For animals that deposit their eggs in terrestrial nests, the most vulnerable stage of life, embryonic development, is exposed to uncontrollable and sometimes unpredictable environmental conditions. Changes in the climate are known to alter temperatures within the nests of reptiles (Hays et al., 2003; Schwanz et al., 2010a). This may be a problem for developing embryos, as incubation temperatures have widespread effects on hatchling survival, morphology and performance (Deeming, 2004; Shine, 2004). In addition, for reptiles with temperature-dependent sex determination, development as a male or female is determined irreversibly during the egg stage (Janzen & Paukstis, 1991). Thus, it seems inevitable that climatic warming and its effects on early life stages will drive these animals to a demographic collapse.

However, the connection between climate and demography is not so straightforward for these species. First, compared with laboratory incubation studies, we know comparatively little about how conditions in natural nests influence phenotypes (see, e.g. Shine, Elphick & Harlow, 1997; Schwanz et al., 2010a). Secondly, mean annual nest temperatures may not vary with annual climate if females alter their nesting behaviour as a function of climate (Doody et al., 2006; Schwanz & Janzen, 2008; Telemeco, Elphick & Shine, 2009). Thirdly, the relationship between incubation temperature and phenotype (survival and sex) could vary with climate (Schwanz, Janzen & Proulx, 2010b) if, for example, yolks contain greater amounts of heat-shock proteins or hormones in extreme-temperature years (Janzen et al., 1998; Bowden, Ewert & Nelson, 2000). Finally, if average nest temperatures warm under climate change and lead to reduced viability and biased sex ratios, selection on nesting behaviours or temperature dependence of phenotypes could lead to local evolutionary response (i.e. evolutionary adaptation).

Refsnider et al. (2013) tackle two of these issues in their paper on nest depth in painted turtles, a species with temperature-dependent sex determination. First, they consider how nest conditions in a natural setting influence offspring phenotype. Secondly, they provide an analysis of whether variation in nest depth (i.e. a component of maternal nesting behaviour) can compensate for annual climatic variation. Moreover, they employ two under-represented methodological approaches – leveraging long-term data on a population (Schwanz et al., 2009) and performing a manipulative experiment.

What the study finds is rather disheartening for animal conservation. Specifically, variation in nest depth, at least in this population of painted turtles, does not appear to be a likely candidate for behavioural compensation or microevolutionary response to climate change. Refsnider et al. (2013) show that nest depth, like the timing of nesting and the shading over the nest, is a component of maternal plasticity in nesting behaviour in painted turtles (Schwanz & Janzen, 2008; McGaugh et al., 2010; Refsnider & Janzen, 2012). Mean nest depth was deeper in warmer years.

Changing nest depth does not seem to ameliorate the effects of climate change, however. In natural nests manipulated to be deep, average or shallow in their depth, nest depth had no statistically detectable effect on nest temperature (e.g. mean, maximum, daily range), nor did it influence nest sex ratio. Interestingly, despite the lack of detectable effect on nest temperature, nest depth treatment influenced offspring performance. Hatchlings from deep nests were faster at righting themselves when turned upside down and were faster in swimming trials. That performance, but not temperature, was influenced by nest depth treatment indicates that either: (1) very small differences in nest temperature can have profound effect on performance in this species or (2) variation in nest depth causes important variation in unmeasured nest traits, such as moisture, which, in turn, strongly influence hatchling performance.

Thanks to Herculean efforts in a few model species, a consistent picture is emerging regarding climate and its effects on hatchling sex ratios. First, across geographical scales, variation in nesting characteristics (nest timing and location) among populations of terrestrial and freshwater reptiles appears to be the main factor minimizing geographic variation in hatchling sex ratios (Bull, Vogt & McCoy, 1982a; Doody et al., 2006). Secondly, and in contrast to the geographical pattern, behavioural plasticity in nesting traits within a population across years appears to be inadequate to prevent climate-driven variation in nest temperatures and hatchling sex ratios (Schwanz & Janzen, 2008; Telemeco et al., 2009; but see Refsnider & Janzen, 2012). This overall picture is compelling, but it comes from a few, well-studied species. Thus, one obvious recommendation for advancing the field is to invest in research on a greater number of species so that we can speak in generality.

Continued examination of model species with long-term data could also provide essential new insight. For example, are the patterns that we see across historical climatic variation predictive of what we can expect at extreme climates? Most notably, the sex ratio of hatchlings in painted turtles varies strongly with July air temperature, such that more males are produced in cool years and more females in warm years (Janzen, 1994; Schwanz et al., 2010a). However, the extremely warm years do not produce all females (Schwanz et al., 2010a). That is to say, at the extreme of warm temperatures (those relevant for climatic warming), behavioural or physiological plasticity may have a promising compensatory effect that they do not have at other temperatures.

Finally, long-term data on model species allow us to address the likelihood of local evolution. Heritability of traits related to reptile sex ratios has been measured in a handful of species, quantifying the potential of a population to respond to selection (Bull, Vogt & Bulmer, 1982b; Janzen, 1992; McGaugh et al., 2010; Rhen et al., 2011). However, we know almost nothing about selection on these traits. What is missing is information on (1) how variation in morphology and performance affects survival and reproductive success throughout an organism's life (Warner & Shine, 2008) and (2) how the strength of selection for survival compares to frequency-dependent selection on the sex ratio.


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  2. References
  • Bowden, R.M., Ewert, M.A. & Nelson, C.E. (2000). Environmental sex determination in a reptile varies seasonally and with yolk hormones. Proc. Biol. Sci. 267, 17451749.
  • Bull, J.J., Vogt, R.C. & Bulmer, M.G. (1982b). Heritability of sex ratio in turtles with environmental sex determination. Evolution 36, 333341.
  • Bull, J.J., Vogt, R.C. & McCoy, C.J. (1982a). Sex determining temperatures in turtles: a geographic comparison. Evolution 36, 326332.
  • Deeming, D.C. (2004). Post-hatching phenotypic effects of incubation in reptiles. In Reptilian incubation: Environment, evolution and behaviour: 229251. Deeming, D.C. (Ed.). Nottingham: Nottingham University Press.
  • Doody, J.S., 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, 307330.
  • Hays, G.C., Broderick, A.C., Glen, F. & Godley, B.J. (2003). Climate chance and sea turtles: a 150-year reconstruction of incubation temperatures at a major marine turtle rookery. Glob. Chang. Biol. 9, 642646.
  • Janzen, F.J. (1992). Heritable variation for sex ratio under environmental sex determination in the common snapping turtle (Chelyrda serpentina). Genetics 131, 155161.
  • Janzen, F.J. (1994). Climate change and temperature-dependent sex determination in reptiles. Proc. Natl. Acad. Sci. USA 91, 74877490.
  • Janzen, F.J. & Paukstis, G.L. (1991). Environmental sex determination in reptiles: ecology, evolution, and experimental design. Q. Rev. Biol. 66, 149179.
  • Janzen, F.J., Wilson, M.E., Tucker, J.K. & Ford, S.P. (1998). Endogenous yolk steroid hormones in turtles with different sex-determining mechanisms. Gen. Comp. Endocrinol. 111, 306317.
  • McGaugh, S., Schwanz, L.E., Bowden, R.M., Gonzalez, J.E. & Janzen, F.J. (2010). Inheritance of nesting behaviour across natural environmental variation in a turtle with temperature-dependent sex determination. Proc. Biol. Sci. 277, 12191226.
  • Refsnider, J.M. & Janzen, F.J. (2012). Behavioural plasticity may compensate for climate change in a long-lived reptile with temperature-dependent sex determination. Biol. Conserv. 152, 9095.
  • Refsnider, J.M., Bodensteiner, B.L., Reneker, J.L. & Janzen, F.J. (2013). Nest depth may not compensate for sex ratio skews caused by climate change in turtles. Anim. Conserv. 16, 481490.
  • Rhen, T., Schroeder, A., Sakata, J.T., Huang, V. & Crews, D. (2011). Segregating variation for temperature-dependent sex determination in a lizard. Heredity 106, 649660.
  • Schwanz, L.E. & Janzen, F.J. (2008). Climate change and temperature-dependent sex determination: can plasticity in maternal nesting behavior prevent extreme sex ratios? Physiol. Biochem. Zool. 81, 826834.
  • Schwanz, L.E., Bowden, R.M., Spencer, R.-J. & Janzen, F.J. (2009). Nesting ecology and offspring recruitment in a long-lived turtle. Ecology 90, 17091710.
  • Schwanz, L.E., Spencer, R.-J., Bowden, R.M. & Janzen, F.J. (2010a). Climate and predation dominate early life-stages and adult recruitment in a turtle with temperature-dependent sex determination: insight from a long-term study. Ecology 91, 30163026.
  • Schwanz, L.E., Janzen, F.J. & Proulx, S.R. (2010b). Sex allocation based on relative and absolute condition. Evolution 64, 13311345.
  • Shine, R. (2004). Adaptive consequences of developmental plasticity. In Reptilian incubation: Environment, evolutionand behaviour: 187210. Deeming, D.C. (Ed.). Nottingham: Nottingham University Press.
  • Shine, R., Elphick, M.J. & Harlow, P.S. (1997). The influence of natural incubation environments on the phenotypic traits of hatchlings lizards. Ecology 78, 25592568.
  • Telemeco, R.S., Elphick, M.J. & Shine, R. (2009). Nesting lizards (Bassiana duperreyi) compensate partly, but not completely, for climate change. Ecology 90, 1722.
  • Warner, D.A. & Shine, R. (2008). The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451, 566569.