Ecol Genet Physiol 123:571–594
Yamamoto T (1958) Artificial induction of functional sex-reversal in genotypic females of the medaka (Oryzias latipes). J Exp Zool 137(2):227–263
Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C, Cabau C, Bouchez O, Fostier A, Guiguen Y (2012) An immune-related gene evolved into the master sex-determining gene in rainbow trout, Oncorhynchus mykiss. Curr Biol 22(15):1423–1428. https://doi.org/10.1016/j.cub.2012.05.045
Yano A, Nicol B, Jouanno E, Quillet E, Fostier A, Guyomard R, Guiguen Y (2013) The sexually dimorphic on the Y-chromosome gene (sdY) is a conserved male-specific Y-chromosome sequence in many salmonids. Evol Appl 6(3):486–496. https://doi.org/10.1111/eva.12032
Yano A, Nicol B, Jouanno E, Guiguen Y (2014) Heritable targeted inactivation of the rainbow trout (Oncorhynchus mykiss) master sex-determining gene using zinc-finger nucleases. Mar Biotechnol (NY) 16(2):243–250. https://doi.org/10.1007/s10126-013-9546-8
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Japan KK, part of Springer Nature
About this chapter
Cite this chapter
Matsuda, M. (2018). Genetic Control of Sex Determination and Differentiation in Fish. In: Kobayashi, K., Kitano, T., Iwao, Y., Kondo, M. (eds) Reproductive and Developmental Strategies. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56609-0_14
Download citation
DOI: https://doi.org/10.1007/978-4-431-56609-0_14
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-56607-6
Online ISBN: 978-4-431-56609-0
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)