The montane water skink Eulamprus tympanum was one of the first viviparous reptiles reported to show temperature-dependent sex determination (TSD), and two early studies reported that females bias offspring sex ratios in response to the operational sex ratio (OSR), the ratio of fertilizable females to sexually active males in the population. Allsop, Warner, Langkilde, Du and Shine (2006) tested this experimentally with the first field-based manipulation: OSR altered pregnant females' thermoregulatory behaviour (maximum selected temperature) during gestation, but the thermal shift was too small to move litter sex ratios, and no offspring phenotype responded. The paper left a precise and still-unresolved agenda: when in the reproductive cycle females assess OSR, what minimal thermal change is needed to shift offspring sex, which proximate cues mediate any response, and how social and thermal environments interact in natural populations. Later work neither confirmed nor refuted the hypothesis: replication attempts in three viviparous skink/lizard species were negative or non-conforming, proximate cues remain unidentified, and 2018-2022 genomic studies revised the premise itself by revealing cryptic XY sex chromosomes with thermally induced sex reversal in these lineages. The open core is a mechanistic question: whether females of viviparous skinks with thermolabile sex determination can, and do, facultatively bias offspring sex in response to social cues, through what timing, cue, and thermal pathway, and whether this operates in the wild.

Background

Sex-allocation theory predicts that when the fitness returns from sons and daughters differ, mothers benefit from biasing offspring sex. Fisher's equal-investment principle sets the null expectation of equal sex ratios, and Werren and Charnov (1978) showed that in populations with overlapping generations, females should facultatively overproduce the sex that is currently rare in response to the operational sex ratio (OSR) — the ratio of fertilizable females to sexually active males, which measures the intensity of mating competition. Empirical support in vertebrates is weak and inconsistent, and reptiles with temperature-dependent sex determination (TSD, where the temperature experienced by the embryo rather than inherited sex chromosomes determines gonadal sex) offer an unusual candidate mechanism: a mother could in principle adjust offspring sex behaviourally, by choosing body or nest temperatures, without needing sex chromosomes to skew segregation. The candidate problem sits squarely in this setting. The montane water skink Eulamprus tympanum is a viviparous (live-bearing) lizard from south-eastern Australia in which gestation temperature, not sex chromosomes, was long thought to determine embryo sex: constant warm gestation (around 32 °C) yields male offspring and cooler gestation yields females, with the middle third of gestation believed to house the thermosensitive window. Robert and Thompson (2001) reported that females of this species could 'select sex of embryos' via body temperature, Robert, Thompson and Seebacher (2003) reported that wild E. tympanum females in male-scarce years produced male-biased litters, and Olsson and Shine (2001) reported operational-sex-ratio-conforming shifts in the snow skink Niveoscincus microlepidotus — but Le Galliard et al. (2005) found no such adjustment in the common lizard. Allsop, Warner, Langkilde, Du and Shine (2006) then ran the first field-plus-laboratory experimental manipulation, assigning gravid E. tympanum females to female-biased or male-biased OSR enclosures during gestation: the manipulation shifted only one component of maternal thermoregulation (the maximum selected temperature, about 0.8 °C higher under female-biased OSR), a change too small to alter litter sex ratios or any offspring trait measured. Genomic work after 2018 has since revised the premise's mechanistic basis — cryptic XY sex chromosomes with temperature-induced sex reversal (rather than 'pure' temperature-dependent sex determination) appear to underlie these and allied lineages — which sharpens, but does not answer, the question of whether mothers can behaviourally modulate offspring sex in response to the social environment. The unresolved question inherited from Allsop et al. (2006) is therefore mechanistic and ecological at once: when females could assess OSR, how large a thermal change would actually be needed, through which proximate cues, and whether any such pathway operates in nature.

Problem Statement

Determine whether, and by what pathway, females of viviparous skinks with thermolabile sex determination (Eulamprus tympanum and the allied snow-skink lineage, in which cryptic XY chromosomes can be overridden by developmental temperature) facultatively adjust the sex of their offspring in response to the operational sex ratio (OSR — the ratio of fertilizable females to sexually active males) of the population, in the four linked respects left open by Allsop et al. (2006): (1) timing — the phase of the reproductive cycle at which females assess OSR (pre-ovulation versus during the gestational window of sexual differentiation), and whether information gathered before ovulation can be acted upon later in development, which the source's gestation-only OSR manipulation leaves open; (2) dose — the minimum magnitude, temporal pattern (mean, maximum, variance of selected body temperature), and timing relative to the thermosensitive period of the maternal thermal change that actually shifts offspring sex ratios, with the interpretive caution that in lineages with cryptic XY chromosomes a thermal shift could act through temperature-induced sex reversal rather than maternal allocation; (3) mechanism — the proximate cues beyond raw adult sex composition (e.g. mating frequency, perceived male density, endocrine state, mating scars) that females could use to forecast offspring-specific fitness returns and mediate the allocation; and (4) ecological validity — whether the pathway operates in natural populations, where microhabitat variation in thermal opportunity, among-year variation in breeding participation, and the social environment jointly determine offspring sex ratios. These four components jointly characterize one question — is social-environment-driven maternal control of offspring sex a real, mechanistically identifiable phenomenon in viviparous reptiles, or an artefact of small-sample correlative studies — and a resolution consists of either establishing the phenomenon for at least one lineage by answering all four respects (1)–(4), or definitively refuting it as an artefact for the whole class of viviparous skinks with thermolabile sex determination (Eulamprus tympanum and the allied snow-skink lineage); answering only a subset of the four respects, or refuting the phenomenon in a single lineage, is a partial result that does not by itself resolve the task.

References

  1. Allsop, D. J., Warner, D. A., Langkilde, T., Du, W., & Shine, R. (2006). Do operational sex ratios influence sex allocation in viviparous lizards with temperature-dependent sex determination? Journal of Evolutionary Biology 19(4):1175–1182. DOI: 10.1111/j.1420-9101.2006.01086.x. URL: https://doi.org/10.1111/j.1420-9101.2006.01086.x
  2. Olsson, M., & Shine, R. (2001). Facultative sex allocation in snow skink lizards (Niveoscincus microlepidotus). Journal of Evolutionary Biology 14(1):120–128. DOI: 10.1046/j.1420-9101.2001.00255.x. URL: https://doi.org/10.1046/j.1420-9101.2001.00255.x
  3. Robert, K. A., & Thompson, M. B. (2001). Viviparous lizard selects sex of embryos. Nature 412(6848):698–699. DOI: 10.1038/35089135. URL: https://doi.org/10.1038/35089135
  4. Robert, K. A., Thompson, M. B., & Seebacher, F. (2003). Facultative sex allocation in the viviparous lizard Eulamprus tympanum, a species with temperature-dependent sex determination. Australian Journal of Zoology 51(4):367–370. DOI: 10.1071/zo03016. URL: https://doi.org/10.1071/zo03016
  5. Le Galliard, J.-F., Fitze, P. S., Cote, J., Massot, M., & Clobert, J. (2005). Female common lizards (Lacerta vivipara) do not adjust their sex-biased investment in relation to the adult sex ratio. Journal of Evolutionary Biology 18(6):1455–1463. DOI: 10.1111/j.1420-9101.2005.00950.x. URL: https://doi.org/10.1111/j.1420-9101.2005.00950.x
  6. Werren, J. H., & Charnov, E. L. (1978). Facultative sex ratios and population dynamics. Nature 272(5651):349–350. DOI: 10.1038/272349a0. URL: https://doi.org/10.1038/272349a0
  7. Warner, D. A., & Shine, R. (2007). Reproducing lizards modify sex allocation in response to operational sex ratios. Biology Letters 3(1):47–50. DOI: 10.1098/rsbl.2006.0579. URL: https://doi.org/10.1098/rsbl.2006.0579
  8. Warner, D. A., & Shine, R. (2008). The adaptive significance of temperature-dependent sex determination in a reptile. Nature 451(7178):566–568. DOI: 10.1038/nature06519. URL: https://doi.org/10.1038/nature06519
  9. Wapstra, E., Uller, T., Pen, I., Komdeur, J., Olsson, M., & Shine, R. (2007). Disentangling the complexities of vertebrate sex allocation: a role for squamate reptiles? Oikos 116(6):1051–1057. DOI: 10.1111/j.2007.0030-1299.15811.x. URL: https://doi.org/10.1111/j.2007.0030-1299.15811.x
  10. Wapstra, E., & Warner, D. A. (2010). Sex allocation and sex determination in squamate reptiles. Sexual Development 4(1–2):110–118. DOI: 10.1159/000272459. URL: https://doi.org/10.1159/000272459
  11. Robert, K. A., & Thompson, M. B. (2010). Viviparity and temperature-dependent sex determination. Sexual Development 4(1–2):119–128. DOI: 10.1159/000260373. URL: https://doi.org/10.1159/000260373
  12. 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. URL: https://doi.org/10.1111/j.1365-2656.2008.01470.x
  13. While, G. M., & Wapstra, E. (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. URL: https://doi.org/10.1163/156853909X436254
  14. Baron, J.-P., Tully, T., & Le Galliard, J.-F. (2010). Sex-specific fitness returns are too weak to select for non-random patterns of sex allocation in a viviparous snake. Oecologia 164(2):369–378. DOI: 10.1007/s00442-010-1660-y. URL: https://doi.org/10.1007/s00442-010-1660-y
  15. 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. URL: https://doi.org/10.1038/nature09512
  16. Navara, K. J. (2013). Hormone-mediated adjustment of sex ratio in vertebrates. Integrative and Comparative Biology 53(6):877–887. DOI: 10.1093/icb/ict081. URL: https://doi.org/10.1093/icb/ict081
  17. Zhang, D.-J., Tang, X.-L., Yue, F., Chen, Z., Li, R.-D., & Chen, Q. (2010). Effect of gestation temperature on sexual and morphological phenotypes of offspring in a viviparous lizard, Eremias multiocellata. Journal of Thermal Biology 35(3):129–133. DOI: 10.1016/j.jtherbio.2010.01.003. URL: https://doi.org/10.1016/j.jtherbio.2010.01.003
  18. Tang, X.-L., Yue, F., Zhang, D.-J., Yan, X.-F., Xin, Y., Wang, C., & Chen, Q. (2012). The effect of operational sex ratio on sex allocation and neonate phenotype in a viviparous lizard Eremias multiocellata. Amphibia-Reptilia 33(3–4):485–493. DOI: 10.1163/15685381-00002851. URL: https://doi.org/10.1163/15685381-00002851
  19. Tang, X.-L., Yue, F., Yan, X.-F., Zhang, D.-J., Xin, Y., Wang, C., & Chen, Q. (2012). Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude. Journal of Thermal Biology 37(6):438–444. DOI: 10.1016/j.jtherbio.2012.03.002. URL: https://doi.org/10.1016/j.jtherbio.2012.03.002
  20. 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. URL: https://doi.org/10.1098/rsbl.2017.0218
  21. 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. URL: https://doi.org/10.1111/jeb.13219
  22. 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. URL: https://doi.org/10.1093/gbe/evy042
  23. Cornejo-Páramo, P., Dissanayake, D. S. B., Lira-Noriega, A., Martínez-Pacheco, M. L., Acosta, A., Ramírez-Suástegui, C., Méndez-de-la-Cruz, F. R., Székely, T., Urrutia, A. O., Georges, A., & Cortez, D. (2020). Viviparous reptile regarded to have temperature-dependent sex determination has old XY chromosomes. Genome Biology and Evolution 12(6):924–930. DOI: 10.1093/gbe/evaa104. URL: https://doi.org/10.1093/gbe/evaa104
  24. Hill, P., 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. URL: https://doi.org/10.1098/rspb.2022.0689
  25. Hansson, A., Wapstra, E., While, G. M., Lindsay, W. R., & Olsson, M. (2023). Context-dependent thermolability of sex determination in a lacertid lizard with heteromorphic sex chromosomes. Biology Open 12(5):059967. DOI: 10.1242/bio.059967. URL: https://doi.org/10.1242/bio.059967
  26. Santidrián Tomillo, P. (2024). Re-equilibrating sex ratios: adjustment of reaction norms in species with temperature-dependent sex determination. Global Change Biology 30(11):e17568. DOI: 10.1111/gcb.17568. URL: https://doi.org/10.1111/gcb.17568