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What Went Wrong at Jurassic Park? Modes of Sex Determination and Adaptive Sex Allocation in Reptiles

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Choosing Sexes

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Abstract

While birds and mammals determine sex of offspring via sex chromosomes, reptiles developed a new way to determine offspring sex—through temperature. We now know that reptiles display a range of sex-determining systems, including systems that show strict genetic sex determination, systems that have genetic sex determination with a temperature override, and finally systems in which temperature determines sex with no apparent genetic underpinning. In this chapter, I will outline the many different modes of sex determination found in reptiles and discuss the evidence for adaptive sex allocation in reptilian systems.

There is no unauthorized breeding at Jurassic Park…because all the animals in Jurassic Park are female. We’ve engineered them that way

Dr. Henry Wu, Chief Geneticist at Jurassic Park

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References

  • 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 

  • Bulmer M, Bull J (1982) Models of polygenic sex determination and sex ratio control. Evolution 36:13–26

    Article  CAS  PubMed  Google Scholar 

  • Burger J, Zappalorti R (1988) Effects of incubation temperature on sex ratios in pine snakes: differential vulnerability of males and females. Am Nat 132(4):492–505

    Article  Google Scholar 

  • Burke RL (1993) Adaptive value of sex determination mode and hatchling sex ratio bias in reptiles. Copeia 1993(3):854–859

    Article  Google Scholar 

  • Calsbeek R, Sinervo B (2002) Uncoupling direct and indirect components of female choice in the wild. Proc Natl Acad Sci 99(23):14897–14902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calsbeek R, Sinervo B (2004) Within-clutch variation in offspring sex determined by differences in sire body size: cryptic mate choice in the wild. J Evol Biol 17(2):464–470

    Article  PubMed  Google Scholar 

  • Charnov EL, Bull J (1977) When is sex environmentally determined? Nature 266(5605):828–830

    Article  CAS  PubMed  Google Scholar 

  • Cohen M, Gans C (1970) The chromosomes of the order Crocodilia. Cytogenetic 9(2):81–105

    Article  CAS  Google Scholar 

  • Cox RM, Calsbeek R (2010) Cryptic sex-ratio bias provides indirect genetic benefits despite sexual conflict. Science 328(5974):92–94

    Article  CAS  PubMed  Google Scholar 

  • Cox RM, Duryea MC, Najarro M, Calsbeek R (2011) Paternal condtion drives progeny sex ratio bias in a lizard that lacks parental care. Evolution 65(1):220–230

    Article  PubMed  Google Scholar 

  • Demas S, Duronslet M, Wachtel S, Caillouet C, Nakamura D (1990) Sex-specific DNA in reptiles with temperature sex determination. J Exp Zool 253(3):319–324

    Article  CAS  PubMed  Google Scholar 

  • Dunlap KD, Lang JW (1990) Offspring sex ratio varies with maternal size in the common garter snake, Thamnophis sirtalis. Copeia 1990(2):568–570

    Article  Google Scholar 

  • Elphick MJ, Shine R (1999) Sex differences in optimal incubation temperatures in a scincid lizard species. Oecologia 118(4):431–437

    Article  PubMed  Google Scholar 

  • Ewert MA, Nelson CE (1991) Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1991:50–69

    Article  Google Scholar 

  • Ewert MA, Jackson DR, Nelson CE (1994) Patterns of temperature-dependent sex determination in turtles. J Exp Zool 270(1):3–15

    Article  Google Scholar 

  • Ezaz T, Quinn AE, Miura I, Sarre SD, Georges A, Graves JAM (2005) The dragon lizard Pogona vitticeps has ZZ/ZW micro-sex chromosomes. Chromosom Res 13(8):763–776

    Article  CAS  Google Scholar 

  • Fisher R (1930) Genetical theory of sex allocation. Claredon Press, London

    Google Scholar 

  • Freedberg S, Wade MJ (2001) Cultural inheritance as a mechanism for population sex-ratio bias in reptiles. Evolution 55(5):1049–1055

    Article  CAS  PubMed  Google Scholar 

  • Gibbons JW, Scott DE, Ryan TJ, Buhlmann KA, Tuberville TD, Metts BS, Greene JL, Mills T, Leiden Y, Poppy S (2000) The Global Decline of Reptiles, DĂ©jĂ  Vu Amphibians Reptile species are declining on a global scale. Six significant threats to reptile populations are habitat loss and degradation, introduced invasive species, environmental pollution, disease, unsustainable use, and global climate change. Bioscience 50(8):653–666

    Article  Google Scholar 

  • González JE (2004) Inheritance of nest-site choice in the field in a turtle with temperature-dependent sex determination. Doctoral dissertation. Iowa State University

    Google Scholar 

  • Harlow PS, Taylor JE (2000) Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Austral Ecol 25(6):640–652

    Article  Google Scholar 

  • Hays GC, Fossette S, Katselidis KA, Schofield G, Gravenor MB (2010) Breeding periodicity for male sea turtles, operational sex ratios, and implications in the face of climate change. Conserv Biol 24(6):1636–1643

    Article  PubMed  Google Scholar 

  • Holleley CE, O’Meally D, Sarre SD, Graves JAM, Ezaz T, Matsubara K, Azad B, Zhang X, Georges A (2015) Sex reversal triggers the rapid transition from genetic to temperature-dependent sex. Nature 523(7558):79–82

    Article  CAS  PubMed  Google Scholar 

  • Janzen FJ (1994) Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci 91(16):7487–7490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Janzen FJ, Krenz JG (2004) Which was first, TSD or GSD? In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, DC, pp 121–130

    Google Scholar 

  • Janzen FJ, Morjan CL (2002) Egg size, incubation temperature, and posthatching growth in painted turtles (Chrysemys picta). J Herpetol 36(2):308–311

    Article  Google Scholar 

  • Janzen FJ, Paukstis GL (1991) Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q Rev Biol 66(2):149–179

    Article  CAS  PubMed  Google Scholar 

  • Janzen F, Phillips P (2006) Exploring the evolution of environmental sex determination, especially in reptiles. J Evol Biol 19(6):1775–1784

    Article  CAS  PubMed  Google Scholar 

  • Ji X, Lin LH, Luo LG, Lu HL, Gao JF, Han J (2006) Gestation temperature affects sexual phenotype, morphology, locomotor performance, and growth of neonatal brown forest skinks, Sphenomorphus indicus. Biol J Linn Soc 88(3):453–463

    Article  Google Scholar 

  • Juliana JRS, Bowden RM, Janzen FJ (2004) The impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle, Chelydra serpentina. Behav Ecol Sociobiol 56(3):270–278

    Article  Google Scholar 

  • Kamel SJ, Mrosovsky N (2005) Repeatability of nesting preferences in the hawksbill sea turtle, Eretmochelys imbricata, and their fitness consequences. Anim Behav 70(4):819–828

    Article  Google Scholar 

  • Kolbe JJ, Janzen FJ (2002) Impact of nest-site selection on nest success and nest temperature in natural and disturbed habitats. Ecology 83(1):269–281

    Article  Google Scholar 

  • Lemen CA, Voris HK (1981) A comparison of reproductive strategies among marine snakes. J Anim Ecol 50:89–101

    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 

  • McGaugh SE, Schwanz LE, Bowden RM, Gonzalez JE, Janzen FJ (2009) Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination. Proc Biol Sci 277(1685):1219–1226

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller D, Summers J, Silber S (2004) Environmental versus genetic sex determination: a possible factor in dinosaur extinction? Fertil Steril 81(4):954–964

    Article  CAS  PubMed  Google Scholar 

  • Mitchell NJ, Nelson NJ, Cree A, Pledger S, Keall SN, Daugherty CH (2006) Support for a rare pattern of temperature-dependent sex determination in archaic reptiles: evidence from two species of tuatara (Sphenodon). Front Zool 3(1):9

    Article  PubMed  PubMed Central  Google Scholar 

  • Morjan CL (2003) Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination. Behav Ecol Sociobiol 53(4):254–261

    Article  Google Scholar 

  • Mork L, Czerwinski M, Capel B (2014) Predetermination of sexual fate in a turtle with temperature-dependent sex determination. Dev Biol 386(1):264–271

    Article  CAS  PubMed  Google Scholar 

  • Mrosovsky N, Pieau C (1991) Transitional range of temperature, pivotal temperatures and thermosensitive stages for sex determination in reptiles. Amphibia-Reptilia 12(2):169–179

    Article  Google Scholar 

  • O’Steen S (1998) Embryonic temperature influences juvenile temperature choice and growth rate in snapping turtles Chelydra serpentina. J Exp Biol 201(3):439–449

    Google Scholar 

  • O’Steen S, Janzen FJ (1999) Embryonic temperature affects metabolic compensation and thyroid hormones in hatchling snapping turtles. Physiol Biochem Zool 72(5):520–533

    Article  PubMed  Google Scholar 

  • Olsson M, Madsen T, Wapstra E, Silverin B, Ujvari B, Wittzell H (2005a) MHC, health, color, and reproductive success in sand lizards. Behav Ecol Sociobiol 58(3):289–294

    Article  Google Scholar 

  • Olsson M, Wapstra E, Uller T (2005b) Differential sex allocation in sand lizards: bright males induce daughter production in a species with heteromorphic sex chromosomes. Biol Lett 1(3):378–380

    Article  PubMed  PubMed Central  Google Scholar 

  • Paitz RT, Clairardin SG, Griffin AM, Holgersson MC, Bowden RM (2010) 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 

  • Paladino FV, Dodson P, Hammond JK, Spotila JR (1989) Temperature-dependent sex determination in dinosaurs? Implications for population dynamics and extinction. Geol Soc Am Spec Pap 238:63–70

    Google Scholar 

  • Parrott BB, Kohno S, Cloy-McCoy JA, Guillette 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

    Article  PubMed  Google Scholar 

  • Peare T, Parker PG (1996) Local genetic structure within two rookeries of Chelonia mydas (the green turtle). Heredity 77(6):619–628

    Article  PubMed  Google Scholar 

  • Place AR, Lance VA (2004) The temperature-dependent sex determination drama: same cast, different stars. In: Valenzuela N, Lance VA (eds) Temperature dependent sex determination in vertebrates. Smithsonian Institution, Washington, DC, pp 99–110

    Google Scholar 

  • Quinn AE, Georges A, Sarre SD, Guarino F, Ezaz T, Graves JAM (2007) Temperature sex reversal implies sex gene dosage in a reptile. Science 316(5823):411–411

    Article  CAS  PubMed  Google Scholar 

  • Radder RS, Quinn AE, Georges A, Sarre SD, Shine R (2008) Genetic evidence for co-occurrence of chromosomal and thermal sex-determining systems in a lizard. Biol Lett 4(2):176–178

    Article  CAS  PubMed  Google Scholar 

  • Radder RS, Pike DA, Quinn AE, Shine R (2009) Offspring sex in a lizard depends on egg size. Curr Biol 19(13):1102–1105

    Article  CAS  PubMed  Google Scholar 

  • Reinhold K (1998) Nest-site philopatry and selection for environmental sex determination. Evol Ecol 12(2):245–250

    Article  Google Scholar 

  • Rhen T, Lang JW (1995) Phenotypic plasticity for growth in the common snapping turtle: effects of incubation temperature, clutch, and their interaction. Am Nat 146(5):726–747

    Article  Google Scholar 

  • Rhen T, Lang JW (1999) Incubation temperature and sex affect mass and energy reserves of hatchling snapping turtles, Chelydra serpentina. Oikos 86:311–319

    Article  Google Scholar 

  • Riley JL, Tattersall GJ, Litzgus JD (2014) Potential sources of intra-population variation in the overwintering strategy of painted turtle (Chrysemys picta) hatchlings. J Exp Biol 217(23):4174–4183

    Article  PubMed  Google Scholar 

  • Robert KA, Thompson MB (2001) Sex determination: viviparous lizard selects sex of embryos. Nature 412(6848):698–699

    Article  CAS  PubMed  Google Scholar 

  • Robert KA, Thompson MB, Seebacher F (2003) Facultative sex allocation in the viviparous lizard Eulamprus tympanum, a species with temperature-dependent sex determination. Aust J Zool 51(4):367–370

    Article  Google Scholar 

  • Roosenburg WM (1996) Maternal condition and nest site choice: an alternative for the maintenance of environmental sex determination? Am Zool 36(2):157–168

    Article  Google Scholar 

  • Roosenburg WM, Kelley KC (1996) The effect of egg size and incubation temperature on growth in the turtle, Malaclemys terrapin. J Herpetol 30:198–204

    Article  Google Scholar 

  • Sarre SD, Georges A, Quinn A (2004) The ends of a continuum: genetic and temperature-dependent sex determination in reptiles. Bioessays 26(6):639–645

    Article  PubMed  Google Scholar 

  • Sarre SD, Ezaz T, Georges A (2011) Transitions between sex-determining systems in reptiles and amphibians. Annu Rev Genomics Hum Genet 12:391–406

    Article  CAS  PubMed  Google Scholar 

  • Schwanz LE, Janzen FJ, Proulx SR (2010) Sex allocation based on relative and absolute condition. Evolution 64(5):1331–1345

    PubMed  Google Scholar 

  • Shine R (1999) Why is sex determined by nest temperature in many reptiles? Trends Ecol Evol 14(5):186–189

    Article  CAS  PubMed  Google Scholar 

  • Shine R (2002) Eggs in autumn: responses to declining incubation temperatures by the eggs of montane lizards. Biol J Linn Soc 76(1):71–77

    Google Scholar 

  • Shine R, Elphick M, Donnellan S (2002) Co-occurrence of multiple, supposedly incompatible modes of sex determination in a lizard population. Ecol Lett 5(4):486–489

    Article  Google Scholar 

  • Spencer R-J, Janzen FJ (2014) A novel hypothesis for the adaptive maintenance of environmental sex determination in a turtle. Proc R Soc Lond B Biol Sci 281(1789):20140831

    Article  Google Scholar 

  • Tang X-L, Yue F, Yan X-F, Zhang D-J, Xin Y, Wang C, Chen Q (2012) Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude. J Therm Biol 37(6):438–444

    Article  Google Scholar 

  • Valenzuela NM, Janzen FJ (2001) Nest-site philopatry and the evolution of temperature-dependent sex determination. Evol Ecol Res 3:779–794

    Google Scholar 

  • Valenzuela N, Lance V (2004) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, DC

    Google Scholar 

  • Valenzuela N, Badenhorst D, Montiel EE, Literman R (2014) Molecular cytogenetic search for cryptic sex chromosomes in painted turtles Chrysemys picta. Cytogenet Genome Res 144(1):39–46

    Article  PubMed  Google Scholar 

  • Viets BE, Tousignant A, Ewert MA, Nelson CE, Crews D (1993) Temperature-dependent sex determination in the leopard gecko, Eublepharis macularius. J Exp Zool A Ecol Genet Physiol 265(6):679–683

    CAS  Google Scholar 

  • Wapstra E, Olsson M, Shine R, Edwards A, Swain R, Joss JM (2004) Maternal basking behaviour determines offspring sex in a viviparous reptile. Proc R Soc Lond B Biol Sci 271(Suppl 4):S230–S232

    Article  Google Scholar 

  • Warner DA, Shine R (2007) Reproducing lizards modify sex allocation in response to operational sex ratios. Biol Lett 3(1):47–50

    Article  PubMed  Google Scholar 

  • Warner DA, Shine R, Schwenk K (2005) The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard. Evolution 59(10):2209–2221

    Article  PubMed  Google Scholar 

  • Warner DA, Lovern MB, Shine R (2007) Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination. Proc R Soc Lond B Biol Sci 274(1611):883–890

    Article  CAS  Google Scholar 

  • Warner DA, Uller T, Shine R (2013) Transgenerational sex determination: the embryonic environment experienced by a male affects offspring sex ratio. Sci Rep 3:4

    Article  Google Scholar 

  • Weatherhead PJ, Brown GP, Prosser MR, Kissner KJ (1998) Variation in offspring sex ratios in the northern water snake (Nerodia sipedon). Can J Zool 76(12):2200–2206

    Article  Google Scholar 

  • Zaborski P, Dorizzi M, Pieau C (1982) H-Y antigen expression in temperature sex-reversed turtles (Emys orbicularis). Differentiation 22(1–3):73–78

    Article  CAS  PubMed  Google Scholar 

  • Zaborski P, Dorizzi M, Pieau C (1988) Temperature-dependent gonadal differentiation in the turtle Emys orbicularis: concordance between sexual phenotype and serological H-Y antigen expression at threshold temperature. Differentiation 38(1):17–20

    Article  CAS  PubMed  Google Scholar 

  • Zhang D-J, Tang X-L, Yue F, Chen Z, Chen Q (2010) Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata. J Therm Biol 35(3):129–133

    Article  Google Scholar 

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Navara, K.J. (2018). What Went Wrong at Jurassic Park? Modes of Sex Determination and Adaptive Sex Allocation in Reptiles. In: Choosing Sexes. Fascinating Life Sciences. Springer, Cham. https://doi.org/10.1007/978-3-319-71271-0_8

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