Evolutionary Ecology

, Volume 20, Issue 4, pp 307–330 | Cite as

Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination

  • J. Sean Doody
  • Enzo Guarino
  • Arthur Georges
  • Ben Corey
  • Glen Murray
  • Michael Ewert
Research article


Theoretical models suggest that in changing environments natural selection on two traits, maternal nesting behaviour and pivotal temperatures (those that divide the sexes) is important for maintaining viable offspring sex ratios in species with environmental sex determination (ESD). Empirical evidence, however, is lacking. In this paper, we provide such evidence from a study of clinal variation in four sex-determining traits (maternal nesting behaviour, pivotal temperatures, nesting phenology, and nest depth) in Physignathus lesueurii, a wide-ranging ESD lizard inhabiting eastern Australia. Despite marked differences in air and soil temperatures across our five study sites spanning 19° latitude and 1200 m in elevation, nest temperatures did not differ significantly among sites. Lizards compensated for climatic differences chiefly by selecting more open nest sites with higher incident radiation at cooler sites. Clinal variation in the onset of nesting also compensated for climatic differences, but to a lesser extent. There was no evidence of compensation through pivotal temperatures or nest depth. More broadly, our results extend to the egg stage the life history prediction that behaviour is the chief compensatory mechanism for climatic differences experienced by species spanning environmental extremes. Furthermore, our study was unique in revealing that nest site choice influenced mainly the daily range in nest temperatures, rather than mean temperatures, in a shallow-nesting reptile. Finally, indirect evidence suggests that the cue used by nesting lizards was radiation or temperature (through basking or assessing substrate temperatures), not visual detection of canopy openness. We conclude that maternal nesting behaviour and nesting phenology are traits subject to sex ratio selection in P. lesueurii, and thus, must be considered among the repertoire of ESD species for responding to climate change.


lizard nest depth nest site choice nesting phenology Physignathus pivotal temperature temperature-dependent sex determination water dragon 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adolph, S.C., Porter, W.P. 1993Temperature, activity, and lizard life historiesAm. Nat.142273295CrossRefPubMedGoogle Scholar
  2. Bragg, W.K., Fawcett, J.D., Bragg, T.B, Viets, B.E. 2000Nest-site selection in two eublepharid gecko species with temperature-dependent sex determination and one with genotypic sex determinationBiol. J. Linn. Soc.69319332CrossRefGoogle Scholar
  3. Brown, J.H. 1995MacroecologyUniversity of Chicago PressChicagoGoogle Scholar
  4. Bull, J.J. 1980Sex determination in reptilesQuart. Rev. Biol.55321CrossRefGoogle Scholar
  5. Bull, J.J. 1983Evolution of Sex Determining MechanismsBenjamin CummingsCaliforniaGoogle Scholar
  6. Bull, J.J. 1987Temperature-sensitive periods of sex determination in a lizard: comparisons with crocodiles and turtlesJ. Exp. Zool.241143148CrossRefGoogle Scholar
  7. Bull, J.J., Vogt, R.C., Bulmer, M.G. 1982aHeritability of sex ratio in turtles with environmental sex determinationEvolution36333341CrossRefGoogle Scholar
  8. Bull, J.J., Vogt, R.C., McCoy, C.J. 1982bSex determining temperatures in turtles: A geographic comparisonEvolution36326332CrossRefGoogle Scholar
  9. Bull, J.J., Gutzke, W.H.N., Bulmer, M.G. 1988Nest choice in a captive lizard with temperature-dependent sex determinationJ. Evol. Biol.1177184CrossRefGoogle Scholar
  10. Bulmer, M.G., Bull, J.J. 1982Models of polygenic sex determination and sex ratio controlEvolution361326CrossRefGoogle Scholar
  11. Carvalho, A.B., Sampaio, M.C., Varandas, F.R., Klaczko, L.B. 1998An experimental demonstration of Fisher’s principle: Evolution of sexual proportion by natural selectionGenetics148719731PubMedGoogle Scholar
  12. Charnov, E.L. 1982The Theory of Sex AllocationPrinceton University PressNew JerseyGoogle Scholar
  13. Cogger, H. 2000Reptiles and Amphibians of AustraliaNew Holland ReedSydneyGoogle Scholar
  14. Conover, D.O. 2004

    Temperature-dependent sex determination in fishes

    Valenzuela, N.Lance, V. eds. Temperature-Dependent Sex Determination in VertebratesSmithsonian Institute PressWashington, DC1132
    Google Scholar
  15. Conover, D.O., Voorhees, D.A. 1990Evolution of a balanced sex ratio by frequency-dependent selection in a fishScience25015561158PubMedGoogle Scholar
  16. Darwin, C. 1871The Descent of Man and Selection in Relation to SexJohn MurrayLondonGoogle Scholar
  17. Davenport, J. 1997Temperature and the life history strategies of sea turtlesJ. Therm. Biol.22479488CrossRefGoogle Scholar
  18. Defaure, J.P., Hubert, J. 1961Table dé developpement du lézard vivipare: Lacerta (Zootoca) vivipara JacquinArchives d’Anatomie Microscopique et de Morphologie Experimentale50309328Google Scholar
  19. Doody, J.S., Georges, A., Young, J.E. 2004Determinants of reproductive success and offspring sex in a turtle with environmental sex determinationBiol. J. Linn. Soc.81116CrossRefGoogle Scholar
  20. Dunham, A.E., Grant, B.W., Overall, K.L. 1989Interfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectothermsPhysiol. Zool.62335355Google Scholar
  21. Ellner, L.R., Karasov, W.H. 1993Latitudinal variation in the thermal biology of ornate box turtlesCopeia1993447455CrossRefGoogle Scholar
  22. Ewert, M.A., Jackson, D.R., Nelson, C.E. 1994Patterns of temperature-dependant sex determination in turtlesJ. Exp. Zool.270315CrossRefGoogle Scholar
  23. Ewert, M.A., Etchberger, C.R., Nelson, C.E. 2004

    Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates

    Valenzuela, N.Lance, V. eds. Temperature-dependent Sex Determination in VertebratesSmithsonian Institution PressWashington, DC2132
    Google Scholar
  24. Ewert, M.A, Lang, J.W., Nelson, C.E. 2005Geographic variation in the pattern of temperature-dependant sex determination in the American snapping turtle (Chelydra serpenina)J. Zool.2658195CrossRefGoogle Scholar
  25. Fisher, R.A. 1930The Genetical Theory of Natural SelectionOxford University PressOxfordGoogle Scholar
  26. Folland, C.K., Karl, T.R., Christy, J.R., Clarke, R.A., Gruza, G.V., Jouzel, J., Mann, M.E., Oerlemans, J., Salinger, M.J., Wang, S.W. 2001

    Observed Climate Variability and Change

    Houghton, J.T.Ding, Y.Griggs, D.J.Noguer, M.Linden, Dai, X.Maskell, K.Johnson, C.A. eds. Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the intergovernmental Panel on Climate ChangeCambridge University PressCambridge, United Kingdom4994
    Google Scholar
  27. Forchhammer, M.C., Post, E., Stenseth, N.C. 1998Breeding phenology and climateNature3912930CrossRefGoogle Scholar
  28. Frazer, G.W., Canham, C.D., Lertzman, K.P. 1999Gap Light Analyser (GLA): Imaging Software to Extract Canopy Structure and Gap Light Transmission Indices from True-colour Fisheye Photographs, Users Manual and Program DocumentationSimon Fraser University, British Columbia; and the Institute of Ecosystem StudiesNew YorkGoogle Scholar
  29. Freedberg, S., Wade, M.J. 2004Male combat favours female-biased sex ratios under environmental sex determinationAnim. Behav.67177181CrossRefGoogle Scholar
  30. Georges, A. 1989Female turtles from hot nests: Is it duration of incubation or proportion of development that matters?Oecologia81323328Google Scholar
  31. Georges, A. 1992Thermal characteristics and sex determination in field nests of the pig-nosed turtle, Carettochelys insculpta (Chelonia: Carettochelydidae), from northern AustraliaAust. J. Zool.40511521CrossRefGoogle Scholar
  32. Georges, A., Limpus, C., Stoutjesdijk, R. 1994Hatchling sex in the marine turtle Caretta caretta is determined by proportion of development at a temperature, not daily duration of exposureJ. Exp. Zool.270432444CrossRefGoogle Scholar
  33. Georges, A., Doody, J.S., Beggs, K., Young, J.E. 2004

    Thermal models of TSD under laboratory and field conditions

    Valenzuela, N.Lance, V. eds. Temperature-Dependent Sex Determination in VertebratesSmithsonian Institution PressWashington, DC7989
    Google Scholar
  34. Giorgi, F., Hewitson, B., Christensen, J., Hulme, M., Storch, H., Whetton, P., Jones, R., Mearns, L., Fu, C. 2001

    Regional Climate Information – Evaluation and Projections

    Houghton, J.T.Ding, Y.Griggs, D.J.Noguer, M.van der, P.J.Dai, X.Maskell, K.Johnson, C.A. eds. Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate ChangeCambridge University PressCambridge, United Kingdom374407
    Google Scholar
  35. Giorgi, F.B., Fransisco, R. 2000Uncertainties in regional climate change prediction: a regional analysis of ensemble simulations with the HADCM2 coupled AOGCM’Clim. Dyn.16169182CrossRefGoogle Scholar
  36. Girondot, M., Delmas, V., Rivalan, P., Courchamp, F., Prevot-Julliard, A., Godfrey, M.H. 2004

    Implications of temperature-dependent sex determination for population dynamics

    Valenzuela, N.Lance, V. eds. Temperature-Dependent Sex Determination in VertebratesSmithsonian Institute PressWashington, DC148155
    Google Scholar
  37. Gvozdik, L. 2002To heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradientCan. J. Zool.80479492CrossRefGoogle Scholar
  38. Harlow, P.S. 1996A harmless technique for sexing hatchling lizardsHerpetol. Rev.277172Google Scholar
  39. Harlow P.S. (2001) The ecology of sex-determining mechanisms in Australian agamid lizards. Unpubl. PhD Thesis, Macquarie University, Sydney, AustraliaGoogle Scholar
  40. Harlow, P.S., Harlow, M.F. 1997Captive reproduction and longevity in the eastern water dragon (Physignathus lesueurii)Herpetofauna271419Google Scholar
  41. Hay, M. 1972The breeding of Physignathuslesueurii in captivityHerpetofauna523Google Scholar
  42. Hertz, P.E. 1992Temperature regulation in Puerto Rican Anolis lizards: a field test using null hypothesisEcology7314051417CrossRefGoogle Scholar
  43. Hertz, P.E., Huey, R.B. 1981Compensation for altitudinal changes in the thermal environment by some Anolis lizards on HispaniolaEcology62515521CrossRefGoogle Scholar
  44. Huey, R.B., Bennett, A.F. 1990Physiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspectiveCold Spring Harbor Monogr. Ser.193759Google Scholar
  45. Janzen, F.J. 1992Heritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina)Genetics131155161PubMedGoogle Scholar
  46. Janzen, F.J. 1994aVegetational cover predicts the sex ratio of hatchling turtles in natural nestsEcology7515931599CrossRefGoogle Scholar
  47. Janzen, F.J. 1994bClimate change and temperature-dependent sex determination in reptilesProc. Nat. Acad. Sci., USA9174877490CrossRefGoogle Scholar
  48. Janzen, F.J., Morjan, C.L. 2001Repeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determinationAnim. Behav.627382CrossRefGoogle Scholar
  49. Janzen, F.J., Paukstis, G.L. 1991Environmental sex determination in reptiles: ecology, evolution, and experimental designQuart. Rev. Biol.66149179PubMedCrossRefGoogle Scholar
  50. McCarty, J.P. 2001Ecological consequences of recent climate changeConser. Biol.15320331CrossRefGoogle Scholar
  51. Morjan, C.L. 2003Variation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determinationBehav. Ecol. Sociobiol.53254261CrossRefGoogle Scholar
  52. Mrosovsky, N., Kamel, S., Rees, A.F., Margaritoulis, D. 2002Pivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, GreeceCan. J. Zool.8021182124CrossRefGoogle Scholar
  53. Ohno, S. 1967Sex Chromosomes and Sex-linked GenesSpringer-VerlagBerlinGoogle Scholar
  54. Parmesan, C., Yohe, G. 2004A globally coherent fingerprint of climate change impacts across natural systemsNature4213742CrossRefGoogle Scholar
  55. Pringle, R.M., Webb, J.K, Shine, R. 2003Canopy structure, microclimate, and habitat selection by a nocturnal snake, Hoplocephalus bungaroidesEcology8426682679Google Scholar
  56. Rhen, T., Lang, J.W. 1998Among-family variation for environmental sex determination in reptilesEvolution5215141520CrossRefGoogle Scholar
  57. Roff, D.A. 1996The evolution of threshold traits in animalsQuart. Rev. Biol.71335CrossRefGoogle Scholar
  58. Roosenburg, W.M. 1996Maternal condition and nest site choice: An alternative for the maintenance of environmental sex determinationAm. Zool.36157168Google Scholar
  59. Root, T.L., Price, J.T., Hall, K.L. 2003Fingerprints of global warming on wild animals and plantsNature4215760PubMedCrossRefGoogle Scholar
  60. SAS Institute1998SAS 8.00SAS Institute IncCary, NCGoogle Scholar
  61. Shaw, R.F., Mohler, J.D. 1953The selective significance of the sex ratioAm. Nat.87337342CrossRefGoogle Scholar
  62. Shine, R. 1999Why is sex determined by nest temperature in many reptiles?TREE14186189PubMedGoogle Scholar
  63. Shine, R. 2002Reconstructing an adaptionist scenario: what selective forces favour the evolution of viviparity in montane reptiles?Am. Nat.16082593CrossRefGoogle Scholar
  64. Shine, R., Harlow, P.S. 1996Maternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizardEcology7718081817CrossRefGoogle Scholar
  65. Shine, R., Elphick, M.J., Barrott, E.G. 2003Sunny side up: lethally high, not low, nest temperatures may prevent oviparous reptiles from reproducing at high elevationsBiol. J. Linn. Soc.78325334CrossRefGoogle Scholar
  66. Shine, R., Elphick, M.J., Harlow, P.S. 1997The influence of natural incubation environments on the phenotypic traits of hatchling lizardsEcology7825592568CrossRefGoogle Scholar
  67. St Juliana, J.R., Bowden, R.M., Janzen, F.J. 2004The impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle, Chelydra serpentinaBehav. Ecol. Sociobiol.53270278Google Scholar
  68. Systat1998SYSTAT 8.0SPSS ScienceChicago, IllinoisGoogle Scholar
  69. Sæther, B.E, Tufto, J., Engen, S., Jerstad, K., Rostad, O.W., Skatan, K.E. 2000Population dynamical consequences of climate change for a small temperate songbirdScience287854856PubMedCrossRefGoogle Scholar
  70. Valenzuela, N. 2004

    Evolution and maintenance of temperature-dependent sex determination

    Valenzuela, N.Lance, v. eds. Temperature-Dependent Sex Determination in VertebratesSmithsonian Institution PressWashington, DC131147
    Google Scholar
  71. Vogt, R.C., Flores-Villela, O. 1992Effects of incubation temperature on sex determination in a community of neotropical freshwater turtles in southern MexicoHerpetologica48265270Google Scholar
  72. West, S.A., Reece, S.E., Sheldon, B.C. 2002Sex ratiosHeredity88117124PubMedCrossRefGoogle Scholar
  73. Werren, J.H., Charnov, E.L. 1978Facultative sex ratios and population dynamicsNature272349350PubMedCrossRefGoogle Scholar
  74. Williams, G.C. 1979The question of adaptive sex ratio in outcrossed vertebratesProc. Roy. Soc. Lond. B205567580CrossRefGoogle Scholar

Copyright information

© Springer 2006

Authors and Affiliations

  • J. Sean Doody
    • 1
  • Enzo Guarino
    • 1
  • Arthur Georges
    • 1
  • Ben Corey
    • 1
  • Glen Murray
    • 1
  • Michael Ewert
    • 2
  1. 1.Institute for Applied EcologyUniversity of CanberraCanberraAustralia
  2. 2.Department of BiologyBloomingtonUSA

Personalised recommendations