Skip to main content

Advertisement

SpringerLink
Log in

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

  • Research article
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • S.C. Adolph W.P. Porter (1993) ArticleTitleTemperature, activity, and lizard life histories Am. Nat. 142 273–295 Occurrence Handle10.1086/285538 Occurrence Handle19425979 Occurrence Handle1:STN:280:DC%2BD1Mzjt1Gmtw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • W.K. Bragg J.D. Fawcett T.B Bragg B.E. Viets (2000) ArticleTitleNest-site selection in two eublepharid gecko species with temperature-dependent sex determination and one with genotypic sex determination Biol. J. Linn. Soc. 69 319–332 Occurrence Handle10.1006/bijl.1999.0359

    Article  Google Scholar 

  • J.H. Brown (1995) Macroecology University of Chicago Press Chicago

    Google Scholar 

  • J.J. Bull (1980) ArticleTitleSex determination in reptiles Quart. Rev. Biol. 55 3–21 Occurrence Handle10.1086/411613

    Article  Google Scholar 

  • J.J. Bull (1983) Evolution of Sex Determining Mechanisms Benjamin Cummings California

    Google Scholar 

  • J.J. Bull (1987) ArticleTitleTemperature-sensitive periods of sex determination in a lizard: comparisons with crocodiles and turtles J. Exp. Zool. 241 143–148 Occurrence Handle10.1002/jez.1402410118

    Article  Google Scholar 

  • J.J. Bull R.C. Vogt M.G. Bulmer (1982a) ArticleTitleHeritability of sex ratio in turtles with environmental sex determination Evolution 36 333–341 Occurrence Handle10.2307/2408052

    Article  Google Scholar 

  • J.J. Bull R.C. Vogt C.J. McCoy (1982b) ArticleTitleSex determining temperatures in turtles: A geographic comparison Evolution 36 326–332 Occurrence Handle10.2307/2408051

    Article  Google Scholar 

  • J.J. Bull W.H.N. Gutzke M.G. Bulmer (1988) ArticleTitleNest choice in a captive lizard with temperature-dependent sex determination J. Evol. Biol. 1 177–184 Occurrence Handle10.1046/j.1420-9101.1988.1020177.x

    Article  Google Scholar 

  • M.G. Bulmer J.J. Bull (1982) ArticleTitleModels of polygenic sex determination and sex ratio control Evolution 36 13–26 Occurrence Handle10.2307/2407962

    Article  Google Scholar 

  • A.B. Carvalho M.C. Sampaio F.R. Varandas L.B. Klaczko (1998) ArticleTitleAn experimental demonstration of Fisher’s principle: Evolution of sexual proportion by natural selection Genetics 148 719–731 Occurrence Handle9504919 Occurrence Handle1:STN:280:DyaK1c7os1alsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • E.L. Charnov (1982) The Theory of Sex Allocation Princeton University Press New Jersey

    Google Scholar 

  • H. Cogger (2000) Reptiles and Amphibians of Australia New Holland Reed Sydney

    Google Scholar 

  • D.O. Conover (2004) Temperature-dependent sex determination in fishes N. Valenzuela V. Lance (Eds) Temperature-Dependent Sex Determination in Vertebrates Smithsonian Institute Press Washington, DC 11–32

    Google Scholar 

  • D.O. Conover D.A. Voorhees ParticleVan (1990) ArticleTitleEvolution of a balanced sex ratio by frequency-dependent selection in a fish Science 250 1556–1158 Occurrence Handle17818284

    PubMed  Google Scholar 

  • C. Darwin (1871) The Descent of Man and Selection in Relation to Sex John Murray London

    Google Scholar 

  • J. Davenport (1997) ArticleTitleTemperature and the life history strategies of sea turtles J. Therm. Biol. 22 479–488 Occurrence Handle10.1016/S0306-4565(97)00066-1

    Article  Google Scholar 

  • J.P. Defaure J. Hubert (1961) ArticleTitleTable dé developpement du lézard vivipare: Lacerta (Zootoca) vivipara Jacquin Archives d’Anatomie Microscopique et de Morphologie Experimentale 50 309–328

    Google Scholar 

  • J.S. Doody A. Georges J.E. Young (2004) ArticleTitleDeterminants of reproductive success and offspring sex in a turtle with environmental sex determination Biol. J. Linn. Soc. 81 1–16 Occurrence Handle10.1111/j.1095-8312.2004.00250.x

    Article  Google Scholar 

  • A.E. Dunham B.W. Grant K.L. Overall (1989) ArticleTitleInterfaces between biophysical and physiological ecology and the population ecology of terrestrial vertebrate ectotherms Physiol. Zool. 62 335–355

    Google Scholar 

  • L.R. Ellner W.H. Karasov (1993) ArticleTitleLatitudinal variation in the thermal biology of ornate box turtles Copeia 1993 447–455 Occurrence Handle10.2307/1447144

    Article  Google Scholar 

  • M.A. Ewert D.R. Jackson C.E. Nelson (1994) ArticleTitlePatterns of temperature-dependant sex determination in turtles J. Exp. Zool. 270 3–15 Occurrence Handle10.1002/jez.1402700103

    Article  Google Scholar 

  • M.A. Ewert C.R. Etchberger C.E. Nelson (2004) Turtle sex-determining modes and TSD patterns, and some TSD pattern correlates N. Valenzuela V. Lance (Eds) Temperature-dependent Sex Determination in Vertebrates Smithsonian Institution Press Washington, DC 21–32

    Google Scholar 

  • M.A Ewert J.W. Lang C.E. Nelson (2005) ArticleTitleGeographic variation in the pattern of temperature-dependant sex determination in the American snapping turtle (Chelydra serpenina) J. Zool. 265 81–95 Occurrence Handle10.1017/S0952836904006120

    Article  Google Scholar 

  • R.A. Fisher (1930) The Genetical Theory of Natural Selection Oxford University Press Oxford

    Google Scholar 

  • C.K. Folland T.R. Karl J.R. Christy R.A. Clarke G.V. Gruza J. Jouzel M.E. Mann J. Oerlemans M.J. Salinger S.W. Wang (2001) Observed Climate Variability and Change J.T. Houghton Y. Ding D.J. Griggs M. Noguer Linden Particlevan der X. Dai K. Maskell C.A. Johnson (Eds) Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the intergovernmental Panel on Climate Change Cambridge University Press Cambridge, United Kingdom 49–94

    Google Scholar 

  • M.C. Forchhammer E. Post N.C. Stenseth (1998) ArticleTitleBreeding phenology and climate Nature 391 29–30 Occurrence Handle1:CAS:528:DyaK1cXktFShuw%3D%3D Occurrence Handle10.1038/34070

    Article  CAS  Google Scholar 

  • G.W. Frazer C.D. Canham K.P. Lertzman (1999) Gap Light Analyser (GLA): Imaging Software to Extract Canopy Structure and Gap Light Transmission Indices from True-colour Fisheye Photographs, Users Manual and Program Documentation Simon Fraser University, British Columbia; and the Institute of Ecosystem Studies New York

    Google Scholar 

  • S. Freedberg M.J. Wade (2004) ArticleTitleMale combat favours female-biased sex ratios under environmental sex determination Anim. Behav. 67 177–181 Occurrence Handle10.1016/j.anbehav.2003.01.004

    Article  Google Scholar 

  • A. Georges (1989) ArticleTitleFemale turtles from hot nests: Is it duration of incubation or proportion of development that matters? Oecologia 81 323–328

    Google Scholar 

  • A. Georges (1992) ArticleTitleThermal characteristics and sex determination in field nests of the pig-nosed turtle, Carettochelys insculpta (Chelonia: Carettochelydidae), from northern Australia Aust. J. Zool. 40 511–521 Occurrence Handle10.1071/ZO9920511

    Article  Google Scholar 

  • A. Georges C. Limpus R. Stoutjesdijk (1994) ArticleTitleHatchling sex in the marine turtle Caretta caretta is determined by proportion of development at a temperature, not daily duration of exposure J. Exp. Zool. 270 432–444 Occurrence Handle10.1002/jez.1402700504

    Article  Google Scholar 

  • A. Georges J.S. Doody K. Beggs J.E. Young (2004) Thermal models of TSD under laboratory and field conditions N. Valenzuela V. Lance (Eds) Temperature-Dependent Sex Determination in Vertebrates Smithsonian Institution Press Washington, DC 79–89

    Google Scholar 

  • F. Giorgi B. Hewitson J. Christensen M. Hulme H. Storch ParticleVan P. Whetton R. Jones L. Mearns C. Fu (2001) Regional Climate Information – Evaluation and Projections J.T. Houghton Y. Ding D.J. Griggs M. Noguer P.J. van der Particle Linden X. Dai K. Maskell C.A. Johnson (Eds) Climate Change 2001: The Scientific Basis. Contribution of Working Group I to the Third Assessment Report of the Intergovernmental Panel on Climate Change Cambridge University Press Cambridge, United Kingdom 374–407

    Google Scholar 

  • F.B. Giorgi R. Fransisco (2000) ArticleTitleUncertainties in regional climate change prediction: a regional analysis of ensemble simulations with the HADCM2 coupled AOGCM’ Clim. Dyn. 16 169–182 Occurrence Handle10.1007/PL00013733

    Article  Google Scholar 

  • M. Girondot V. Delmas P. Rivalan F. Courchamp A. Prevot-Julliard M.H. Godfrey (2004) Implications of temperature-dependent sex determination for population dynamics N. Valenzuela V. Lance (Eds) Temperature-Dependent Sex Determination in Vertebrates Smithsonian Institute Press Washington, DC 148–155

    Google Scholar 

  • L. Gvozdik (2002) ArticleTitleTo heat or to save time? Thermoregulation in the lizard Zootoca vivipara (Squamata: Lacertidae) in different thermal environments along an altitudinal gradient Can. J. Zool. 80 479–492 Occurrence Handle10.1139/z02-015

    Article  Google Scholar 

  • P.S. Harlow (1996) ArticleTitleA harmless technique for sexing hatchling lizards Herpetol. Rev. 27 71–72

    Google Scholar 

  • Harlow P.S. (2001) The ecology of sex-determining mechanisms in Australian agamid lizards. Unpubl. PhD Thesis, Macquarie University, Sydney, Australia

  • P.S. Harlow M.F. Harlow (1997) ArticleTitleCaptive reproduction and longevity in the eastern water dragon (Physignathus lesueurii) Herpetofauna 27 14–19

    Google Scholar 

  • M. Hay (1972) ArticleTitleThe breeding of Physignathus lesueurii in captivity Herpetofauna 5 2–3

    Google Scholar 

  • P.E. Hertz (1992) ArticleTitleTemperature regulation in Puerto Rican Anolis lizards: a field test using null hypothesis Ecology 73 1405–1417 Occurrence Handle10.2307/1940686

    Article  Google Scholar 

  • P.E. Hertz R.B. Huey (1981) ArticleTitleCompensation for altitudinal changes in the thermal environment by some Anolis lizards on Hispaniola Ecology 62 515–521 Occurrence Handle10.2307/1937714

    Article  Google Scholar 

  • R.B. Huey A.F. Bennett (1990) ArticleTitlePhysiological adjustments to fluctuating thermal environments: an ecological and evolutionary perspective Cold Spring Harbor Monogr. Ser. 19 37–59

    Google Scholar 

  • F.J. Janzen (1992) ArticleTitleHeritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelydra serpentina) Genetics 131 155–161 Occurrence Handle1592234 Occurrence Handle1:STN:280:DyaK383nsFeitg%3D%3D

    PubMed  CAS  Google Scholar 

  • F.J. Janzen (1994a) ArticleTitleVegetational cover predicts the sex ratio of hatchling turtles in natural nests Ecology 75 1593–1599 Occurrence Handle10.2307/1939620

    Article  Google Scholar 

  • F.J. Janzen (1994b) ArticleTitleClimate change and temperature-dependent sex determination in reptiles Proc. Nat. Acad. Sci., USA 91 7487–7490 Occurrence Handle1:STN:280:DyaK2czivFGnsg%3D%3D Occurrence Handle10.1073/pnas.91.16.7487

    Article  CAS  Google Scholar 

  • F.J. Janzen C.L. Morjan (2001) ArticleTitleRepeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determination Anim. Behav. 62 73–82 Occurrence Handle10.1006/anbe.2000.1732

    Article  Google Scholar 

  • F.J. Janzen G.L. Paukstis (1991) ArticleTitleEnvironmental sex determination in reptiles: ecology, evolution, and experimental design Quart. Rev. Biol. 66 149–179 Occurrence Handle1891591 Occurrence Handle1:STN:280:DyaK3MzmvVSisg%3D%3D Occurrence Handle10.1086/417143

    Article  PubMed  CAS  Google Scholar 

  • J.P. McCarty (2001) ArticleTitleEcological consequences of recent climate change Conser. Biol. 15 320–331 Occurrence Handle10.1046/j.1523-1739.2001.015002320.x

    Article  Google Scholar 

  • C.L. Morjan (2003) ArticleTitleVariation in nesting patterns affecting nest temperatures in two populations of painted turtles (Chrysemys picta) with temperature-dependent sex determination Behav. Ecol. Sociobiol. 53 254–261 Occurrence Handle10.1007/s00265-002-0570-3

    Article  Google Scholar 

  • N. Mrosovsky S. Kamel A.F. Rees D. Margaritoulis (2002) ArticleTitlePivotal temperature for loggerhead turtles (Caretta caretta) from Kyparissia Bay, Greece Can. J. Zool. 80 2118–2124 Occurrence Handle10.1139/z02-204

    Article  Google Scholar 

  • S. Ohno (1967) Sex Chromosomes and Sex-linked Genes Springer-Verlag Berlin

    Google Scholar 

  • C. Parmesan G. Yohe (2004) ArticleTitleA globally coherent fingerprint of climate change impacts across natural systems Nature 421 37–42 Occurrence Handle10.1038/nature01286 Occurrence Handle1:CAS:528:DC%2BD3sXoslM%3D

    Article  CAS  Google Scholar 

  • R.M. Pringle J.K Webb R. Shine (2003) ArticleTitleCanopy structure, microclimate, and habitat selection by a nocturnal snake, Hoplocephalus bungaroides Ecology 84 2668–2679

    Google Scholar 

  • T. Rhen J.W. Lang (1998) ArticleTitleAmong-family variation for environmental sex determination in reptiles Evolution 52 1514–1520 Occurrence Handle10.2307/2411322

    Article  Google Scholar 

  • D.A. Roff (1996) ArticleTitleThe evolution of threshold traits in animals Quart. Rev. Biol. 71 3–35 Occurrence Handle10.1086/419266

    Article  Google Scholar 

  • W.M. Roosenburg (1996) ArticleTitleMaternal condition and nest site choice: An alternative for the maintenance of environmental sex determination Am. Zool. 36 157–168

    Google Scholar 

  • T.L. Root J.T. Price K.L. Hall (2003) ArticleTitleFingerprints of global warming on wild animals and plants Nature 421 57–60 Occurrence Handle12511952 Occurrence Handle1:CAS:528:DC%2BD3sXovVc%3D Occurrence Handle10.1038/nature01333

    Article  PubMed  CAS  Google Scholar 

  • InstitutionalAuthorNameSAS Institute (1998) SAS 8.00 SAS Institute Inc Cary, NC

    Google Scholar 

  • R.F. Shaw J.D. Mohler (1953) ArticleTitleThe selective significance of the sex ratio Am. Nat. 87 337–342 Occurrence Handle10.1086/281794

    Article  Google Scholar 

  • R. Shine (1999) ArticleTitleWhy is sex determined by nest temperature in many reptiles? TREE 14 186–189 Occurrence Handle10322531

    PubMed  Google Scholar 

  • R. Shine (2002) ArticleTitleReconstructing an adaptionist scenario: what selective forces favour the evolution of viviparity in montane reptiles? Am. Nat. 160 82–593 Occurrence Handle10.1086/342815

    Article  Google Scholar 

  • R. Shine P.S. Harlow (1996) ArticleTitleMaternal manipulation of offspring phenotypes via nest-site selection in an oviparous lizard Ecology 77 1808–1817 Occurrence Handle10.2307/2265785

    Article  Google Scholar 

  • R. Shine M.J. Elphick E.G. Barrott (2003) ArticleTitleSunny side up: lethally high, not low, nest temperatures may prevent oviparous reptiles from reproducing at high elevations Biol. J. Linn. Soc. 78 325–334 Occurrence Handle10.1046/j.1095-8312.2003.00140.x

    Article  Google Scholar 

  • R. Shine M.J. Elphick P.S. Harlow (1997) ArticleTitleThe influence of natural incubation environments on the phenotypic traits of hatchling lizards Ecology 78 2559–2568 Occurrence Handle10.2307/2265914

    Article  Google Scholar 

  • J.R. St Juliana R.M. Bowden F.J. Janzen (2004) ArticleTitleThe impact of behavioral and physiological maternal effects on offspring sex ratio in the common snapping turtle, Chelydra serpentina Behav. Ecol. Sociobiol. 53 270–278

    Google Scholar 

  • InstitutionalAuthorNameSystat (1998) SYSTAT 8.0 SPSS Science Chicago, Illinois

    Google Scholar 

  • B.E Sæther J. Tufto S. Engen K. Jerstad O.W. Rostad K.E. Skatan (2000) ArticleTitlePopulation dynamical consequences of climate change for a small temperate songbird Science 287 854–856 Occurrence Handle10657299 Occurrence Handle10.1126/science.287.5454.854

    Article  PubMed  Google Scholar 

  • N. Valenzuela (2004) Evolution and maintenance of temperature-dependent sex determination N. Valenzuela v. Lance (Eds) Temperature-Dependent Sex Determination in Vertebrates Smithsonian Institution Press Washington, DC 131–147

    Google Scholar 

  • R.C. Vogt O. Flores-Villela (1992) ArticleTitleEffects of incubation temperature on sex determination in a community of neotropical freshwater turtles in southern Mexico Herpetologica 48 265–270

    Google Scholar 

  • S.A. West S.E. Reece B.C. Sheldon (2002) ArticleTitleSex ratios Heredity 88 117–124 Occurrence Handle11932770 Occurrence Handle1:STN:280:DC%2BD387pslOisQ%3D%3D Occurrence Handle10.1038/sj.hdy.6800018

    Article  PubMed  CAS  Google Scholar 

  • J.H. Werren E.L. Charnov (1978) ArticleTitleFacultative sex ratios and population dynamics Nature 272 349–350 Occurrence Handle634359 Occurrence Handle1:STN:280:DyaE1c7jsFCntw%3D%3D Occurrence Handle10.1038/272349a0

    Article  PubMed  CAS  Google Scholar 

  • G.C. Williams (1979) ArticleTitleThe question of adaptive sex ratio in outcrossed vertebrates Proc. Roy. Soc. Lond. B 205 567–580 Occurrence Handle1:STN:280:DyaL3c%2FnvFyrsg%3D%3D Occurrence Handle10.1098/rspb.1979.0085

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute for Applied Ecology, University of Canberra, 2601, Canberra, ACT, Australia

    J. Sean Doody, Enzo Guarino, Arthur Georges, Ben Corey & Glen Murray

  2. Department of Biology, 1001 East Third Street, Bloomington, IN, 47405-3700, USA

    Michael Ewert

Authors
  1. J. Sean Doody
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Enzo Guarino
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arthur Georges
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ben Corey
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Glen Murray
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Michael Ewert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to J. Sean Doody.

Additional information

Michael Ewert: Deceased

Co-ordinating editor: K. Lindtsröm

Rights and permissions

Reprints and permissions

About this article

Cite this article

Doody, J.S., Guarino, E., Georges, A. et al. Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evol Ecol 20, 307–330 (2006). https://doi.org/10.1007/s10682-006-0003-2

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-006-0003-2

Keywords

Search

Navigation