Abstract
Teleost fishes are the most speciose group of vertebrate animals, and their study has been fundamental to understanding the mechanisms underlying sex determination, development, physiology, and evolution. Teleosts display extraordinary diversity in a variety of phenotypes, with sexual patterns and determination mechanisms being no exception. Sexual patterns range from familiar male–female gonochorism to various forms of hermaphroditism, including systems where individuals undergo functional sex change over their life cycle, or are capable of self-fertilization. There is also considerable variety in how gonochoristic species determine sex, with mechanisms using social, environmental, and genetic inputs to direct sexual development. Within genetic sex determination systems, there is additional diversity, with monogenic and polygenic systems found in various chromosomal contexts. Here, we review the above diversity and describe how it has revealed broad mechanistic and evolutionary insights into sexual phenotypes. We further discuss why fish display such amazing diversity in sex determination systems and how the necessary evolutionary transitions producing that diversity may have taken place.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Albertson RC, Powder KE, Hu Y, Coyle KP, Roberts RB, Parsons KJ (2014) Genetic basis of continuous variation in the levels and modular inheritance of pigmentation in cichlid fishes. Mol Ecol 23(21):5135–5150. https://doi.org/10.1111/mec.12900
Arnold AP, Breedlove SM (1985) Organizational and activational effects of sex steroids on brain and behavior: a reanalysis. Horm Behav 19:469–498
Asoh K (2003) Reproductive parameters of female Hawaiian damselfish Dascyllus albisella with comparison to other tropical and subtropical damselfishes. Mar Biol 143(4):803–810
Asoh K (2005) Gonadal development and diandric protogyny in two populations of Dascyllus reticulatus from Madang, Papua New Guinea. J Fish Biol 66(4):1127–1148
Atz JW (1964) Intersexuality in fishes. In: Armstrong CN, Marshall AJ (eds) Intersexuality in vertebrates including man. Academic, New York, pp 145–224
Avise JC (2015) Evolutionary perspectives on clonal reproduction in vertebrate animals. PNAS 112(29):8867–8873
Baroiller JF, D’Cotta H, Saillant E (2009) Environmental effects on fish sex determination and differentiation. Sex Dev 3(2–3):118–135. https://doi.org/10.1159/000223077
Behringer RR, Finegold MJ, Cate RL (1994) Müllerian-inhibiting substance function during mammalian sexual development. Cell 79(3):415–425
Black MP, Balthazart J, Baillien M, Grober MS (2005) Socially induced and rapid increases in aggression are inversely related to brain aromatase activity in a sex-changing fish, Lythrypnus dalli. Proc R Soc B: Biol Sci 272(1579):2435–2440. https://doi.org/10.1098/rspb.2005.3210
Black MP, Balthazart J, Baillien M, Grober MS (2011) Rapid increase in aggressive behavior precedes the decrease in brain aromatase activity during socially mediated sex change in Lythrypnus dalli. Gen Comp Endocrinol 170(1):119–124. https://doi.org/10.1016/j.ygcen.2010.09.019
Blaser O, Neuenschwander S, Perrin N (2011) On the maintenance of sex chromosome polymorphism by sex-antagonistic selection. Am Nat 178(4):515–524. https://doi.org/10.1086/661895
Blaser O, Grossen C, Neuenschwander S, Perrin N (2013) Sex-chromosome turnovers induced by deleterious mutation load. Evol Int J Org Evol 67(3):635–645. https://doi.org/10.1111/j.1558-5646.2012.01810.x
Böhne A, Wilson CA, Postlethwait JH, Salzburger W (2016) Variations of a theme: genomics of sex determination in the cichlid fish Astatotilapia burtoni. BMC Genomics. https://doi.org/10.1186/s12864-016-3178-0
Brantley RK, Wingfield JC, Bass AH (1993) Sex steroid levels in Porichthys notatus, a fish with alternative reproductive tactics, and a review of the hormonal bases for male dimorphism among teleost fishes. Horm Behav 27(3):332–347. https://doi.org/10.1006/hbeh.1993.1025
Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin/Cummings, Advanced Book Program
Camacho JPM, Sharbel TF, Beukeboom LW (2000) B chromosome evolution. Philos Trans R Soc Lond B 355:163–178
Cardwell JR, Liley NR (1991a) Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride. Gen Comp Endocrinol 81(1):7–20
Cardwell JR, Liley NR (1991b) Androgen control of social status in males of a wild population of stoplight parrotfish, Sparisoma viride (Scaridae). Horm Behav 25(1):1–18. https://doi.org/10.1016/0018-506x(91)90035-g
Charlesworth B, Charlesworth D (2000) The degeneration of Y chromosomes. Philos Trans R Soc Lond Ser B, Biol Sci 355(1403):1563–1572. https://doi.org/10.1098/rstb.2000.0717
Chen S, Zhang G, Shao C, Huang Q, Liu G, Zhang P et al (2014) Whole-genome sequence of a flatfish provides insights into ZW sex chromosome evolution and adaptation to a benthic lifestyle. Nat Genet 46(3):253–260. https://doi.org/10.1038/ng.2890
Chen S, Zhang H, Wang F, Zhang W, Peng G (2016) nr0b1 (DAX1) mutation in zebrafish causes female-to-male sex reversal through abnormal gonadal proliferation and differentiation. Mol Cell Endocrinol 433:105–116. https://doi.org/10.1016/j.mce.2016.06.005
Clark FE, Conte MA, Ferreira-Bravo IA, Poletto AB, Martins C, Kocher TD (2016) Dynamic sequence evolution of a sex-associated b chromosome in Lake Malawi Cichlid Fish. J Heredity. https://doi.org/10.1093/jhered/esw059
Cole KS, Shapiro DY (1995) Social facilitation and sensory mediation of adult sex change in a cryptic, benthic marine goby. J Exp Mar Biol Ecol 186(1):65–75
Conover DO, Fleisher MH (1986) Temperature-sensitive period of sex determination in the Atlantic Silverside, Menidia menidia. Can J Fish Aquat Sci 43(3):514–520. https://doi.org/10.1139/f86-061
Cortez D, Marin R, Toledo-Flores D, Froidevaux L, Liechti A, Waters PD et al (2014) Origins and functional evolution of Y chromosomes across mammals. Nature 508(7497):488–493. https://doi.org/10.1038/nature13151
de Mitcheson YS, Liu M (2008) Functional hermaphroditism in teleosts. Fish Fish 9:1–43
Devlin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208(3):191–364. https://doi.org/10.1016/S0044-8486(02)00057-1
Duffy TA, Hice LA, Conover DO (2015) Pattern and scale of geographic variation in environmental sex determination in the Atlantic silverside, Menidia menidia. Evolution 69(8):2187–2195. https://doi.org/10.1111/evo.12724
Eisbrenner WD, Botwright N, Cook M, Davidson EA, Dominik S, Elliott NG et al (2014) Evidence for multiple sex-determining loci in Tasmanian Atlantic salmon (Salmo salar). Heredity 113(1):86–92. https://doi.org/10.1038/hdy.2013.55
Fernandino JI, Hattori RS, Kishii A, Strussmann CA, Somoza GM (2012) The cortisol and androgen pathways cross talk in high temperature-induced masculinization: the 11β-hydroxysteroid dehydrogenase as a key enzyme. Endocrinology 153:6003–6011
Fischer EA (1980) The relationship between mating system and simultaneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae). Anim Behav 28(2):620–633. https://doi.org/10.1016/S0003-3472(80)80070-4
Fischer EA (1984) Local mate competition and sex allocation in simultaneous hermaphrodites. Am Nat 124(4):590–596. https://doi.org/10.1086/284298
Forconi M, Canapa A, Barucca M, Biscotti MA, Capriglione T, Buonocore F, Fausto AM, Makapedua DM, Pallavicini A, Gerdol M, De Moro G, Scapigliati G, Olmo E, Schartl M (2013) Characterization of sex determination and sex differentiation genes in Latimeria. PLoS One 8(4):e56006
Forlano PM, Schlinger BA, Bass AH (2006) Brain aromatase: new lessons from non-mammalian model systems. Front Neuroendocrinol 27(3):247–274. https://doi.org/10.1016/j.yfrne.2006.05.002
Fowler BLS, Buonaccorsi VP (2016) Genomic characterization of sex-identification markers in Sebastes carnatus and Sebastes chrysomelas rockfishes. Mol Ecol 25(10):2165–2175. https://doi.org/10.1111/mec.13594
Francis RC (1992) Sexual lability in teleosts – developmental factors. Q Rev Biol 67:1–18
Francis RC, Barlow GW (1993) Social control of primary sex differentiation in the Midas cichlid. Proc Natl Acad Sci 90(22):10673–10675
Fricke HW (1983) Social control of sex: field experiments with the anemonefish Amphiprion bicinctus. Z Teirpsychol 61:71–77
Fricke HW, Fricke S (1977) Monogamy and sex change by aggressive dominance in coral reef fish. Nature 266:830–832
Fricke HW, Holzberg S (1974) Scial units and hermaphroditism in a pomacentrid fish. Natuwissenschaften 61:367–368
Frisch A, Walker S, McCormick M, Solomon-Lane T (2007) Regulation of protogynous sex change by competition between corticosteroids and androgens: An experimental test using sandperch, Parapercis cylindrica. Horm Behav 52(4):540–545. https://doi.org/10.1016/j.yhbeh.2007.07.008
Furman BLS, Evans BJ (2016) Sequential Turnovers of sex chromosomes in African Clawed Frogs (Xenopus) suggest some genomic regions are good at sex determination. G3 (Bethesda, Md). https://doi.org/10.1534/g3.116.033423
Gautier A, Le Gac F, Lareyre J-J (2011) The gsdf gene locus harbors evolutionary conserved and clustered genes preferentially expressed in fish previtellogenic oocytes. Gene 472(1–2):7–17. https://doi.org/10.1016/j.gene.2010.10.014
Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208
Godwin JR (1994a) Histological aspects of protandrous sex change in the anemonefish Amphiprion melanopus. J Zool (Lond) 232:199–213
Godwin JR (1994b) Behavioral aspects of protandrous sex change in the anemonefish Amphiprion melanopus and endocrine correlates. Anim Behav 48:551–567
Godwin JR (1995) Phylogenetic and habitat influences on mating systems in the damselfish genus Dascyllus (Pomacentridae, Teleostei). Bull Mar Sci 57(3):637–652
Godwin J (2010) Neuroendocrinology of sexual plasticity in teleost fishes. Front Neuroendocrinol 31(2):203–216. https://doi.org/10.1016/j.yfrne.2010.02.002
Godwin JR, Fautin DF (1992) Defense of host actinians by anemonefishes. Copeia 1992(3):902–908
Godwin JR, Thomas P (1993) Sex change and steroid profiles in the protandrous anemonefish, Amphiprion melanopus. (Pomacentridae, Teleostei). Gen Comp Endocrinol 91:144–157
Godwin J, Crews D, Warner RR (1996) Behavioral sex change in the absence of gonads in a coral reef fish. Proc R Soc Ser B 263(1377):1683–1688
Graves JAM (2016) Evolution of vertebrate sex chromosomes and dosage compensation. Nat Rev Genet 17(1):33–46. https://doi.org/10.1038/nrg.2015.2
Gross MR (1982) Sneakers, satellites and parentals: polymorphic mating strategies in North American sunfishes. Ethology 60(1):1–26. https://doi.org/10.1111/j.1439-0310.1982.tb01073.x
Gross MR (1991) Evolution of alternative reproductive strategies: frequency-dependent sexual selection in male Bluegill sunfish. Philos Trans R Soc Lond Ser B Biol Sci 332(1262):59–66. https://doi.org/10.1098/rstb.1991.0033
Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11(2):92–98
Hastings PA, Petersen CW (1986) A novel sexual pattern in serranid fishes: simultaneous hermaphrodites and secondary males in Serranus fasciatus. Environ Biol Fishes 15(1):59–68. https://doi.org/10.1007/BF00005389
Hattori A, Yanigisawa Y (1991) Life-history pathways in relation to gonadal sex differentiation in the anemonefish, Amphiprion clarkii, in temperate waters of Japan. Environ Biol Fishes 31:139–155
Hattori RS, Fernandino JI, Kishii A, Kimura H, Kinno T, Oura M, Somoza GM, Yokota M, Strüssmann CA, Watanabe S (2009) Cortisol-induced masculinization: does thermal stress affect gonadal fate in pejerrey, a teleost fish with temperature-dependent sex determination. PLoS One 4:e6548. https://doi.org/10.1371/journal.pone.0006548
Hattori RS, Murai Y, Oura M, Masuda S, Majhi SK, Sakamoto T, Fernandino JI, Somoza GM, Yokota M, Strüssmann CA (2012) A Y-linked anti-Müllerian hormone duplication takes over a critical role in sex determination. Proc Natl Acad Sci USA 109(8):2955–2959. https://doi.org/10.1073/pnas.1018392109
Herpin A, Schartl M (2011) Dmrt1 genes at the crossroads: a widespread and central class of sexual development factors in fish. FEBS J 278(7):1010–1019. https://doi.org/10.1111/j.1742-4658.2011.08030.x
Higa M, Ogasawara K, Sakaguchi A, Nagahama Y, Nakamura M (2003) Role of steroid hormones in sex change of protogynous wrasse. Fish Physiol Biochem 28(1–4):149–150
Hiraki T, Takeuchi A, Tsumaki T, Zempo B, Kanda S, Oka Y, Nagahama Y, Okubo K (2012) Female-specific target sites for both oestrogen and androgen in the teleost brain. Proc R Soc B: Biol Sci 279(1749):5014–5023. https://doi.org/10.1098/rspb.2012.2011
Hobbs JA, Munday PL, Jones GP (2004) Social induction of maturation and sex determination in a coral reef fish. Proc R Soc B: Biol Sci 271(1553):2109–2114. https://doi.org/10.1098/rspb.2004.2845
Hubbs CL, Hubbs LC (1932) Apparent parthenogenesis in nature. in a form of fish of hybrid origin. Science 76:628–630
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(1):109–114. https://doi.org/10.1016/j.bbrc.2015.09.112
Jost A (1970) Hormonal factors in the sex differentiation of the mammalian foetus. Philos Trans R Soc Lond Ser B Biol Sci 259(828):119–131
Kamiya T, Kai W, Tasumi S, Oka A, Matsunaga T, Mizuno N et al (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
Kaneko H, Ijiri S, Kobayashi T, Izumi H, Kuramochi Y, Wang D-S et al (2015) Gonadal soma-derived factor (gsdf), a TGF-beta superfamily gene, induces testis differentiation in the teleost fish Oreochromis niloticus. Mol Cell Endocrinol 415:87–99. https://doi.org/10.1016/j.mce.2015.08.008
Katoh K, Miyata T (1999) A heuristic approach of maximum likelihood method for inferring phylogenetic tree and an application to the mammalian SOX-3 origin of the testis-determining gene SRY. FEBS Lett 463(1-2):129–132
Kikuchi K, Hamaguchi S (2013) Novel sex-determining genes in fish and sex chromosome evolution. Dev Dyn 242(4):339–353. https://doi.org/10.1002/dvdy.23927
Kitano T, Takamune K, Kobayashi T, Nagahama Y, Abe S-I (1999) Suppression of P450 aromatase gene expression in sex-reversed males produced by rearing genetically female larvae at a high water temperature during a period of sex differentiation in the Japanese flounder (Paralichthys olivaceus). J Mol Endocrinol 23:167–176
Kitano T, Takamune K, Nagahama Y, Abe S-I (2000) Aromatase inhibitor and 17_-methyltestosterone cause sex-reversal from genetical females to phenotypic males and suppression of P450 aromatase gene expression in Japanese flounder (Paralichthys olivaceus). Mol Reprod Dev 56:1–5
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 79:719–726
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 et al (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
Kosswig C (1964) Polygenic sex determination. Experientia 20(4):190–199
Kroon FJ, Munday PL, Pankhurst NW (2003) Steroid hormone levels and bi-directional sex change in Gobiodon histrio. J Fish Biol 62(1):153–167
Kroon FJ, Munday PL, Westcott DA, Hobbs JPA, Liley NR (2005) Aromatase pathway mediates sex change in each direction. Proc Biol Sci R Soc 272(1570):1399–1405. https://doi.org/10.1098/rspb.2005.3097
Kuwamura T, Suzuki S, Kadota T (2011) Reversed sex change by widowed males in polygynous and protogynous fishes: female removal experiments in the field. Naturwissenschaften 98:1041–1048
Kuwamura T, Suzuki S, Kadota T (2014) Testing the low-density hypothesis for reversed sex change in polygynous fish: experiments in Labroides dimidiatus. Sci Rep 4:4369. https://doi.org/10.1038/srep04369
Kwon JY, Haghpanah V, Kogson-Hurtado LM, McAndrew BJ, Penman DJ (2000) Masculinization of genetic female Nile tilapia (Oreochromis niloticus) by dietary administration of an aromatase inhibitor during sexual differentiation. J Exp Zool 287(1):46–53
Lagomarsino IV, Conover DO (1993) Variation in environmental and genotypic sex-determining mechanisms across a latitudinal gradient in the fish, Menidia menidia. Evolution 47(2):487. https://doi.org/10.2307/2410066
Lahn BT, Page DC (1999) Four evolutionary strata on the human X chromosome. Science 286(5441):964–967
Lamm MS, Liu H, Gemmell NJ, Godwin JR (2015) The need for speed: neuroendocrine regulation of socially-controlled sex change. Am Zool 55(2):307–322. https://doi.org/10.1093/icb/icv041
Le Page Y, Diotel N, Vaillant C, Pellegrini E, Anglade I, Mérot Y, Kah O (2010) Aromatase, brain sexualization and plasticity: the fish paradigm. Eur J Neurosci 32(12):2105–2115. https://doi.org/10.1111/j.1460-9568.2010.07519.x
Lee B-Y, Hulata G, Kocher TD (2004) Two unlinked loci controlling the sex of blue tilapia (Oreochromis aureus). Heredity 92(6):543–549. https://doi.org/10.1038/sj.hdy.6800453
Li M, Sun Y, Zhao J, Shi H, Zeng S, Ye K 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(11):e1005678. https://doi.org/10.1371/journal.pgen.1005678
Li X-Y, Zhang Q-Y, Zhang J, Zhou L, Li Z, Zhang X-J et al (2016) Extra microchromosomes play male determination role in polyploid gibel carp. Genetics 203(3):1415–1424. https://doi.org/10.1534/genetics.115.185843
Liew WC, Orbán L (2014) Zebrafish sex: a complicated affair. Brief Funct Genomics 13(2):172–187. https://doi.org/10.1093/bfgp/elt041
Liu H, Lamm MS, Rutherford K, Black MA, Godwin JR, Gemmell NJ (2015) Large-scale transcriptome sequencing reveals novel expression patterns for key sex-related genes in a sex-changing fish. Biol Sex Dif 6:26. https://doi.org/10.1186/s13293-015-0044-8
Lorenzi V, Earley RL, Rodgers EW, Pepper DR, Grober MS (2008) Diurnal patterns and sex differences in cortisol, 11-ketotestosterone, testosterone, and 17 beta-estradiol in the bluebanded goby (Lythrypnus dalli). Gen Comp Endocrinol 155(2):438–446
Lubieniecki KP, Botwright NA, Taylor RS, Evans BS, Cook MT, Davidson WS (2015) Expression analysis of sex-determining pathway genes during development in male and female Atlantic salmon (Salmo salar). Physiol Genomics 47(12):581–587. https://doi.org/10.1152/physiolgenomics.00013.2015
Luckenbach JA, Godwin J, Daniels HV, Borski RJ (2003) Gonadal differentiation and effects of temperature on sex determination in southern flounder (Paralichthys lethostigma). Aquaculture 216(1–4):315–327. https://doi.org/10.1016/S0044-8486(02)00407-6
Luckenbach JA, Early LW, Rowe AH, Borski RJ, Daniels HV, Godwin J (2005) Aromatase cytochrome P450: cloning, intron variation, and ontogeny of gene expression in southern flounder (Paralichthys lethostigma). J Exp Zool Part A 303A(8):643–656. https://doi.org/10.1002/jez.a.198
Luckenbach JA, Borski RJ, Daniels HV, Godwin J (2009) Sex determination in flatfishes: mechanisms and environmental influences. Semin Cell Dev Biol 20:1–8. https://doi.org/10.1016/j.semcdb.2008.12.002
Lutnesky M (1994) Density-dependent protogynous sex change in territorial-haremic fishes: models and evidence. Behav Ecol 5:375–383
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. Am Zool 53(4):755–765. https://doi.org/10.1093/icb/ict093
Marsh-Hunkin KE, Heinz HM, Hawkins MB, Godwin J (2013) Estrogenic control of behavioral sex change in the bluehead wrasse, Thalassoma bifasciatum. Integr Comp Biol 53(6):951–959
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
Matsuda M, Sakaizumi M (2015) Evolution of the sex-determining gene in the teleostean genus Oryzias. Gen Comp Endocrinol 239:80–88. https://doi.org/10.1016/j.ygcen.2015.10.004
Matsuda M, Nagahama Y, Shinomiya A, Sato T, Matsuda C, Kobayashi T et al (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, Shinomiya A, Kinoshita M, Suzuki A, Kobayashi T, Paul-Prasanth B, Lau EL, Hamaguchi S, Sakaizumi M, Nagahama Y (2007) DMY gene induces male development in genetically female (XX) medaka fish. Proc Natl Acad Sci USA 104(10):3865–3870
Montalvo AJ, Faulk CK, Holt GJ (2012) Sex determination in southern flounder, Paralichthys lethostigma, from the Texas Gulf Coast. J Exp Mar Biol Ecol 432–433(C):186–190. https://doi.org/10.1016/j.jembe.2012.07.017
Moore EC, Roberts RB (2013) Polygenic sex determination. Curr Biol 23(12):R510–R512. https://doi.org/10.1016/j.cub.2013.04.004
Morinaga C, Saito D, Nakamura S, Sasaki T, Asakawa S, Shimizu N et al (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 104(23):9691–9696. https://doi.org/10.1073/pnas.0611379104
Myosho T, Otake H, Masuyama H, Matsuda M, Kuroki Y, Fujiyama A et al (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
Myosho T, Takehana Y, Hamaguchi S, Sakaizumi M (2015) Turnover of sex chromosomes in celebensis group medaka fishes. G3 (Bethesda, Md) 5(12):2685–2691. https://doi.org/10.1534/g3.115.021543
Nakamura M, Hourigan TF, Yamauchi K, Nagahama Y, Grau EG (1989) Histological and ultrastructural evidence for the role of gonadal steroid hormones in sex change in the protogynous wrasse Thalassoma duperrey. Environ Biol Fishes 24(2):117–136
Nanda I, Kondo M, Hornung U, Asakawa S, Winkler C, Shimizu A et al (2002) A duplicated copy of [i]DMRT1[/i] in the sex-determining region of the Y chromosome of the medaka, [i]Oryzias latipes[/i]. Proc Natl Acad Sci 99(18):11778–11783. https://doi.org/10.1073/pnas.182314699
Nanda I, Schories S, Tripathi N, Dreyer C, Haaf T, Schmid M, Schartl M (2014) Sex chromosome polymorphism in guppies. Chromosoma 123(4):373–383. https://doi.org/10.1007/s00412-014-0455-z
Neff BD, Knapp R (2009) Paternity, parental behavior and circulating steroid hormone concentrations in nest-tending male bluegill. Horm Behav 56(2):239–245. https://doi.org/10.1016/j.yhbeh.2009.05.002
Oliveira RF, Canario AVM, Grober MS (2001) Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces: Blenniidae). Horm Behav 40(2):266–275. https://doi.org/10.1006/hbeh.2001.1683
Oliveira RF, Ros AFH, Gonçalves DM (2005) Intra-sexual variation in male reproduction in teleost fish: a comparative approach. Horm Behav 48(4):430–439. https://doi.org/10.1016/j.yhbeh.2005.06.002
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:e2837
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 105(3):247–256
Palaiokostas C, Bekaert M, Taggart JB, Gharbi K, McAndrew BJ, Chatain B et al (2015) A new SNP-based vision of the genetics of sex determination in European sea bass (Dicentrarchus labrax). Genet Sel Evol 47:68. https://doi.org/10.1186/s12711-015-0148-y
Perry AN, Grober MS (2003) A model for social control of sex change: interactions of behavior, neuropeptides, glucocorticoids, and sex steroids. Horm Behav 43:31–38
Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on teh tissues mediating mating behavior in the female guinea pig. Endocrinology 65:369–382
Piferrer F (2011) Endocrine control of sex differentiation in fish. In: Farrell AP (ed) Encyclopedia of fish physiology: from gene to environment, vol 2. Academic, San Diego, pp 1490–1499
Raymond CS, Shamu CE, Shen MM, Seifert KJ, Hirsch B, Hodgkin J, Zarkower D (1998) Evidence for evolutionary conservation of sex-determining genes. Nature 391(6668):691–695. https://doi.org/10.1038/35618
Raymond CS, Murphy MW, O’Sullivan MG, Bardwell VJ, Zarkower D (2000) Dmrt1, a gene related to worm and fly sexual regulators, is required for mammalian testis differentiation. Genes Dev 14(20):2587–2595
Reichwald K, Petzold A, Koch P, Downie BR, Hartmann N, Pietsch S et al (2015) Insights into sex chromosome evolution and aging from the genome of a short-lived fish. Cell 163(6):1527–1538. https://doi.org/10.1016/j.cell.2015.10.071
Reinboth R (1980) Can sex inversion be environmentally induced? Biol Reprod 22(1):49–59
Roberts RB, Ser JR, Kocher TD (2009) Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes. Science 326(5955):998–1001. https://doi.org/10.1126/science.1174705
Roberts NB, Juntti SA, Coyle KP, Dumont BL, Stanley MK, Ryan AQ, Fernald RD, Roberts RB (2016) Polygenic sex determination in the cichlid fish Astatotilapia burtoni. BMC Genomics. https://doi.org/10.1186/s12864-016-3177-1
Robertson (1972) Social control of sex reversal in a coral-reef fish. Science 177:1007–1009
Rodriguez-Mar IA, Postlethwait JH (2011) The role of Fanconi anemia/BRCA genes in zebrafish sex determination. Methods Cell Biol 105:461–490. https://doi.org/10.1016/B978-0-12-381320-6.00020-5
Roesti M, Moser D, Berner D (2013) Recombination in the threespine stickleback genome—patterns and consequences. Mol Ecol 22(11):3014–3027. https://doi.org/10.1111/mec.12322
Rondeau EB, Messmer AM, Sanderson DS, Jantzen SG, von Schalburg KR, Minkley DR et al (2013) Genomics of sablefish (Anoplopoma fimbria): expressed genes, mitochondrial phylogeny, linkage map and identification of a putative sex gene. BMC Genomics 14:452. https://doi.org/10.1186/1471-2164-14-452
Ross RM (1978) Reproductive behavior of the anemonefish Amphiprion melanopus on Guam. Copeia 1978:103–107
Ross (1983) Sex change in a coral-reef fish- dependence of stimulation and inhibition on relative size. Science 221(4610):574–575
Ross JA, Peichel CL (2008) Molecular cytogenetic evidence of rearrangements on the Y chromosome of the threespine stickleback fish. Genetics 179(4):2173–2182. https://doi.org/10.1534/genetics.108.088559
Ross RM, Hourigan TF, Lutnesky MMF, Singh I (1990) Multiple simultaneous sex changes in social groups of a coral-reef fish. Copeia 1990(2):427. https://doi.org/10.2307/1446348
Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL (2009) Turnover of sex chromosomes in the stickleback fishes (gasterosteidae). PLoS Genet 5(2):e1000391. https://doi.org/10.1371/journal.pgen.1000391
Ser JR, Roberts RB, Kocher TD (2010) Multiple interacting loci control sex determination in lake Malawi cichlid fish. Evolution 64(2):486–501. https://doi.org/10.1111/j.1558-5646.2009.00871.x
Shao C, Li Q, Chen S, Zhang P, Lian J, Hu Q et al (2014) Epigenetic modification and inheritance in sexual reversal of fish. Genome Res 24(4):604–615. https://doi.org/10.1101/gr.162172.113
Shapiro DY (1980) Serial female sex changes after simultaneous removal of males from social groups of a coral reef fish. Science 209(4461):1136–1137
Sinclair AH, Berta P, Palmer MS, Hawkins JR, Griffiths BL, Smith MJ et al (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
Smith CA, Roeszler KN, Ohnesorg T, Cummins DM, Farlie PG, Doran TJ, Sinclair AH (2009) The avian Z-linked gene DMRT1 is required for male sex determination in the chicken. Nature 461(7261):267–271. https://doi.org/10.1038/nature08298
Solomon-Lane TK, Crespi EJ, Grober MS (2013) Stress and serial adult metamorphosis: multiple roles for the stress axis in socially regulated sex change. Front Neurosci 7:210. https://doi.org/10.3389/fnins.2013.00210
St. Mary CM (1994) Sex allocation in a simultaneous hermaphrodite, the blue banded goby (Lythrypnus dalli)—the effect of body size and behavioral gender and the consequences for reproduction. Behav Ecol 5:304–313
Stacey NE (2015) Hormonally derived pheromones in teleost fishes. In: Sorensen PW, Wisenden BD (eds) Fish pheromones and related cues. Wiley, Hoboken, pp 33–88
Stacey NE, Sorensen PW (2011) Hormonal pheromones. In: Farrell AP (ed) Encyclopedia of fish physiology: from genome to environment, vol 1. Elsevier, San Diego, pp 1553–1562
Strüssmann CA, Moriyama S, Hanke EF, Cota JCC, Takashima F (1996) Evidence of thermolabile sex determination in pejerrey. J Fish Biol 48(4):643–651. https://doi.org/10.1111/j.1095-8649.1996.tb01459.x
Strüssmann, C. A., Saito, T., Usui, M., Yamada, H., & Takashima, F. (1997). Thermal thresholds and critical period of thermolabile sex determination in two atherinid fishes, Odontesthes bonariensis and Patagonina hatcheri. J Exp Zool Part A: Ecol Genet Physiol, 278(3), 167–177. https://doi.org/10.1002/(SICI)1097-010X(19970615)278:3<167::AID-JEZ6>3.0.CO;2-M
Taborsky M (1998) Sperm competition in fish: ‘bourgeois’ males and parasitic spawning. Trends Ecol Evol 13(6):222–227
Takehana Y, Matsuda M, Myosho T, Suster ML, Kawakami K, Shin-I T et al (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
Tree of Sex Consortium (2014) Tree of sex: a database of sexual systems. Sci Data 1:561–572. https://doi.org/10.1038/sdata.2014.15
Uno Y, Nishida C, Yoshimoto S, Ito M, Oshima Y, Yokoyama S et al (2008) Diversity in the origins of sex chromosomes in anurans inferred from comparative mapping of sexual differentiation genes for three species of the Raninae and Xenopodinae. Chromosom Res 16(7):999–1011. https://doi.org/10.1007/s10577-008-1257-z
van Doorn GS, Kirkpatrick M (2007) Turnover of sex chromosomes induced by sexual conflict. Nature 449(7164):909–912. https://doi.org/10.1038/nature06178
Vrijenhoek RC (1994) Unisexual fish: model systems for studying ecology and evolution. Annu Rev Ecol Syst 25:71–96
Wallen K (2009) The organizational hypothesis: reflections on the 50th anniversary of the publication of Phoenix, Goy, Gerall, and Young (1959). Horm Behav 55:561–565
Warner RR (1978) The evolution of hermaphroditism and unisexuality in aquatic and terrestrial vertebrates. In: Reese ES, Lighter FJ (eds) Contrasts in behavior: adaptations in the aquatic and terrestrial environments. Wiley, New York, pp 77–101
Warner RR (1984) Mating behavior and hermaphroditism in coral-reef fishes. Am Sci 72:128–136
Warner RR, Swearer SE (1991) Social control of sex change in the bluehead Wrasse, Thalassoma bifasciatum (Pisces: Labridae). Biol Bull 181(2):199. https://doi.org/10.2307/1542090
Warner RR, Robertson DR, Leigh EG (1975) Sex change and sexual selection. Science 190:633–638
White MA, Kitano J, Peichel CL (2015) Purifying selection maintains dosage-sensitive genes during degeneration of the threespine stickleback Y chromosome. Mol Biol Evol 32(8):1981–1995. https://doi.org/10.1093/molbev/msv078
Wilson CA, High SK, McCluskey BM, Amores A, Yan Y-L, Titus TA et al (2014) Wild sex in zebrafish: loss of the natural sex determinant in domesticated strains. Genetics 198(3):1291–1308. https://doi.org/10.1534/genetics.114.169284
Winge O (1932) The nature of sex chromosomes. Proc Sixth Int Congr Genet 1:343–355
Wong RY, McLeod MM, Godwin J (2014) Limited sex-biased neural gene expression patterns across strains in Zebrafish (Danio rerio). BMC Genomics 15:905. http://www.biomedcentral.com/1471-2164/15/905
Wright AE, Dean R, Zimmer F, Mank JE (2016) How to make a sex chromosome. Nat Commun 7:12087. https://doi.org/10.1038/ncomms12087
Yamaguchi T, Kitano T (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. Biochem Biophys Res Commun 419:287–292
Yamaguchi T, Yoshinaga N, Yazawa T, Gen K, Kitano T (2010) Cortisol is involved in temperature-dependent sex determination in the Japanese flounder. Endocrinology 151(8):3900–3908. https://doi.org/10.1210/en.2010-0228
Yamamoto E (1995) Studies on sex-manipulation and production of cloned populations in hirame flounder, Paralichthys olivaceus. Bull Tottori Pref Fish Exp Stn 34:1–145
Yamamoto E (1999) Studies on sex-manipulation and production of cloned populations in hirame, Paralichthys olivaceus (Temminck et Schlegel). Aquaculture 173(1–4):235–246. https://doi.org/10.1016/S0044-8486(98)00448-7
Yamamoto Y, Zhang Y, Sarida M, Hattori RS, Strüssmann CA (2014) Coexistence of genotypic and temperature-dependent sex determination in pejerrey Odontesthes bonariensis. PLoS One 9(7):e102574. https://doi.org/10.1371/journal.pone.0102574
Yano A, Guyomard R, Nicol B, Jouanno E, Quillet E, Klopp C et al (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
Yoshida K, Terai Y, Mizoiri S, Aibara M, Nishihara H, Watanabe M et al (2011) B chromosomes have a functional effect on female sex determination in Lake Victoria cichlid fishes. PLoS Genet 7(8):e1002203. https://doi.org/10.1371/journal.pgen.1002203
Yoshimoto S, Okada E, Umemoto H, Tamura K, Uno Y, Nishida-Umehara C et al (2008) A W-linked DM-domain gene, DM-W, participates in primary ovary development in Xenopus laevis. Proc Natl Acad Sci USA 105(7):2469–2474. https://doi.org/10.1073/pnas.0712244105
Yoshinaga N, Shiraishi E, Yamamoto T, Iguchi T, Shinichi A, Kitano T (2004) Sexually dimorphic expression of a teleost homologue of Müllerian inhibiting substance during gonadal sex differentiation in Japanese flounder, Paralichthys olivaceus. Biochem Biophys Res Commun 322:508–513
Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED et al (2014) Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346(6215):1246338. https://doi.org/10.1126/science.1246338
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Godwin, J., Roberts, R. (2018). Environmental and Genetic Sex Determining Mechanisms in Fishes. In: Leonard, J. (eds) Transitions Between Sexual Systems. Springer, Cham. https://doi.org/10.1007/978-3-319-94139-4_11
Download citation
DOI: https://doi.org/10.1007/978-3-319-94139-4_11
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-319-94137-0
Online ISBN: 978-3-319-94139-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)