Adaptive responses of the embryos of birds and reptiles to spatial and temporal variations in nest temperatures

Abstract

Natural nests of egg-laying birds and reptiles exhibit substantial thermal variation, at a range of spatial and temporal scales. Rates and trajectories of embryonic development are highly sensitive to temperature, favouring an ability of embryos to respond adaptively (i.e. match their developmental biology to local thermal regimes). Spatially, thermal variation can be significant within a single nest (top to bottom), among adjacent nests (as a function of shading, nest depth etc.), across populations that inhabit areas with different weather conditions, and across species that differ in climates occupied and/or nest characteristics. Thermal regimes also vary temporally, in ways that generate differences among nests within a single population (e.g. due to seasonal timing of laying), among populations and across species. Anthropogenic activities (e.g. habitat clearing, climate change) add to this spatial and temporal diversity in thermal regimes. We review published literature on embryonic adaptations to spatio-temporal heterogeneity in nest temperatures. Although relatively few taxa have been studied in detail, and proximate mechanisms remain unclear, our review identifies many cases in which natural selection appears to have fine-tuned embryogenesis to match local thermal regimes. Developmental rates have been reported to differ between uppermost versus lower eggs within a single nest, between eggs laid early versus late in the season, and between populations from cooler versus warmer climates. We identify gaps in our understanding of thermal adaptations of early (embryonic) phases of the life history, and suggest fruitful opportunities for future research.

Heat tolerance of reptile embryos: Current knowledge, methodological considerations, and future directions

“…This is best exemplified by the extreme difference in ECHT between the desert iguana ( Dipsosaurus dorsalis ) and the tuatara ( Sphenodon punctatus ; ~15°C), which represent the highest (40.2°C) and lowest (24.6°C) estimates of ECHT, respectively. Differences in ECHT could be due to lineage‐specific thermal adaptation (Andrews & Schwarzkopf, 2012; Du et al, 2019). Indeed, nest temperatures of D. dorsalis often exceed 40°C (Muth, 1980) while those of S. punctatus are between 16°C and 20°C in mean temperature (Thompson, Packard, Packard, & Rose, 1996).…”

“…Warming temperatures due to global change threaten biodiversity across the planet. Eggs of non‐avian, reptiles (henceforth “reptiles”) are particularly vulnerable to heat stress due to a lack of parental care during incubation and limited ability to behaviorally thermoregulate (Cordero, Telemeco, & Gangloff, 2018; Telemeco, Elphick, & Shine, 2009; Telemeco et al, 2016; but see Du, Shine, Ma, & Sun, 2019; Li, Zhao, Zhou, Hu, & Du, 2014; Shine & Du, 2018; Teng et al, 2014). Consequently, the biotic impacts of global change have motivated a surge in research devoted to understanding the effects of warming nest temperatures on reptile development.…”

The thermal ecology and physiology of reptiles and amphibians: A user's guide

“…Along the way, we highlight a selection of articles that elegantly demonstrate the utility of using these animals as model organisms in thermal studies; these studies are featured in two inset “boxes.” Our goal is not to provide an exhaustive list of studies on the thermal ecology and physiology of reptiles and amphibians, of which there are thousands. There are many notable reviews of the thermal biology of amphibians (Brattstrom, 1963, 1979; Hutchison & Dupre, 1992) and reptiles (Andrews & Schwarzkopf, 2012; Avery, 1982; Brattstrom, 1965; Du, Shine, Ma, & Sun, 2019; Huey, 1982; Noble, Stenhouse, & Schwanz, 2018; Refsnider, Clifton, & Vazquez, 2019; While et al, 2018). Rather, we summarize the optimal methodologies and highlight important advances in theory and technology that will form the basis of decades of further research on the thermal physiology of reptiles and amphibians, especially as they relate to projecting the impacts of climate change on these diverse classes of organisms.…”

Temperature‐Dependent Sex Determination in Sea Turtles in the Context of Climate Change: Uncovering the Adaptive Significance

“…[54] Thermal limits are correlated to latitude in reptiles, suggesting that populations adapt to the local thermal conditions that they experience by adjusting their thermal tolerances. [55] Thermal tolerance in sea turtles varies among populations and species. Different species lay clutches at distinct depths where thermal conditions differ.…”

“…The existing variability in thermal tolerance within a nesting population, suggests that given enough time, populations would be able to adapt, if the hatchlings produced at high temperatures reproduced and transmitted this thermal tolerance to their descendants. There is currently a gap in knowledge on the genetic basis of embryo adaptation to thermal regimes in reptiles, [ 55 ] but recent work has identified some genes involved in the thermal tolerance of embryonic loggerhead turtles. [ 60 ] This opens new research avenues, which will likely be critical to understand how sea turtles, and reptiles in general, respond and adapt to changing climates.…”