Developmental plasticity in reptiles: Insights from temperature‐dependent gene expression in wall lizard embryos

Abstract

Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress.

Embryonic Temperature Programs Phenotype in Reptiles

“…Along with DNA methylation, histone modifications have been shown to play a crucial role in early embryonic development in reptiles (Feiner et al, 2018). Kdm6b is differentially expressed between gonadal transcriptomes from embryos incubated at male and female producing temperatures in TSD species Alligator mississippiensis (Yatsu et al, 2016) and Trachemys scripta elegans (Czerwinski et al, 2016).…”

Patterns of developmental plasticity in response to incubation temperature in reptiles

“…However, there are a growing number of exceptions. For example, one study of thermal developmental plasticity in wall lizards ( Podarcis muralis ) identified suites of genes that are up‐ or downregulated at low temperatures (Feiner et al., ). Transcripts with the most extreme changes in expression profiles were associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature.…”

“…Given the above, it is perhaps unsurprising that there is a large and growing empirical literature testing the effects of the thermal environment during incubation on the development of a range of traits across all the major reptile taxa (Deeming, 2004;Deeming & Ferguson 1991;Noble, Stenhouse, & Schwanz, 2018b). This includes incubation duration (e.g., While et al, 2015), developmental processes (e.g., gene expression; Feiner, Rago, While, & Uller, 2018a), morphology (e.g., body size, growth rate; Andrews, Mathies, Warner, & Mathies, 2009;Du et al, 2009Du et al, , 2010Monasterio, Shoo, Salvador, Iraeta, & Díaz, 2013), behavior (e.g., antipredator behavior; Burger, 1990;, performance (e.g., sprint speed; Elphick & Shine 1998), physiology (e.g., hormones, metabolic activity, energy, and nutrient content; Crews, Coomber, Baldwin, Azad, & Gonzalez-Lima, 1996Du, Shou, & Liu, 2003;Ji & Braña 1999), cognition (Amiel & Shine 2012;Clark, Amiel, Shine, Noble, & Whiting, 2014;Dayananda & Webb 2017), and, in many species, sex (Valenzuela & Lance 2004). The phenotypic variation generated in response to the thermal environment has been shown to have fitness consequences in both the short-term (e.g., via increased post-hatching growth and survival; Andrews et al, 2009) and the long-term (e.g., future reproductive success; Warner & Shine 2008b).…”

Epigenetic Responses to Temperature and Climate

“…Incubating wall lizard (Podarcis muralis) eggs at sub-critical temperatures had a strong influence on gene expression associated with epigenetic processes during embryonic development, including histone methyltransferase, histone deacetylase and a chromobox protein homolog associated with chromatin remodelling/organisation. Widespread chromatin remodelling under this process can lead to the transcriptional regulation of embryonic developmental processes, such as zygote cellular differentiation (Feiner et al 2018). In addition, Metzger and Schulte (2017) identified 2130 differentially methylated regions (DMRs) that responded to changes in developmental temperature in three-spine stickleback larvae.…”