Skip to main content
SpringerLink
Log in

Fitness effects of the timing of hatching may drive the evolution of temperature-dependent sex determination in short-lived lizards

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

In several species of short-lived Australian agamid lizards, an individual’s sex is determined by the nest temperatures encountered during incubation. The adaptive significance of such systems remains unclear. Here, we explore the hypothesis that (1) the optimal timing of hatching differs between the sexes, and thus (2) temperature-dependent sex determination (TSD) enhances maternal and offspring fitness by generating seasonal shifts in offspring sex ratios. Our model predicts that TSD can indeed enhance maternal fitness returns in short-lived lizards if (1) male–male competition is intense, thus reducing mating success of newly-matured males (but not females), and (2) the nesting season is prolonged, such that seasonal effects become significant. Available data on the distribution of TSD in Australian agamid lizards broadly support these predictions. Because both the level of male–male competition and the length of nesting season can vary at small spatial and temporal scales, selective forces on sex-determining mechanisms also should vary. Hence, our model predicts extensive small-scale (intraspecific) variation in sex-determining systems within agamid lizards, as well as among species.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Andrews RM (2005) Incubation temperature and sex ratio of the veiled chameleon (Chamaeleo calyptratus). J Herpetol 39:515–518

    Article  Google Scholar 

  • Aragón P, López P, Martín J (2006) Roles of male residence and relative size in the social behavior of Iberian rock lizards, Lacerta monticola. Behav Ecol Sociobiol 59:762–769

    Article  Google Scholar 

  • Baroiller JF, Chourrout D, Fostier A, Jalabert B (1995) Temperature and sex chromosomes govern sex ratios of the mouthbrooding cichlid fish Oreochromis niloticus. J Exp Zool 273:216–223

    Article  Google Scholar 

  • Brattstrom BH (1971) Social and thermoregulatory behaviour of the bearded dragon, Amphibolurus barbatus. Copiea 1971:484–497

    Article  Google Scholar 

  • Bull JJ, Vogt RC (1979) Temperature-dependent sex determination in turtles. Science 206:1186–1188

    Article  PubMed  CAS  Google Scholar 

  • Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin/Cummings, Menlo Park, California, USA

    Google Scholar 

  • Bull JJ, Charnov EL (1989) Enigmatic reptilian sex ratios. Evolution 43:1561–1566

    Article  Google Scholar 

  • Carpenter CC, Badham JA, Kimble B (1970) Behavior patterns of three species of Amphibolurus (Agamidae). Copeia 1970:497–505

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cogger HG (1969) A study of the ecology and biology of the mallee dragon (Amphibolurus fordi) and its adaptation to survival in an arid environment. Dissertation, Macquarie University

  • Cogger HG (1978) Reproductive cycles, fat body cycles and socio-sexual behaviour in the mallee dragon, Amphibolurus fordi (Lacertilia: Agamidae). Aust J Zool 26:653–672

    Article  Google Scholar 

  • Cogger HG (2000) Reptiles and amphibians of Australia. Ralph Curtis Publishing, Florida, USA

    Google Scholar 

  • Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Am Nat 123:297–313

    Article  Google Scholar 

  • Conover DO, Heins SW (1987) Adaptive variation in environmental and genetic sex determination in a fish. Nature 326:496–498

    Article  PubMed  CAS  Google Scholar 

  • Cooper WE Jr (2003) Sexual dimorphism in distance from cover but not escape behavior by the keeled earless lizard Holbrookia propinqua. J Herpetol 37:374–378

    Article  Google Scholar 

  • Cree AM, Thompson MB, Daugherty CH (1995) Tuatara sex determination. Nature 375:543

    Google Scholar 

  • Daan S, Dijkstra C, Weissing FJ (1996) An evolutionary explanation for seasonal trends in avian sex ratios. Behav Ecol 7:426–430

    Article  Google Scholar 

  • Doody JS, Georges A, Young JE (2004) Determinants of reproductive success and offspring sex in a turtle with environmental sex determination. Biol J Linn Soc 81:1–16

    Article  Google Scholar 

  • Doody SJ, Guarino E, Georges A, Corey B, Murray G, Ewert M (2006) Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination. Evol Ecol 20:307–330

    Article  Google Scholar 

  • El Mouden EH, Znari M, Pieau C (2001) Effects of incubation temperature on embryonic development and sex determination in the northern African agamid lizard, Agama impalearis. Herpetol J 11:101–108

    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 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford, UK

    Google Scholar 

  • Ferguson MWJ, Joanen T (1982) Temperature of egg incubation determines sex in Alligator mississippiensis. Nature 296:850–853

    Article  PubMed  CAS  Google Scholar 

  • Franco MG, Rubini PG Vecchi M (1982) Sex-determinants and their distribution in various populations of Musca domestica L. of western Europe. Genet Res 40:279–293

    Article  PubMed  CAS  Google Scholar 

  • Greer AE (1989) The biology and evolution of Australian lizards. Surrey Beatty and Sons, Chipping Norton, Australia

    Google Scholar 

  • Griffiths AD (1999) Demography and home range of the frillneck lizard, Chlamydosaurus kingii (Agamidae), in northern Australia. Copeia 1999:1089–1096

    Article  Google Scholar 

  • Harlow PS (2000) Incubation temperature determines hatchling sex in Australian rock dragons (Agamidae: genus Ctenophorus). Copeia 2000:958–964

    Article  Google Scholar 

  • Harlow PS (2001) The ecology of sex-determining mechanisms in Australian agamid lizards. Dissertation, Macquarie University

  • Harlow PS (2004) Temperature-dependent sex determination in lizards. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Institution Press, Washington DC, pp 42–52

    Google Scholar 

  • Harlow PS, Harlow MF (1997) Captive reproduction and longevity in the eastern water dragon (Physignathus lesueurii). Herpetofauna 27:14–19

    Google Scholar 

  • Harlow PS, Shine R (1999) Temperature-dependent sex determination in the frillneck lizard, Chlamydosaurus kingii (Agamidae). Herpetologica 55:205–212

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Janzen FJ, Paukstis GL (1991b) A preliminary test of the adaptive significance of temperature-dependent sex determination in reptiles. Evolution 45:435–440

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Jenssen TA, Decourcy KR, Congdon JD (2005) Assessment in contests of male lizards (Anolis carolinensis): how should smaller males respond when size matters? Anim Behav 69:1325–1336

    Article  Google Scholar 

  • Jun-Yi JW, Kau-Hung L (1982) Population ecology of the lizard Japalurua swinhonis formosensis (Sauria: Agamidae) in Taiwan. Copeia 1982:425–434

    Article  Google Scholar 

  • Kozielska M, Pen I, Beukeboom LW, Weissing FJ (2006) Sex ratio selection and multi-factorial sex determination in the house fly: a dynamic model. J Evol Biol 19:879–888

    Article  PubMed  CAS  Google Scholar 

  • Lagomarsino IV, Conover DO (1993) Variation in environmental and genotypic sex-determining mechanisms across a latitudinal gradient in the fish, Menidia menidia. Evolution 47:487–494

    Article  Google Scholar 

  • LeBas NR (2002) Mate choice, genetic incompatibility, and outbreeding in the ornate dragon lizard, Ctenophorus ornatus. Evolution 56:371–377

    PubMed  Google Scholar 

  • Lister BC, Aguayo AG (1992) Seasonality, predation, and the behaviour of a tropical mainland anole. J Anim Ecol 61:717–733

    Article  Google Scholar 

  • Manning A, Ehmann H (1991) A study of the activity and behaviour of the southern angle-headed dragon using the spool tracking technique. Herpetofauna 21:5–16

    Google Scholar 

  • Olsson M (1992) Contest success in relation to body size and residency in male sand lizards, Lacerta agilis. Anim Behav 44:386–388

    Article  Google Scholar 

  • Olsson M, Shine R (1997) The seasonal timing of oviposition in sand lizards (Lacerta agilis): why early clutches are better. J Evol Biol 10:369–381

    Article  Google Scholar 

  • Olsson M, Madsen T (1998) Sexual selection and sperm competition in reptiles. In: Birkhead TR, Møller AP (eds) Sperm competition and sexual selection. Academic Press, San Diego, California, USA, pp 503–577

    Chapter  Google Scholar 

  • Osborne L (2005) Rival recognition in the territorial tawny dragon (Ctenophorus decresii). Acta Ethol 8:45–50

    Article  Google Scholar 

  • Pen I, Weissing FJ, Daan S (1999) Seasonal sex ratio trend in the European kestrel: an evolutionarily stable strategy analysis. Am Nat 153:384–397

    Article  Google Scholar 

  • Peters RA, Ord TJ (2003) Display response of the jacky dragon, Amphibolurus muricatus (Lacertilia: Agamidae), to intruders: a semi-markovian Process. Aust Ecol 28:449–506

    Article  Google Scholar 

  • Qualls FJ, Shine R (1998) Geographic variation in lizard phenotypes: the importance of incubation temperatures. Biol J Linn Soc 64:477–491

    Article  Google Scholar 

  • Qualls FJ, Shine R (2000) Post-hatching environment contributes greatly to phenotypic variation between two populations of the Australian garden skink, Lampropholis guichenoti. Biol J Linn Soc 71:315–341

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Shine R, Elphick MJ, Harlow PS (1995) Sisters like it hot. Nature 378:451–452

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Smallwood PD, Smallwood JA (1998) Seasonal shifts in sex ratios of fledgling American kestrels (Falco sparverius paulus): the early bird hypothesis. Evol Ecol 12:839–853

    Article  Google Scholar 

  • Stuart-Smith JN, Swain R, Welling A (2005) Reproductive ecology of the mountain dragon, Rankinia (Tympanocryptus) diemensis (Reptilia: Squamata: Agamidae) in Tasmania. Pap Proc R Soc Tas 139:23–28

    Google Scholar 

  • Thompson GG, Thompson SA (2001) Behaviour and spatial ecology of Gilbert’s dragon Lophognathus gilberti (Agamidae: Reptilia). J R Soc West Aust 84:153–158

    Google Scholar 

  • Tinkle DW (1967) The life history and demography of the side-blotched lizard, Uta stansburiana. Misc Publ Mus Zool Univ Michigan 132:1–182

    Google Scholar 

  • Uller T, Olsson M (2006) No seasonal sex ratio shift despite sex-specific fitness returns of hatching date in a lizard with genotypic sex determination. Evolution 60:2131–2136

    PubMed  Google Scholar 

  • Uller T, Mott B, Odierna G, Olsson M (2006) Consistent sex ratio bias of individual female dragon lizards. Biol Lett 2:569–572

    Article  PubMed  Google Scholar 

  • Uller T, Pen I, Wapstra E, Beukeboom L, Komdeur J (2007) Evolution of sex ratios and sex-determining systems. Trends Ecol Evol 22:292–297

    Article  PubMed  Google Scholar 

  • Valenzuela N (2004) Evolution and maintenance of temperature-dependent sex determination. In: Valenzuela N, Lance VA (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Institution Press, Washington DC, pp 131–147

    Google Scholar 

  • Valenzuela N, Lance VA (2004) Temperature-dependent sex determination in vertebrates. Smithsonian Institution Press, Washington DC

    Google Scholar 

  • Viets BE, Ewert MA, Talent LG, Nelson CE (1994) Sex-determining mechanisms in squamate reptiles. J Exp Zool 270:45–56

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    PubMed  Google Scholar 

  • Warner DA, Shine R (2007a) Maternal nest-site choice in a lizard with temperature-dependent sex determination. Anim Behav (in press)

  • Warner DA, Shine R (2007b) Fitness of juvenile lizards depends on seasonal timing of hatching, not offspring body size. Oecologia 154:65–73

    Article  PubMed  Google Scholar 

  • Werren JH, Charnov EL (1978) Facultative sex ratios and population dynamics. Nature 272:349–350

    Article  PubMed  CAS  Google Scholar 

  • Witten GJ (1974) Population movements of the agamid lizard Amphibolurus nobbi. Aust Zool 18:129–132

    Google Scholar 

  • Witten GJ, Heatwole H (1978) Preferred temperature of the agamid lizard Amphibolurus nobbi nobbi. Copeia 1978:362–364

    Article  Google Scholar 

  • Wright DD, Ryser JT, Kiltie RA (1995) First-cohort advantage hypothesis: a new twist on facultative sex ratio adjustment. Am Nat 145:133–145

    Article  Google Scholar 

Download references

Acknowledgements

Comments by M. Olsson, S. Parker, I. Pen, R. Radder, F. Seebacher, M. Thompson, and E. Wapstra improved this manuscript. DAW was supported by an International Postgraduate Research Scholarship and an International Postgraduate Award, TU by the Wenner-Gren Foundations and the Australian Research Council, and RS by the Australian Research Council.

Author information

Author notes

  1. Daniel A. Warner

    Present address: Department of Ecology, Evolution and Organismal Biology, Iowa State University, Ames, IA, 50011, USA

  2. Tobias Uller

    Present address: Edward Grey Institute, School of Zoology, University of Oxford, Oxford, OX1 3PS, UK

Authors and Affiliations

  1. School of Biological Sciences, University of Sydney, Heydon Laurence Building A08, Sydney, NSW, 2006, Australia

    Daniel A. Warner & Richard Shine

  2. School of Biological Sciences, University of Wollongong, Wollongong, NSW, 2522, Australia

    Tobias Uller

Authors
  1. Daniel A. Warner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tobias Uller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard Shine
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel A. Warner.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Warner, D.A., Uller, T. & Shine, R. Fitness effects of the timing of hatching may drive the evolution of temperature-dependent sex determination in short-lived lizards. Evol Ecol 23, 281–294 (2009). https://doi.org/10.1007/s10682-007-9222-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-007-9222-4

Keywords

Search

Navigation