Abstract
Although the adaptive significance of temperature-dependent sex determination (TSD) remains a puzzle, recent models implicate a seasonal bias in offspring sex production that translates into sex-specific fitness benefits later in life. Sex-specific emergence has been linked to fitness gains in some fish, birds and reptiles, but field data supporting the occurrence of a seasonal pattern of sex ratios in oviparous lizards are lacking. We tested the hypothesis that patterns of nest site selection and seasonal temperature changes combine to inhibit the materialization of sex-biased hatching times in a population of water dragons (Intellagama lesueurii). As predicted, a seasonal increase in air and nest temperatures resulted in a sex bias by nesting date; male-producing clutches were laid 17.8 days sooner than female-producing clutches, on average. However, the seasonal ramping of nest temperatures also caused shorter relative incubation periods in the later, all-female clutches. As a consequence of this developmental ‘catch-up’, the mean hatching date for male-producing nests preceded the mean hatching date for female-producing nests by only 7.2 days. We suggest that a contracted distribution of hatching dates compared to the distribution of oviposition dates represents a general pattern for oviparous reptiles in seasonal climates, which in TSD species may largely offset the temporal disparity in nesting dates between the sexes. Although data are needed for other TSD species, such minor age differences between male and female hatchlings may not translate into fitness differences later in life, an assumption of some models for the evolution and maintenance of TSD.
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References
Andersson M, Wallander J, Oring L, Akst E, Reed JM, Fleischer RC (2003) Adaptive seasonal trend in brood sex ratio: test in two sister species with contrasting breeding systems. J Evol Biol 16(3):510–515
Badyaev AV, Schwabl H, Young RL, Duckworth RA, Navara KJ, Parlow AF (2005) Adaptive sex differences in growth of pre-ovulation oocytes in a passerine bird. Proc R Soc B Biol Sci 272(1577):2165–2172
Badyaev AV, Acevedo ED, Navara KJ, Hill GE, Mendonca MT (2006a) Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins. J Evol Biol 19(4):1044–1057
Badyaev AV, Oh KP, Mui R (2006b) Evolution of sex-biased maternal effects in birds: II. Contrasting sex-specific oocyte clustering in native and recently established populations. J Evol Biol 19(3):909–921
Badyaev AV, Young RL, Hill GE, Duckworth RA (2008) Evolution of sex-biased maternal effects in birds. IV. Intra-ovarian growth dynamics can link sex determination and sex-specific acquisition of resources. J Evol Biol 21(2):449–460
Bull JJ (1980) Sex determination in reptiles. Q Rev Biol 55:3–21
Bull JJ (1981) Sex ratio evolution when fitness varies. Heredity 46:9–26
Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton New Jersey
Charnov E, Bull J (1977) When is sex environmentally determined? Nature 266:828–830
Cogger HG (2000) Reptiles and amphibians of Australia, 6th edn. Reed New Holand, Sydney
Conover DO (1984) Adaptive significance of temperature-dependent sex determination in a fish. Am Nat 123:297–313
Conover DO, Heins SW (1987) The environmental and genetic components of sex ratio in Menidia menidia (Pisces: Atherinidae). Copeia 1987(3):732–743
Daan S, Dijkstra C, Weissing F (1996) An evolutionary explanation for seasonal trends in avian sex ratios. Behav Ecol 7:426–430
Daly G (1992) Aggressive territorial behaviour in free range water dragons (Physignathus lesueurii lesueurii). Herpetofauna 21(22):37
de Souza RR, Vogt RC (1994) Incubation temperature influences sex and hatchling size in the neotropical turtle Podocnemis unifilis. J Herpetol 28(4):453
Deeming DC (2004) Reptilian incubation: environment, evolution and behaviour. Nottingham University Press, Nottingham
Doody, J. S. (1995). A comparative nesting study of two syntopic species of softshell turtles (Apalone mutica and Apalone spinifera) in Southeastern Louisiana (unpublished Masters thesis) Southern Luisiana University
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
Doody J, 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(4):307–330
Dufaure JP, Hubert J (1961) Table De Developpement Du Lezard Vivipare-Lacerta (Zootoca) Vivipara Jacquin. Arch Anat Microsc Morphol Exp 50:309–328
Ewert MA, Jackson DR, Nelson CE (1994) Patterns of temperature-dependent sex determination in turtles. J Exp Zool 270:3–15
Frank SA (1990) Sex allocation theory for birds and mammals. Annu Rev Ecol Syst 21(1):13–55
Frazer GW, Canham CD, Lertzman KP (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
Georges A (1989) Female turtles from hot nests: is it duration of incubation or proportion of development at high temperatures that matters? Oecologia 81(3):323–328
Georges A, Beggs K, Young JE, Doody JS (2005) Modelling development of reptile embryos under fluctuating temperature regimes. Physiol Biochem Zool 78(1):18–30
Harlow P (1996) A harmless technique for sexing hatchling lizards. Herpetol Rev 27:71–72
Harlow PS (2001) The ecology of sex-determining mechanisms in Australian agamid lizards (unpublished Ph.d. thesis) Maquarie University
Harlow P (2004) Temperature-dependent sex determination in lizards. In: Valenzuela N, Lance V (eds) Temperature-dependent sex determination in vertebrates. Smithsonian Books, Washington, p 42
Harlow P, Harlow M (1997) Captive reproduction and longevity in the eastern water dragon (Physignathus Lesueurii). Herpetofauna 27:14–19
Harlow PS, Taylor JE (2000) Reproductive ecology of the jacky dragon (Amphibolurus muricatus): an agamid lizard with temperature-dependent sex determination. Austral Ecol 25:640–652
Komdeur J, Pen I (2002) Adaptive sex allocation in birds: the complexities of linking theory and practice. Philos Trans R Soc B Biol Sci 357:373–380
Komdeur J, Magrath MJL, Krackow S (2002) Pre-ovulation control of hatchling sex ratio in the Seychelles warbler. Proc R Soc B Biol Sci 269:1067–1072
Korpelainen H (1990) Sex ratios and conditions required for environmental sex determination in animals. Biol Rev 65(2):147–184
Pen I, Uller T, Feldmeyer B, Harts A, While GM, Wapstra E (2010) Climate-driven population divergence in sex-determining systems. Nature 468(7322):436–438
Radder RS, Warner DA, Shine R (2007) Compensating for a bad start: catch-up growth in juvenile lizards (Amphibolurus muricatus, Agamidae). J Exp Zool 307A(9):500–508
Thompson MB (1990) Incubation of eggs of tuatara, Sphenodon punctatus. J Zool 222(2):303–318
Thompson M (1993) Estimate of the population structure of the estern water dragon, Physignathus lesueurii (Reptilia: Agamidae), along riverside habitat. Wildl Res 20:613–619
Trivers RL, Willard DE (1973) Natural selection of parental ability to vary the sex ratio of offspring. Science 179(4068):90–92
Valenzuela N, Botero R, Martínez E (1997) Field study of sex determination in Podocnemis expansa from Colombian Amazonia. Herpetologica 53(3):390–398
Vitt LJ, Caldwell JP (2013) Reproduction and life histories. In: Vitt LJ, Caldwell JP (eds) Herpetology: an introductory biology of amphibians and reptiles. Academic Press, New York, pp 117–175
Warner DA, Shine R (2005) The adaptive significance of temperature-dependent sex determination: experimental tests with a short-lived lizard. Evolution 59:2209
Warner DA, Shine R (2008) The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451:566–568
Warner DA, Shine R (2011) Interactions among thermal parameters determine offspring sex under temperature-dependent sex determination. Proc R Soc B Biol Sci 278:256–265
Warner DA, Uller T, Shine R (2009) 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
Yamahira K, Conover DO (2003) Interpopulation variability in temperature-dependent sex determination of the Tidewater Silverside Menidia peninsulae. Copeia 2003:155–159
Acknowledgments
The research was aided by funding from the ACT Society of Herpetologists, the Australian Society of Herpetologists, the Peter Rankin Trust Fund for Herpetology and the Wildlife Preservation Society of Australia. NP was supported by a University of Sydney Postgraduate Award. We thank the Australian National Botanic Gardens for facilitating and supporting the study, Jacquie F. Herbert for assistance with incubations and Arthur Georges for use of incubators and facilities at the Institute for Applied Ecology (University of Canberra).
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Pezaro, N., Thompson, M.B. & Doody, J.S. Seasonal sex ratios and the evolution of temperature-dependent sex determination in oviparous lizards. Evol Ecol 30, 551–565 (2016). https://doi.org/10.1007/s10682-016-9820-0
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DOI: https://doi.org/10.1007/s10682-016-9820-0