The environment experienced by individuals can have significant effects on their phenotype and ultimately fitness. While plastic responses can occur across all life-history stages, they are often most pervasive early in life when an organism undergoes most of its growth and development. Such developmental plasticity is partly unavoidable, for example, as a by-product of physical or physiological limits. However, the extent and form of plasticity is also shaped by natural selection such that developmental responses are fine-tuned to particular environmental conditions. In either case, developmental plasticity is a major source of phenotypic variation that mediates how organisms respond to environmental change at both local and global scales.
Reptiles have been widely used in developmental plasticity research. The environmental factor that has been best studied in this context is temperature (“thermal developmental plasticity”). Indeed, most reptile embryos do not successfully develop when incubated at constant temperatures lower than 20ºC or higher than 35ºC and, within this range, developmental processes are further optimised at particular temperatures. As a result, a large number of studies have shown effects of the thermal environment on the development of a range of traits across all the major reptile taxa (Figure 1). These traits include incubation duration, developmental processes (e.g., gene expression), morphology, behaviour, performance, physiology, cognition and, in many species, sex. Even viviparous reptiles, which have a greater capacity to buffer external thermal conditions throughout development via maternal basking behaviour have been widely studied in this respect, with conditions experienced by the mother before and throughout gestation having a significant effect on offspring phenotype (“maternal thermal effects”).
Figure 1: The phylogenetic distribution of studies into thermal developmental plasticity in egg laying reptiles (from While et al. in press).
Despite this, there are a number areas of research that remain to be fully explored with regards to thermal developmental plasticity in reptiles. First, we know almost nothing about the about the underlying mechanisms generating and maintaining different developmental outcomes in response to thermal environments. Nor do we understand the extent to which parental (especially maternal) environmental effects interact with the thermal environment to impact offspring development. Second, the adaptive significance of thermal developmental plasticity remains unclear for the majority of species and traits. Third, we have a poor understanding of the extent to which thermal developmental plasticity varies across spatial or temporal scales.
To address this, we use a combination of field, laboratory, molecular and comparative approaches that are specifically designed to explore the causes and consequences of thermal developmental plasticity and, specifically, maternal thermal effects. The majority of this work focuses on a number of viviparous skink species’. This work combines field and laboratory approaches to i) characterise the extent of thermal developmental plasticity across a range of traits, ii) explore how these maternal thermal effects varies across a range of climatic conditions and ii) test the fitness consequences of maternal thermal effects. Much of this work is closely tied with our work examining the evolutionary dynamics of sex determination. Ongoing research is combining these approaches with a more detailed examination of the molecular causes and consequences of maternal thermal effects (e.,g., the role of heat shock proteins and telomeres). In addition to this, our work on Wall Lizards combines incubation experiments with sophisticated molecular techniques to examine the extent to which thermal developmental plasticity plays out at the level of gene expression. This work has identified suites of genes that are up- or down-regulated at low temperatures and has suggested that these effects are mediated by a number of epigenetic mechanisms. Finally, our collaborative work with the Reptile Developmental Database (“RepDevo“), provides us with a unique data set of almost 10,000 effect sizes on developmental responses of oviparous species to incubation temperature that can be used to explore how thermal developmental plasticity plays out a macro-ecological scale.
This work is carried out in collaboration with Daniel Noble (UNSW), Lisa Schwanz (UNSW), Dan Warner (Auburn), Wei-Gu Duo (Chinese Academy of Sciences), Tobias Uller (Lund), Nathalie Feiner (Lund), Alfredo Rago (Lund), Mats Olsson (Gothenburg) and Rick Shine (Sydney).
If you want to know more:
Cunningham, G.D., While, G.M., Olsson, M., Ljungstrom, G. and Wapstra, E. (2020) Degrees of change: between and within population variation in thermal reaction norms of phenology in a viviparous lizard. Ecology. 101: e03136.
While, G.M., Noble, D. W. A., Uller, T., Warner, D.A., Riley, J.E., Du, W.G. and Schwanz, L. E. (2018) Patterns of developmental plasticity in response to the thermal incubation environment in reptiles. Journal of Experimental Zoology, Part A (invited contribution). 329: 162-176.
Feiner, N., Rago, A., While, G.M. and Uller, T. (2018) Developmental plasticity in reptiles: Insights from temperature-dependent gene expression in wall lizards. Journal of Experimental Zoology, Part A (invited contribution). 329: 351-361.
Noble, D. W. A., Stenhouse, V., Riley, J. E., Warner, D. A., While, G.M., Du, W-G., Uller, T. and Schwanz, L E.. (2018) A comprehensive database of thermal developmental plasticity in reptiles. Scientific Data. 5:180138.
Uller, T., While, G.M., Cadby, C.D., Harts, A., O’Connor, K., Pen, I., and Wapstra, E. (2011) Thermal opportunity, maternal effects, and offspring survival at different climatic extremes in a viviparous lizard. Evolution, 65: 2313–2324.
Cadby, C.D., Jones, S.M. and Wapstra, E. (2010) Are elevated levels of maternal corticosterone adaptive to offspring? A test using a viviparous lizard with complex placenta (Niveoscincus ocellatus). Functional Ecology, 24: 409-416
Uller, T., Wapstra, E. & Badyaev, A. V. (2009) Evolution of Parental Effects. Conceptual Issues and Empirical Patterns. Philosophical Transactions of the Royal Society, theme issue, Volume 364.