, Volume 160, Issue 3, pp 493–506

Temperature-dependent sex determination and global change: are some species at greater risk?

  • Vincent Hulin
  • Virginie Delmas
  • Marc Girondot
  • Matthew H. Godfrey
  • Jean-Michel Guillon
Population Ecology - Original Paper


In species with temperature-dependent sex determination (TSD), global climate change may result in a strong sex ratio bias that could lead to extinction. The relationship between sex ratio and egg incubation at constant temperature in TSD species is characterized by two parameters: the pivotal temperature (P) and the transitional range of temperature that produces both sexes (TRT). Here, we show that the proportion of nests producing both sexes is positively correlated to the width of the TRT by a correlative approach from sex ratio data collected in the literature and by simulations of TSD using a mechanistic model. From our analyses, we predict that species with a larger TRT should be more likely to evolve in response to new thermal conditions, thus putting them at lower risk to global change.


Pivotal temperature Transitional range of temperature Global warming Sex ratio Turtles 


  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automat Contr 19:716–723CrossRefGoogle Scholar
  2. Bell G, Collins S (2008) Adaptation, extinction and global change. Evol Appl 1:3–16CrossRefGoogle Scholar
  3. Binckley CA, Spotila JR, Wilson KS, Paladino FV (1998) Sex determination and sex ratios of pacific leatherback turtles, Dermochelys coriacea. Copeia 2:291–300CrossRefGoogle Scholar
  4. Bowden RM, Ewert MA, Nelson CE (2000) Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc R Soc London B Biol Sci 267:1745–1749CrossRefGoogle Scholar
  5. Bowden RM, Harms HK, Paitz RT, Janzen FJ (2004) Does optimal egg size vary with demographic stage because of a physiological constraint? Funct Ecol 18:522–529CrossRefGoogle Scholar
  6. Bull JJ (1980) Sex determination in reptiles. Q Rev Biol 55:3–21CrossRefGoogle Scholar
  7. Bull JJ (1983) Environmental sex determination (ESD). Evolution of sex determining mechanisms. Benjamin-Cummings, Menlo Park, CAGoogle Scholar
  8. Bull JJ (1985) Sex ratio and nest temperature in turtles: comparing field and laboratory data. Ecology 66:1115–1122CrossRefGoogle Scholar
  9. Bull JJ, Vogt RC (1979) Temperature-dependent sex determination in turtles. Science 206:1186–1188PubMedCrossRefGoogle Scholar
  10. Bull JJ, Vogt RC, Bulmer MG (1982a) Heritability of sex ratio in turtles with environmental sex determination. Evolution 35:333–341CrossRefGoogle Scholar
  11. Bull JJ, Vogt RC, McCoy CJ (1982b) Sex determining temperatures in turtles: a geographic comparison. Evolution 36:13–26CrossRefGoogle Scholar
  12. Davenport J (1997) Temperature and the life-history strategies of sea turtles. J Therm Biol 22:479–488CrossRefGoogle Scholar
  13. De Souza RR, Vogt RC (1994) Incubation temperature influences sex and hatchling size in the neotropical turtle Podocnemis unifilis. J Herpetol 28:453–464CrossRefGoogle Scholar
  14. Delmas V, Prévot-Julliard A-C, Pieau C, Girondot M (2008) A mechanistic model of temperature-dependent sex determination in a Chelonian, the European pond turtle. Funct Ecol 22:84–93Google Scholar
  15. Demuth JP (2001) The effects of constant and fluctuating incubation temperatures on sex determination, growth, and performance in the tortoise Gopherus polyphemus. Can J Zool 79:1609–1620CrossRefGoogle Scholar
  16. Doody S, Guarino E, Georges A, Corey B, Murray G, Ewert MA (2006) Nest site choice compensates for climate effects on sex ratio in a lizard with environmental sex determination. Evol Ecol 20:307–330CrossRefGoogle Scholar
  17. Eendebak BT (1995) Incubation period and sex ratio of Hermann’s Tortoise. Chelonian Conserv Biol 1:227–231Google Scholar
  18. Etchberger CR, Ewert MA, Raper BA, Nelson CE (1992) Do low incubation temperatures yield females in painted turtles? Can J Zool 70:391–394CrossRefGoogle Scholar
  19. Ewert MA, Nelson CE (1991) Sex determination in turtles: diverse patterns and some possible adaptive values. Copeia 1:50–69CrossRefGoogle Scholar
  20. Ewert MA, Jackson DR, Nelson CE (1994) Patterns of temperature-dependent sex determination in turtles. J Exp Zool 270:3–15CrossRefGoogle Scholar
  21. Ewert MA, Etchberger CR, Nelson CE (2004a) Turtle sex-determination modes and TSD patterns, and some TSD pattern correlates. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, DC, pp 21–32Google Scholar
  22. Ewert MA, Hatcher RE, Goode JM (2004b) Sex determination and ontogeny in Malacochersus tornieri, the Pancake tortoise. J Herpetol 38:291–295CrossRefGoogle Scholar
  23. Ewert MA, Lang JW, Nelson CE (2005) Geographic variation in the pattern of temperature-dependent sex determination in the American snapping turtle (Chelydra serpentina). J Zool Lond 265:81–95CrossRefGoogle Scholar
  24. Freedberg S, Wade MJ (2001) Cultural inheritance as a mechanism for population sex-ratio bias in reptiles. Evolution 55:1049–1055PubMedCrossRefGoogle Scholar
  25. Georges A, Limpus CJ, Stoutjestjik 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 270:432–444CrossRefGoogle Scholar
  26. Georges A, Doody S, Beggs K, Young JE (2004) Thermal models of TSD under laboratory and field conditions. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, DC, pp 79–89Google Scholar
  27. Georges A, Beggs K, Young JE, Doody S (2005) Modelling development of reptile embryos under fluctuating temperature regimes. Physiol Biochem Zool 78:18–30PubMedCrossRefGoogle Scholar
  28. Girondot M (1999) Statistical description of temperature-dependent sex determination using maximum likelihood. Evol Ecol Res 1:479–486Google Scholar
  29. Girondot M, Delmas V, Rivalan P, Courchamp F, Prévot-Julliard A-C, Godfrey MH (2004) Implication of temperature-dependent sex determination for population dynamics. In: Valenzuela N, Bull JJ (eds) Temperature-dependent sex determination. Smithsonian Books, Washington, pp 148–155Google Scholar
  30. Glen F, Mrosovsky N (2004) Antigua revisited: the impact of climate change on sand and nest temperatures at a hawksbill turtle (Eretmochelys imbricata) nesting beach. Glob Chang Biol 10:2036–2045CrossRefGoogle Scholar
  31. Godfrey MH, Mrosovsky N (2006) Pivotal temperature for green turtles, Chelonia mydas, nesting in Suriname. Herpetol J 16:55–61Google Scholar
  32. Godfrey MH, Barreto R, Mrosovsky N (1996) Estimating past and present sex ratios of sea turtles in Suriname. Can J Zool 74:267–277CrossRefGoogle Scholar
  33. Godfrey MH, D’Amato AF, Marcovaldi MÂ, Mrosovsky N (1999) Pivotal temperature and predicted sex ratios for hatchling hawksbill turtles from Brazil. Can J Zool 77:1465–1473CrossRefGoogle Scholar
  34. Godfrey MH, Delmas V, Girondot M (2003) Assessment of patterns of temperature-dependent sex determination using maximum likelihood model selection. Ecoscience 10:265–272Google Scholar
  35. Gutzke WHN, Paukstis GL (1983) Influence of the hydric environment on sexual differentiation of turtles. J Exp Zool 226:467–469PubMedCrossRefGoogle Scholar
  36. Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Glob Chang Biol 13:923–932CrossRefGoogle Scholar
  37. Hoerl AE, Kennard RW (1970) Ridge regression: biased estimation for nonorthogonal problems. Technometrics 12:55–67CrossRefGoogle Scholar
  38. Hulin V, Girondot M, Godfrey MH, Guillon J-M (2008) Mixed and uniform brood sex ratio strategy in turtles: the facts, the theory and their consequences. In: Wyneken J, Bels V, Godfrey MH (eds) Turtles: from structures to strategies of life. CRC, Boca Raton, pp 279–300Google Scholar
  39. Hurvich CM, Tsai C-L (1989) Regression and time series model selection in small samples. Biometrika 76:297–307CrossRefGoogle Scholar
  40. IPCC (2007) Climate Change 2007: the physical basis. Contribution of Working Group I to the fourth assessment. Report of the intergovernmental panel on climate change. Cambridge University Press, CambridgeGoogle Scholar
  41. Janzen FJ (1992) Heritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina). Genetics 131:155–161PubMedGoogle Scholar
  42. Janzen FJ (1994) Climate change and temperature-dependent sex determination in reptiles. Proc Natl Acad Sci USA 91:7487–7490PubMedCrossRefGoogle Scholar
  43. Jump AS, Penuelas J (2005) Running to stand still: adaptation and the response of plants to rapid climate change. Ecol Lett 8:1010–1020CrossRefGoogle Scholar
  44. Lang JW, Andrews HV (1994) Temperature-dependent sex determination in crocodilians. J Exp Zool 270:28–44CrossRefGoogle Scholar
  45. Lewis-Winokur V, Winokur RM (1995) Incubation temperature affects sexual differentiation, incubation time, and posthatchling survival in desert tortoise (Gopherus agassizi). Can J Zool 73:2091–2097CrossRefGoogle Scholar
  46. Limpus CJ, Reed PC, Miller JD (1985) Temperature dependent sex determination in Queensland sea turtles: intraspecific variation in Caretta caretta. In: Grigg G, Shine R, Ehmann H (eds) Biology of Australasian frogs and reptiles. Royal Zoological Society, Sydney, pp 343–351Google Scholar
  47. Marcovaldi MÂ, Godfrey MH, Mrosovsky N (1997) Estimating sex ratios of loggerhead turtles in Brazil from pivotal incubation durations. Can J Zool 75:755–770CrossRefGoogle Scholar
  48. Maxwell JA, Motara MA, Frank GH (1988) A micro-environmental study of the effect of temperature on the sex ratios of the loggerhead turtle, Caretta caretta, from Tongaland, Natal. S Afr J Zool 23:342–350Google Scholar
  49. McCoy CJ, Vogt RC, Censky EJ (1983) Temperature-controlled sex determination in the sea turtle Lepidochelys olivacea. J Herpetol 17:404–406CrossRefGoogle Scholar
  50. Miller D, Summers J, Silber S (2004) Environmental versus genetic sex determination: a possible factor in dinosaur extinction? Fertil Steril 81:954–964PubMedCrossRefGoogle Scholar
  51. Morjan CL (2003a) How rapidly can maternal behavior affecting primary sex ratio evolve in a reptile with environmental sex determination? Am Nat 162:205–219PubMedCrossRefGoogle Scholar
  52. Morjan CL (2003b) Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination. Behav Ecol Sociobiol 53:254–261CrossRefGoogle Scholar
  53. Mrosovsky N (1982) Sex ratio bias in hatchling sea turtles from artificially incubated eggs. Biol Conserv 23:309–314CrossRefGoogle Scholar
  54. Mrosovsky N (1988) Pivotal temperatures for loggerhead turtles (Caretta caretta) from northern and southern nesting beaches. Can J Zool 66:661–669CrossRefGoogle Scholar
  55. Mrosovsky N, Benabib M (1990) An assessment of 2 methods of sexing hatchling sea-turtles. Copeia 2:589–591CrossRefGoogle Scholar
  56. Mrosovsky N, Provancha J (1989) Sex ratio of loggerhead sea turtles hatching on a Florida beach. Can J Zool 67:2533–2539CrossRefGoogle Scholar
  57. Mrosovsky N, Provancha J (1992) Sex ratio of hatchling loggerhead sea turtles: data and estimates from a 5-year study. Can J Zool 70:530–538CrossRefGoogle Scholar
  58. Mrosovsky N, Dutton PH, Whitmore CP (1984a) Sex-ratios of two species of sea turtle nesting in Suriname. Can J Zool 62:2227–2239CrossRefGoogle Scholar
  59. Mrosovsky N, Hopkins-Murphy SR, Richardson JE (1984b) Sex ratios of sea turtles: seasonal changes. Science 225:739–741PubMedCrossRefGoogle Scholar
  60. Mrosovsky N, Bass A, Corliss LA, Richardson JI, Richardson TH (1992) Pivotal and beach temperatures for hawksbill turtles nesting in Antigua. Can J Zool 70:1920–1925CrossRefGoogle Scholar
  61. Mrosovsky N, Baptistotte C, Godfrey MH (1999) Validation of incubation duration as an index of the sex ratio of hatchling sea turtles. Can J Zool 77:831–835CrossRefGoogle Scholar
  62. Mrosovsky N, Kamel SJ, Rees AF, Margaritoulis D (2002) Pivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, Greece. Can J Zool 80:2118–2124CrossRefGoogle Scholar
  63. Nelson NJ, Thompson MB, Pledger S, Keall SN, Daugherty CH (2004) Do TSD, sex ratios, and nest characteristics influence the vulnerability of tuatara to global warming? Int Congr Ser 1275:250–257CrossRefGoogle Scholar
  64. Packard GC, Packard MJ, Birchard GF (1989) Sexual-differentiation and hatching success by painted turtles incubating in different thermal and hydric environments. Herpetologica 45:385–392Google Scholar
  65. Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669CrossRefGoogle Scholar
  66. Pertoldi C, Bach LA (2007) Evolutionary aspects of climate-induced changes and the need for multidisciplinarity. J Therm Biol 32:118–124CrossRefGoogle Scholar
  67. Pieau C (1971) Sur la proportion sexuelle chez les embryons de deux Chéloniens (Testudo graeca L. et Emys orbicularis L.) issues d’oeufs incubés articifiellement. C R Acad Sci Paris 272:3071–3074Google Scholar
  68. Pieau C (1972) Effets de la température sur le développement des glandes génitales chez les embryons de deux chéloniens, Emys orbicularis L. et Testudo graeca L. C R Acad Sci Paris 274:719–722Google Scholar
  69. Pieau C (1975) Temperature and sex differentiation in embryos of two Chelonians, Emys orbicularis L. and Testudo graeca L. In: Reinboth R (ed) Intersexuality in the Animal Kingdom. Springer, New York, pp 332–339Google Scholar
  70. Pieau C (1982) Modalities of the action of temperature on sexual differentiation in field-developing embryos of the European pond turtle Emys orbicularis (Emydidae). J Exp Zool 220:353–360CrossRefGoogle Scholar
  71. Pieau C, Girondot M, Desvages G, Dorizzi M, Richard-Mercier N, Zaborski P (1994) Environmental control of gonadal differentiation. In: Short RV, Balaban E (eds) The differences between the sexes. Cambridge University Press, Cambridge, pp 433–448Google Scholar
  72. Pieau C, Dorizzi M, Richard-Mercier N, Desvages G (1999) Sexual differentiation of gonads as a function of temperature in the turtle Emys orbicularis: Endocrine function, intersexuality and growth. J Exp Zool 281:400–408CrossRefGoogle Scholar
  73. Raynaud A, Pieau C (1985) Embryonic development of the genital system. In: Gans C, Billett FS (eds) Biology of the reptilia. Wiley, New York, pp 149–300Google Scholar
  74. Rhen T, Lang JW (1998) Among-family variation for environmental sex determination in reptiles. Evolution 52:1514–1520CrossRefGoogle Scholar
  75. Rimblot F, Fretey J, Mrosovsky N, Lescure J, Pieau C (1985) Sexual differentiation as a function of the incubation temperature of eggs in the sea-turtle Dermochelys coriacea (Vandelli, 1761). Amphib-Reptil 6:83–92CrossRefGoogle Scholar
  76. Rimblot-Baly F, Lescure J, Fretey J, Pieau C (1987) Sensibilité à la température de la différenciation sexuelle chez la tortue luth, Dermochelys coriacea (Vandelli, 1761); application des données de l’incubation artificielle à l’étude de la sex-ratio dans la nature. Ann Sci Nat Zool Paris 8:277–290Google Scholar
  77. Spotila JR et al (1994) Effects of incubation conditions on sex determination, hatching success, and growth of hatchling desert tortoises, Gopherus agassizii. Herpetol Monogr 8:103–116CrossRefGoogle Scholar
  78. Stainforth D et al (2005) Uncertainty in predictions of the climate response to rising levels of greenhouse gases. Nature 433:403–406PubMedCrossRefGoogle Scholar
  79. Sugiura N (1978) Further analysis of the data by Akaike’s information criterion and the finite corrections. Commun Stat A 7:13–26CrossRefGoogle Scholar
  80. Vaillant S, Dorizzi M, Pieau C, Richard-Mercier N (2001) Sex reversal and aromatase in chicken. J Exp Zool 290:727–740PubMedCrossRefGoogle Scholar
  81. Valenzuela N (2001) Constant, shift, and natural temperature effects on sex determination in Podocnemis expansa turtles. Ecology 82:3010–3024Google Scholar
  82. Valenzuela N (2004) Introduction. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates, vol 1. Smithsonian Books, Washington, DC, pp 1–4Google Scholar
  83. Valenzuela N, Botero R, Martinez E (1997) Field study of sex determination in Podocnemis expansa from Colombian Amazonia. Herpetologica 53:390–398Google Scholar
  84. Viets BE, Ewert MA, Talent G, Nelson CE (1994) Sex-determining mechanisms in squamate reptiles. J Exp Zool 270:45–56CrossRefGoogle Scholar
  85. Vogt RC, Flores Villela O (1992) Effects of incubation temperature on sex determination in a community of Neotropical freshwater turtles in southern Mexico. Herpetologica 48:265–270Google Scholar
  86. Walther G-R et al (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  87. Weishampel J, Bagley DA, Ehrhart LM, Rodenbeck B (2003) Spatiotemporal patterns of annual sea turtle nesting behaviors along an East Central Florida beach. Biol Conserv 110:295–303CrossRefGoogle Scholar
  88. Whitmore CP, Dutton PH, Mrosovsky N (1985) Sexing of hatchling sea turtles—gross appearance versus histology. J Herpetol 19:430–431CrossRefGoogle Scholar
  89. Wibbels T, Killebrew FC, Crews D (1991) Sex determination in Cagle’s map turtle: implications for evolution, development, and conservation. Can J Zool 69:2693–2696CrossRefGoogle Scholar
  90. Wibbels T, Rostal DC, Byles R (1998) High pivotal temperature in the sex determination of the olive ridley sea turtle, Lepidochelys olivacea, from Playa Nancite, Costa Rica. Copeia 1998:1086–1088Google Scholar
  91. Yntema CL, Mrosovsky N (1982) Critical periods and pivotal temperatures for sexual differentiation in loggerhead sea turtles. Can J Zool 60:1012–1016CrossRefGoogle Scholar
  92. Zwiers FW (2002) The 20-year forecast. Nature 416:690–691PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Vincent Hulin
    • 1
    • 2
  • Virginie Delmas
    • 1
    • 2
    • 3
  • Marc Girondot
    • 1
    • 2
    • 4
  • Matthew H. Godfrey
    • 5
  • Jean-Michel Guillon
    • 1
    • 2
  1. 1.Laboratoire Ecologie, Systématique et Evolution (UMR8079), Faculté des Sciences d’OrsayUniversité Paris-SudOrsayFrance
  2. 2.AgroParisTechCNRSOrsayFrance
  3. 3.Centre d’Etudes Biologiques de ChizéCNRSBeauvoir-sur-NiortFrance
  4. 4.Département de Systématique et EvolutionMuséum National d’Histoire Naturelle de ParisParisFrance
  5. 5.North Carolina Wildlife Resources CommissionBeaufortUSA

Personalised recommendations