In the viviparous Tasmanian snow skink Carinascincus (formerly Niveoscincus) ocellatus, offspring sex ratios at birth fluctuate among years in step with natural thermal variation, with male-biased cohorts in colder years. The mechanism is now known to be thermally induced sex reversal acting over an XX/XY chromosomal system, and populations at climatic extremes of the range differ adaptively in how strongly temperature influences sex. What remains unresolved is the fate of these climate-driven cohort biases: whether they propagate through sex-specific survival into adult sex ratios and measurable demographic consequences under directional warming or increasing interannual variability, and how much maternal behavioural thermoregulation and evolution of the thermal sensitivity of sex determination can buffer that propagation. The problem asks for field-demographic quantification of cohort-to-adult propagation, quantification of the magnitude and limits of behavioural buffering of offspring sex, and evidence on whether sex-determination reaction norms can shift adaptively across or within populations.

Background

Viviparity (live birth) is widespread in cool-climate reptiles, and a long-standing idea holds that because gravid females thermoregulate behaviourally — basking to maintain body temperatures within a preferred range — the mother shields developing embryos from ambient thermal extremes that an egg in a nest would experience. Sex determination in reptiles spans a continuum from genotypic sex determination (GSD, sex fixed by sex chromosomes at fertilization) to temperature-dependent sex determination (TSD, sex set by the incubation temperature experienced by the embryo, conventionally described by pivotal or threshold temperatures on a reaction norm, i.e. the curve relating incubation temperature to probability of developing as male). Between these poles lie systems with chromosomal sex determination whose outcome can still be overridden by temperature via sex reversal: genetically female (XX) individuals developing as phenotypic males, or the converse. The spotted snow skink, Carinascincus ocellatus (until recently placed in the genus Niveoscincus), is a small short-lived viviparous scincid lizard from Tasmania whose populations occupy steep climatic (altitudinal) gradients, making it a natural experiment for these questions.

Wapstra, Uller, Sinn, Olsson, Mazurek, Joss and Shine (2009) monitored a free-living lowland population over seven field seasons and showed for the first time in a viviparous ectotherm that cohort sex ratios at birth (parturition) fluctuated significantly among years and tracked natural thermal conditions, with the proportion of male offspring increasing in colder years; under warming scenarios this predicts female-biased birth cohorts, and increased interannual variability predicts amplified cohort sex-ratio fluctuations. At the time the species was described as having TSD. Later work substantially revised and advanced that picture. Pen, Uller, Feldmeyer, Harts, While and Wapstra (2010) showed in Nature that populations at climatic extremes of the range use different sex-determining mechanisms — temperature influences sex in the lowlands whereas sex is genotypic at high altitude — and that this divergence is adaptive, predicted by a model parameterized with field life-history data; sex-linked molecular markers and cytogenetics later confirmed conserved XX/XY sex chromosomes with population-level differences in Y differentiation (Hill et al. 2018, 2021), and the divergent populations turn out to have been genetically isolated since the Pleistocene (Hill et al. 2021). A 16-year two-population field study confirmed the population-specificity: female offspring became more common in warm years at the lowland site while birth date advanced with temperature at both sites, showing the sex-ratio response is specific rather than a by-product of a general phenological shift (Cunningham, While and Wapstra 2017). Mechanistically, laboratory thermal experiments demonstrated that sex reversal — XX offspring developing as phenotypic males — occurs in both elevation populations with temperature-dependent frequency, explaining some but not all of the climate-mediated sex-ratio variation (Hill et al. 2022), and a 23-year field study integrating phenotypic and genetic sexing recently provided the first evidence of wild sex reversal in a viviparous reptile: XX males occurred in both populations (up to 23.5% of XX births in the warmer one, associated with colder minimum daily temperatures), sex-reversed adults were rare, and putative XY females suggest bidirectional reversal (Ferre-Ortega et al. 2026, preprint).

On the buffering and evolutionary sides: gravid females of this species fine-tune basking behaviour to the available basking opportunity and thereby buffer their embryos from deleterious developmental temperatures, with alpine females more opportunistic than lowland females (Cadby, Jones and Wapstra 2014); maternal thermoregulatory behaviour diverges altitudinally in ways plausibly driven by selection on offspring survival (Uller et al. 2011); and there is field and experimental evidence of selection on maternal basking for offspring fitness (Wapstra et al. 2010). Yet a multifactorial field-plus-laboratory analysis found the strong field temperature effect on sex allocation was not reproduced under controlled laboratory conditions, and no effect of maternal resource availability (Gruber et al. 2018), so the contribution of behaviour to buffering offspring sex specifically remains unquantified. Theory addresses the evolutionary side — quantitative models of temperature-driven turnovers of sex-determining mechanisms (Grossen, Neuenschwander and Perrin 2011) and a conceptual framework of individual reaction norms for sex determination (Pezaro, Doody and Thompson 2017) — but there is no empirical demonstration that the thermal sensitivity of sex determination can shift adaptively within or between populations of this or any viviparous reptile; across vertebrates, offspring of sex-reversed parents appear unusually sensitive to environmental perturbation (Piferrer and Anastasiadi 2021), an untested hypothesis in this system. Demographic consequences of climate-driven sex ratios have so far been explored only in generic models, which show that whether skewed sex ratios enhance or erode population persistence hinges critically on male limitation of female fecundity and on how survival co-varies with temperature (Boyle et al. 2014a,b); no species-specific empirical demography exists for C. ocellatus.

Problem Statement

In free-living populations of the viviparous snow skink Carinascincus ocellatus — where cohort sex ratios at parturition are now known to vary with natural thermal conditions through thermally induced sex reversal acting over an XX/XY chromosomal system, with population-specific thermal sensitivity — determine: (1) whether and how strongly climate-driven cohort sex-ratio biases at birth propagate into adult and operational sex ratios (the ratio of sexually competing males to fertilizable females in the population) through sex-specific postnatal survival and recruitment, and whether they produce measurable demographic consequences (population growth or viability) under directional warming and increased interannual temperature variability, given the mating-system conditions that determine whether female-biased cohorts translate into population-level change — in particular the extent to which male abundance limits female fecundity, and how cohort sex ratios co-vary with temperature-dependent survival; (2) the magnitude and limits of behavioural compensation by gravid females — adjustments of basking and other thermoregulatory behaviour during gestation — in buffering the effect of natural climatic variation on offspring sex, as distinct from buffering embryonic thermal conditions generally; and (3) whether the thermal sensitivity of sex determination (the temperature thresholds and reaction norms governing sex reversal and embryo thermal response) can shift adaptively across or within populations, or whether selection instead favours changes in maternal traits such as basking preference and timing of reproduction. These are linked components of one objective: the fate of climate-driven offspring sex-ratio bias from mechanism to demography, and the capacity of behaviour and evolution to buffer it.

References

  1. Wapstra, E., Uller, T., Sinn, D. L., Olsson, M., Mazurek, K., Joss, J., & Shine, R. (2009). Climate effects on offspring sex ratio in a viviparous lizard. Journal of Animal Ecology, 78(1), 84–90. DOI: 10.1111/j.1365-2656.2008.01470.x. https://doi.org/10.1111/j.1365-2656.2008.01470.x
  2. Pen, I., Uller, T., Feldmeyer, B., Harts, A., While, G. M., & Wapstra, E. (2010). Climate-driven population divergence in sex-determining systems. Nature, 468(7322), 436–438. DOI: 10.1038/nature09512. https://doi.org/10.1038/nature09512
  3. Cunningham, G. D., While, G. M., & Wapstra, E. (2017). Climate and sex ratio variation in a viviparous lizard. Biology Letters, 13(5), 20170218. DOI: 10.1098/rsbl.2017.0218. https://doi.org/10.1098/rsbl.2017.0218
  4. Hill, P. L., While, G. M., Burridge, C. P., Ezaz, T., Munch, K. L., McVarish, M., & Wapstra, E. (2022). Sex reversal explains some, but not all, climate-mediated sex ratio variation within a viviparous reptile. Proceedings of the Royal Society B: Biological Sciences, 289(1976), 20220689. DOI: 10.1098/rspb.2022.0689. https://doi.org/10.1098/rspb.2022.0689
  5. Ferre-Ortega, C., Saunders, P., Richards, S. A., Burridge, C. P., Fitzpatrick, L., Hill, P., Cunningham, G. D., While, G., Ezaz, T., & Wapstra, E. (2026). Thermally driven sex reversal reveals divergent sex determination dynamics in wild viviparous reptile populations. bioRxiv preprint. DOI: 10.64898/2026.06.25.734438. https://doi.org/10.64898/2026.06.25.734438
  6. Cadby, C. D., Jones, S. M., & Wapstra, E. (2014). Geographical differences in maternal basking behaviour and offspring growth rate in a climatically widespread viviparous reptile. Journal of Experimental Biology, 217(7), 1175–1179. DOI: 10.1242/jeb.089953. https://doi.org/10.1242/jeb.089953
  7. Uller, T., While, G. M., Cadby, C. D., Harts, A., O'Connor, K., Pen, I., & Wapstra, E. (2011). Altitudinal divergence in maternal thermoregulatory behaviour may be driven by differences in selection on offspring survival in a viviparous lizard. Evolution, 65(8), 2313–2324. DOI: 10.1111/j.1558-5646.2011.01303.x. https://doi.org/10.1111/j.1558-5646.2011.01303.x
  8. Gruber, J., Cunningham, G. D., While, G. M., & Wapstra, E. (2018). Disentangling sex allocation in a viviparous reptile with temperature-dependent sex determination: a multifactorial approach. Journal of Evolutionary Biology, 31(2), 267–276. DOI: 10.1111/jeb.13219. https://doi.org/10.1111/jeb.13219
  9. Wapstra, E., Uller, T., While, G. M., Olsson, M., & Shine, R. (2010). Giving offspring a head start in life: field and experimental evidence for selection on maternal basking behaviour in lizards. Journal of Evolutionary Biology, 23(3), 651–657. DOI: 10.1111/j.1420-9101.2009.01924.x. https://doi.org/10.1111/j.1420-9101.2009.01924.x
  10. Pezaro, N., Doody, J. S., & Thompson, M. B. (2017). The ecology and evolution of temperature-dependent reaction norms for sex determination in reptiles: a mechanistic conceptual model. Biological Reviews, 92(3), 1348–1364. DOI: 10.1111/brv.12285. https://doi.org/10.1111/brv.12285
  11. Grossen, C., Neuenschwander, S., & Perrin, N. (2011). Temperature-dependent turnovers in sex-determination mechanisms: a quantitative model. Evolution, 65(1), 64–78. DOI: 10.1111/j.1558-5646.2010.01098.x. https://doi.org/10.1111/j.1558-5646.2010.01098.x
  12. Boyle, M., Hone, J., Schwanz, L. E., & Georges, A. (2014a). Under what conditions do climate-driven sex ratios enhance versus diminish population persistence? Ecology and Evolution, 4(23), 4522–4533. DOI: 10.1002/ece3.1316. https://doi.org/10.1002/ece3.1316
  13. Boyle, M., Schwanz, L. E., Hone, J., & Georges, A. (2014b). How do climate-linked sex ratios and dispersal limit range boundaries? BMC Ecology, 14, 19. DOI: 10.1186/1472-6785-14-19. https://doi.org/10.1186/1472-6785-14-19
  14. Hill, P. L., Burridge, C. P., Ezaz, T., & Wapstra, E. (2018). Conservation of sex-linked markers among conspecific populations of a viviparous skink, Niveoscincus ocellatus, exhibiting genetic and temperature-dependent sex determination. Genome Biology and Evolution, 10(4), 1079–1087. DOI: 10.1093/gbe/evy042. https://doi.org/10.1093/gbe/evy042
  15. Hill, P., Shams, F., Burridge, C., Wapstra, E., & Ezaz, T. (2021a). Differences in homomorphic sex chromosomes are associated with population divergence in sex determination in Carinascincus ocellatus (Scincidae: Lygosominae). Cells, 10(2), 291. DOI: 10.3390/cells10020291. https://doi.org/10.3390/cells10020291
  16. Hill, P., Wapstra, E., Ezaz, T., & Burridge, C. P. (2021b). Pleistocene divergence in the absence of gene flow among populations of a viviparous reptile with intraspecific variation in sex determination. Ecology and Evolution, 11(10), 5575–5583. DOI: 10.1002/ece3.7458. https://doi.org/10.1002/ece3.7458
  17. Wapstra, E., & While, G. M. (2009). Snow skinks (Niveoscincus ocellatus) do not shift their sex allocation patterns in response to mating history. Behaviour, 146(10), 1405–1422. DOI: 10.1163/156853909X436254. https://doi.org/10.1163/156853909X436254
  18. Piferrer, F., & Anastasiadi, D. (2021). Do the offspring of sex reversals have higher sensitivity to environmental perturbations? Sexual Development, 15(1–3), 134–147. DOI: 10.1159/000515192. https://doi.org/10.1159/000515192
  19. Cunningham, G. D., While, G. M., Olsson, M., Ljungström, G., & Wapstra, E. (2020). Degrees of change: between and within population variation in thermal reaction norms of phenology in a viviparous lizard. Ecology, 101(10), e03136. DOI: 10.1002/ecy.3136. https://doi.org/10.1002/ecy.3136