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Mechanisms of Environmental Sex Determination in Fish, Amphibians, and Reptiles

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Choosing Sexes

Part of the book series: Fascinating Life Sciences ((FLS))

Abstract

In many reptiles, amphibians, and fishes, the environment plays a key role in determining the sexes of individuals. Temperature, in particular, appears to be a potent modulator of sex allocation in all three vertebrate classes, yet we do not yet know how temperature interacts with physiology in these systems to influence sexual development. In this chapter, I discuss the gene targets that may be key mediators of temperature sex determination in reptiles, fish, and amphibians, discuss the potential role of hormones in the process of sex determination for all three groups, and highlight the need for comparative studies to explore the potential of a conserved mediator that facilitates sex allocation in response to a variety of environmental and social cues.

Which of these points of view, preformation or epigenesis, we may think more profitable as a working hypothesis is, I believe, the question of the hour. My own preference—or prejudice, perhaps—is for the epigenetic interpretation…

Thomas Hunt Morgan in Hunt (1907)

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References

  • Balthazart J, Ball GF (1995) Sexual differentiation of brain and behavior in birds. Trends Endocrinol Metab 6(1):21–29

    Article  CAS  PubMed  Google Scholar 

  • Blasco M, Somoza GM, Vizziano-Cantonnet D (2013) Presence of 11-ketotestosterone in pre-differentiated male gonads of Odontesthes bonariensis. Fish Physiol Biochem 39(1):71–74

    Article  CAS  PubMed  Google Scholar 

  • Bowden R, Ewert M, Nelson C (2000) Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc R Soc Lond B Biol Sci 267(1454):1745–1749

    Article  CAS  Google Scholar 

  • Bowden RM, Ewert MA, Freedberg S, Nelson CE (2002) Maternally derived yolk hormones vary in follicles of the painted turtle, Chrysemys picta. J Exp Zool A Ecol Genet Physiol 293(1):67–72

    CAS  Google Scholar 

  • Bowden RM, Carter AW, Paitz RT (2014) Constancy in an inconstant world: moving beyond constant temperatures in the study of reptilian incubation. Integr Comp Biol 54(5):830–840

    Article  PubMed  Google Scholar 

  • Bull J (1985) Sex ratio and nest temperature in turtles: comparing field and laboratory data. Ecology 66(4):1115–1122

    Article  Google Scholar 

  • Chojnowski JL, Braun EL (2012) An unbiased approach to identify genes involved in development in a turtle with temperature-dependent sex determination. BMC Genomics 13(1):308

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crews D, Bull JJ (2009) Mode and tempo in environmental sex determination in vertebrates. Semin Cell Dev Biol 20(3):251–255

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Díaz N, Piferrer F (2015) Lasting effects of early exposure to temperature on the gonadal transcriptome at the time of sex differentiation in the European sea bass, a fish with mixed genetic and environmental sex determination. BMC Genomics 16(1):679

    Article  PubMed  PubMed Central  Google Scholar 

  • Elf P (2003) Yolk steroid hormones and sex determination in reptiles with TSD. Gen Comp Endocrinol 132(3):349–355

    Article  CAS  PubMed  Google Scholar 

  • Ellison A, López CMR, Moran P, Breen J, Swain M, Megias M, Hegarty M, Wilkinson M, Pawluk R, Consuegra S (2015) Epigenetic regulation of sex ratios may explain natural variation in self-fertilization rates. Proc R Soc B 282(1819):20151900

    Google Scholar 

  • Fan Z, Zou Y, Jiao S, Tan X, Wu Z, Liang D, Zhang P, You F (2017) Significant association of cyp19a promoter methylation with environmental factors and gonadal differentiation in olive flounder Paralichthys olivaceus. Comp Biochem Physiol A Mol Integr Physiol 208:70–79

    Article  CAS  PubMed  Google Scholar 

  • Ferguson-Smith M (2007) The evolution of sex chromosomes and sex determination in vertebrates and the key role of DMRT1. Sex Dev 1(1):2–11

    Article  CAS  PubMed  Google Scholar 

  • Fernandino JI, Hattori RS, Kishii A, Strüssmann 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(12):6003–6011

    Article  CAS  PubMed  Google Scholar 

  • Fernandino JI, Hattori RS, Acosta ODM, Strüssmann CA, Somoza GM (2013) Environmental stress-induced testis differentiation: androgen as a by-product of cortisol inactivation. Gen Comp Endocrinol 192:36–44

    Article  CAS  PubMed  Google Scholar 

  • Flament S (2016) Sex reversal in amphibians. Sex Dev 10(5-6):267–278

    Article  CAS  PubMed  Google Scholar 

  • Fleming A, Crews D (2001) Estradiol and incubation temperature modulate regulation of steroidogenic factor 1 in the developing gonad of the red-eared slider turtle. Endocrinology 142(4):1403–1411

    Article  CAS  PubMed  Google Scholar 

  • Georges A, Limpus C, Stoutjesdijk R (1994) Hatchling sex in the marine turtle Caretta caretta is determined by proportion of development at a temperature, not daily duration of exposure. J Exp Zool A Ecol Genet Physiol 270(5):432–444

    Google Scholar 

  • Godwin JR, Thomas P (1993) Sex change and steroid profiles in the protandrous anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). Gen Comp Endocrinol 91(2):144–157

    Article  CAS  PubMed  Google Scholar 

  • Godwin J, Thompson R (2012) Nonapeptides and social behavior in fishes. Horm Behav 61(3):230–238

    Article  CAS  PubMed  Google Scholar 

  • Guiguen Y, Fostier A, Piferrer F, Chang C-F (2010) Ovarian aromatase and estrogens: a pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165(3):352–366

    Article  CAS  PubMed  Google Scholar 

  • 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(8):e6548

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 109(8):2955–2959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Hayes TB (1998) Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. J Exp Zool A Ecol Genet Physiol 281(5):373–399

    CAS  Google Scholar 

  • Hunt TM (1907) Sex-determining factors in animals. Science 25(636):382–384

    Google Scholar 

  • Iungman JL, Somoza GM, Piña CI (2015) Are stress-related hormones involved in the temperature-dependent sex determination of the broad-snouted caiman? South Am J Herpetol 10(1):41–49

    Article  Google Scholar 

  • Iwamatsu T, Kobayashi H, Sagegami R, Shuo T (2006) Testosterone content of developing eggs and sex reversal in the medaka (Oryzias latipes). Gen Comp Endocrinol 145(1):67–74

    Article  CAS  PubMed  Google Scholar 

  • Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(3s):245

    Article  CAS  PubMed  Google Scholar 

  • Janzen F, Wilson M, Tucker J, Ford S (1998) Endogenous yolk steroid hormones in turtles with different sex-determining mechanisms. Gen Comp Endocrinol 111(3):306–317

    Article  CAS  PubMed  Google Scholar 

  • Khan M, Renaud R, Leatherland J (1997) Metabolism of estrogens and androgens by embryonic tissues of Arctic charr, Salvelinus alpinus. Gen Comp Endocrinol 107(1):118–127

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi S, Isotani A, Mise N, Yamamoto M, Fujihara Y, Kaseda K, Nakanishi T, Ikawa M, Hamada H, Abe K (2006) Comparison of gene expression in male and female mouse blastocysts revealed imprinting of the X-linked gene, Rhox5/Pem, at preimplantation stages. Curr Biol 16(2):166–172

    Article  CAS  PubMed  Google Scholar 

  • Kohno S, Katsu Y, Urushitani H, Ohta Y, Iguchi T, Guillette L Jr (2010) Potential contributions of heat shock proteins to temperature-dependent sex determination in the American alligator. Sex Dev 4(1–2):73–87

    Article  CAS  PubMed  Google Scholar 

  • Kohno S, Bernhard MC, Katsu Y, Zhu J, Bryan TA, Doheny BM, Iguchi T, Guillette LJ Jr (2015) Estrogen receptor 1 (ESR1; ERα), not ESR2 (ERβ), modulates estrogen-induced sex reversal in the American alligator, a species with temperature-dependent sex determination. Endocrinology 156(5):1887–1899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuntz S, Chesnel A, Duterque-Coquillaud M, Grillier-Vuissoz I, Callier M, Dournon C, Flament S, Chardard D (2003) Differential expression of P450 aromatase during gonadal sex differentiation and sex reversal of the newt Pleurodeles waltl. J Steroid Biochem Mol Biol 84(1):89–100

    Article  CAS  PubMed  Google Scholar 

  • Lee YH, Du JL, Yueh WS, Lin BY, Huang JD, Lee CY, Lee MF, Lau EL, Lee FY, Morrey C (2001) Sex change in the protandrous black porgy, Acanthopagrus schlegeli: a review in gonadal development, estradiol, estrogen receptor, aromatase activity and gonadotropin. J Exp Zool A Ecol Genet Physiol 290(7):715–726

    CAS  Google Scholar 

  • Liu H (2016) Genomic basis of sex change in fish. University of Otago

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto Y, Crews D (2012) Molecular mechanisms of temperature-dependent sex determination in the context of ecological developmental biology. Mol Cell Endocrinol 354(1):103–110

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto Y, Buemio A, Chu R, Vafaee M, Crews D (2013) Epigenetic control of gonadal aromatase (cyp19a1) in temperature-dependent sex determination of red-eared slider turtles. PLoS One 8(6):e63599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCoy JA, Hamlin HJ, Thayer L, Guillette LJ, Parrott BB (2016) The influence of thermal signals during embryonic development on intrasexual and sexually dimorphic gene expression and circulating steroid hormones in American alligator hatchlings (Alligator mississippiensis). Gen Comp Endocrinol 238:47–54

    Article  CAS  PubMed  Google Scholar 

  • Merchant-Larios H, Fierro IV, Urruiza BC (1989) Gonadal morphogenesis under controlled temperature in the sea turtle Lepidochelys olivacea. Herpetol Monogr 3:43–61

    Article  Google Scholar 

  • Murdock C, Wibbels T (2006) Dmrt1 expression in response to estrogen treatment in a reptile with temperature-dependent sex determination. J Exp Zool B Mol Dev Evol 306(2):134–139

    Article  PubMed  Google Scholar 

  • Nakamura M (2009) Sex determination in amphibians. Semin Cell Dev Biol 3:271–282

    Article  Google Scholar 

  • Narberhaus F, Waldminghaus T, Chowdhury S (2005) RNA thermometers. FEMS Microbiol Rev 30(1):3–16

    Article  Google Scholar 

  • Navarro-Martín L, Viñas J, Ribas L, Díaz N, Gutiérrez A, Di Croce L, Piferrer F (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet 7(12):e1002447

    Article  PubMed  PubMed Central  Google Scholar 

  • Neuwald JL, Valenzuela N (2011) The lesser known challenge of climate change: thermal variance and sex-reversal in vertebrates with temperature-dependent sex determination. PLoS One 6(3):e18117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nozu R, Nakamura M (2015) Cortisol administration induces sex change from ovary to testis in the protogynous wrasse, Halichoeres trimaculatus. Sex Dev 9(2):118–124

    Article  CAS  PubMed  Google Scholar 

  • Paitz RT, Clairardin SG, Griffin AM, Holgersson MC, Bowden RM (2010a) Temperature fluctuations affect offspring sex but not morphological, behavioral, or immunological traits in the Northern Painted Turtle (Chrysemys picta). Can J Zool 88(5):479–486

    Article  Google Scholar 

  • Paitz RT, Gould AC, Holgersson MC, Bowden RM (2010b) Temperature, phenotype, and the evolution of temperature-dependent sex determination: how do natural incubations compare to laboratory incubations? J Exp Zool B Mol Dev Evol 314(1):86–93

    Article  PubMed  Google Scholar 

  • Parrott BB, Kohno S, Cloy-McCoy JA, Guillette Jr LJ (2014) Differential incubation temperatures result in dimorphic DNA methylation patterning of the SOX9 and aromatase promoters in gonads of alligator (Alligator mississippiensis) embryos. Biol Reprod 90(1):2, 1–11

    Google Scholar 

  • Piferrer F (2001) Endocrine sex control strategies for the feminization of teleost fish. Aquaculture 197(1):229–281

    Article  CAS  Google Scholar 

  • Piferrer F (2013) Epigenetics of sex determination and gonadogenesis. Dev Dyn 242(4):360–370

    Article  CAS  PubMed  Google Scholar 

  • Piquet J (1930) Détermination du sexe chez les Batraciens en fonction de la température. Universite de Geneve

    Google Scholar 

  • Radder RS (2007) Maternally derived egg yolk steroid hormones and sex determination: review of a paradox in reptiles. J Biosci 32:1213–1220

    Article  CAS  PubMed  Google Scholar 

  • Ramsey M, Crews D (2009) Steroid signaling and temperature-dependent sex determination—Reviewing the evidence for early action of estrogen during ovarian determination in turtles. Semin Cell Dev Biol 3:283–292

    Article  Google Scholar 

  • Raynaud A (1985) Embryonic development of the genital system. In: Gans S, Billeu F (eds) Biology of the reptilia. Wiley, New York, pp 149–299

    Google Scholar 

  • Rhen T, Schroeder A (2010) Molecular mechanisms of sex determination in reptiles. Sex Dev 4(1-2):16–28

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rowell CB, Watts SA, Wibbels T, Hines GA, Mair G (2002) Androgen and estrogen metabolism during sex differentiation in mono-sex populations of the Nile tilapia, Oreochromis niloticus. Gen Comp Endocrinol 125(2):151–162

    Article  CAS  PubMed  Google Scholar 

  • Sakata N, Tamori Y, Wakahara M (2004) P450 aromatase expression in the temperature-sensitive sexual differentiation of salamander (Hynobius retardatus) gonads. Int J Dev Biol 49(4):417–425

    Article  Google Scholar 

  • Schroeder AL, Metzger KJ, Miller A, Rhen T (2016) A novel candidate gene for temperature-dependent sex determination in the common snapping turtle. Genetics 203(1):557–571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shao C, Li Q, Chen S, Zhang P, Lian J, Hu Q, Sun B, Jin L, Liu S, Wang Z (2014) Epigenetic modification and inheritance in sexual reversal of fish. Genome Res 24(4):604–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shen Z-G, Wang H-P (2014) Molecular players involved in temperature-dependent sex determination and sex differentiation in Teleost fish. Genet Sel Evol 46(1):26

    Article  PubMed  PubMed Central  Google Scholar 

  • Shi Y, Zhang Y, Li S, Liu Q, Lu D, Liu M, Meng Z, Cheng CH, Liu X, Lin H (2010) Molecular identification of the Kiss2/Kiss1ra system and its potential function during 17alpha-methyltestosterone-induced sex reversal in the orange-spotted grouper, Epinephelus coioides. Biol Reprod 83(1):63–74

    Article  CAS  PubMed  Google Scholar 

  • Shoemaker CM, Crews D (2009) Analyzing the coordinated gene network underlying temperature-dependent sex determination in reptiles. Semin Cell Dev Biol 3:293–303

    Article  Google Scholar 

  • Sifuentes-Romero I, Merchant-Larios H, Milton SL, Moreno-Mendoza N, Díaz-Hernández V, García-Gasca A (2013) RNAi-mediated gene silencing in a gonad organ culture to study sex determination mechanisms in sea turtle. Genes 4(2):293–305

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 7:1–12

    Article  Google Scholar 

  • Sun L-X, Wang Y-Y, Zhao Y, Wang H, Li N, Ji XS (2016) Global DNA methylation changes in Nile tilapia gonads during high temperature-induced masculinization. PLoS One 11(8):e0158483

    Article  PubMed  PubMed Central  Google Scholar 

  • Telemeco RS, Abbott KC, Janzen FJ (2013) Modeling the effects of climate change–induced shifts in reproductive phenology on temperature-dependent traits. Am Nat 181(5):637–648

    Article  PubMed  Google Scholar 

  • Thomas EO, Light P, Wibbels T, Crews D (1992) Hydroxysteroid dehydrogenase activity associated with sexual differentiation in embryos of the turtle Trachemys scripta. Biol Reprod 46(1):140–145

    Article  CAS  PubMed  Google Scholar 

  • Todd EV, Liu H, Muncaster S, Gemmell NJ (2016) Bending genders: the biology of natural sex change in fish. Sex Dev 10(5–6):223–241

    Article  CAS  PubMed  Google Scholar 

  • Uller T, Hollander J, Astheimer L, Olsson M (2009) Sex-specific developmental plasticity in response to yolk corticosterone in an oviparous lizard. J Exp Biol 212(8):1087–1091

    Article  PubMed  Google Scholar 

  • Wang X, Liu Q, Xiao Y, Yang Y, Wang Y, Song Z, You F, An H, Li J (2017) High temperature causes masculinization of genetically female olive flounder (Paralichthys olivaceus) accompanied by primordial germ cell proliferation detention. Aquaculture 479:808–816

    Article  Google Scholar 

  • Warner DA, Radder RS, Shine R (2009) Corticosterone exposure during embryonic development affects offspring growth and sex ratios in opposing directions in two lizard species with environmental sex determination. Physiol Biochem Zool 82(4):363–371

    Article  PubMed  Google Scholar 

  • Wibbels T, Crews D (1992) Specificity of steroid hormone-induced sex determination in a turtle. J Endocrinol 133(1):121–129

    Article  CAS  PubMed  Google Scholar 

  • Wibbels T, Bull J, Crews D (1991) Synergism between temperature and estradiol: a common pathway in turtle sex determination? J Exp Zool A Ecol Genet Physiol 260(1):130–134

    CAS  Google Scholar 

  • Wibbels T, Bull JJ, Crews D (1994) Temperature-dependent sex determination: a mechanistic approach. J Exp Zool A Ecol Genet Physiol 270(1):71–78

    Google Scholar 

  • Witschi E (1914) Experimentelle Untersuchungen über die Entwicklungsgeschichte der Keimdrüsen von Rana temporaria. Arch Mikrosk Anat 85(1):A9–A113

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto T-O (1969) Sex differentiation. Fish Physiol 3:117–175

    Article  CAS  Google Scholar 

  • Yamamoto Y, Hattori R, Kitahara A, Kimura H, Yamashita M, Strüssmann C (2013) Thermal and endocrine regulation of gonadal apoptosis during sex differentiation in pejerrey Odontesthes bonariensis. Sex Dev 7(6):316–324

    Article  CAS  PubMed  Google Scholar 

  • Yatsu R, Miyagawa S, Kohno S, Saito S, Lowers RH, Ogino Y, Fukuta N, Katsu Y, Ohta Y, Tominaga M (2015) TRPV4 associates environmental temperature and sex determination in the American alligator. Sci Rep 5:18581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yatsu R, Miyagawa S, Kohno S, Parrott BB, Yamaguchi K, Ogino Y, Miyakawa H, Lowers RH, Shigenobu S, Guillette LJ (2016) RNA-seq analysis of the gonadal transcriptome during Alligator mississippiensis temperature-dependent sex determination and differentiation. BMC Genomics 17(1):77

    Article  PubMed  PubMed Central  Google Scholar 

  • Yeoh C-G, Schreck CB, Fitzpatrick MS, Feist GW (1996) In vivosteroid metabolism in embryonic and newly hatched steelhead trout (Oncorhynchus mykiss). Gen Comp Endocrinol 102(2):197–209

    Article  CAS  PubMed  Google Scholar 

  • Zaborski P (1986) Temperature and estrogen dependent changes of sex phenotype and HY antigen expression in gonads of a newt. Prog Clin Biol Res 217:163–169

    Google Scholar 

  • Zhang Y, Zhang S, Liu Z, Zhang L, Zhang W (2013) Epigenetic modifications during sex change repress gonadotropin stimulation of cyp19a1a in a teleost ricefield eel (Monopterus albus). Endocrinology 154(8):2881–2890

    Article  CAS  PubMed  Google Scholar 

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Navara, K.J. (2018). Mechanisms of Environmental Sex Determination in Fish, Amphibians, and Reptiles. In: Choosing Sexes. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-71271-0_10

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