Latitudinal embryonic thermal tolerance and plasticity shape the vulnerability of oviparous species to climate change

Abstract

Heat tolerance at the immobile embryonic stage is expected to be critical in determining species vulnerability to climate change. However, how the mean and developmental plasticity of embryonic heat tolerance vary geographically, and how these geographic variations affect species' vulnerability under climate change remain unknown. We experimentally determined the mean and developmental plasticity of embryonic acute heat tolerance (EAHT, i.e., heat shock temperature at which embryonic heartbeats ceased) for three latitudinally distributed populations of an oviparous lacertid lizard. The experimental results suggested that the mean EAHT decreased with decreasing latitude and that the reaction norms of EAHT in relation to developmental temperatures showed “flat,” “bell‐shaped,” and “decreasing” patterns at high, medium, and low latitudes, respectively. Based on the means and plasticity of EAHT and weather data across China, we project that the heat stress frequency would increase from the present to the future and increase toward low latitudes. Furthermore, heat stress becomes more extensive with the incorporation of developmental plasticity. Incorporating the mean EAHT during the embryonic development season, heat stress frequency, and climate variables in a species distribution model projects that suitable habitats could move northward in response to ongoing climate change and shrink due to the loss of southern habitat. Moreover, even lizards within the areas that are predicted to remain highly suitable are expected to experience increases in heat stress over time, particularly at medium and low latitudes. Our study reveals geographic variation in the mean and developmental plasticity of EAHT and highlights its importance for predicting species vulnerability and range shifts in response to climate change.

Moderate climate warming scenarios during embryonic and post‐embryonic stages benefit a cold‐climate lizard

“…In addition to the warming environment, the embryos and hatchlings in the mesocosm are naturally exposed to extreme climatic conditions including heat events and torrential rainfall in summer, and cold snaps in deep fall and winter. These extreme climatic conditions can result in direct mortality (Hall & Sun, 2021; Sun et al., 2021), or indirectly depress survival by imposing physiological stress, weakening immunocompetence and resistance to parasites (e.g. Scharsack et al., 2021; Sun, Wang, et al., 2018; Wang et al., 2016; Zhang et al., 2018).…”

Higher metabolic plasticity in temperate compared to tropical lizards suggests increased resilience to climate change

“…Their habitat covers a latitudinal range ~1175 km, from the high‐latitudinal species ( T. wolteri ) to the low‐latitudinal species ( T. sexlineatus ). The natural habitats for these three species are similar, with mixtures of shrub and grasslands (Sun, Ma, et al, 2021; Zhao et al, 1999). The yearly average ambient temperatures of the sample sites decreased and the yearly thermal fluctuation increased as latitude increased (Figure 1a).…”

The behavioural and physiological ecology of embryos: responding to the challenges of life inside an egg

“…Previous studies have integrated a number of physiological parameters such as body temperature, thermal tolerance, and metabolic rate to construct mechanistic SDMs based on energetic and biophysical principles (e.g. foraging energetic models or biophysical threshold models) for predicting the impact of climate warming and identifying the species most vulnerable to climate warming (Buckley, Nufio & Kingsolver, 2014;Sunday et al, 2014). However, most studies are only concerned with how organisms respond to climate change during the adult stages of the life cycle (Levy et al, 2015), despite the fact that the embryonic stage is highly sensitive to environmental conditions (Du & Shine, 2015).…”

“…However, most studies are only concerned with how organisms respond to climate change during the adult stages of the life cycle (Levy et al ., 2015), despite the fact that the embryonic stage is highly sensitive to environmental conditions (Du & Shine, 2015). Therefore, integrating developmental traits of embryos and ecological modelling provides a promising way to predict a species' vulnerability to environmental change, and inputting the biological information of all life‐history stages into SDMs will enhance the accuracy of these models for predicting the future distribution of organisms (Radchuk, Turlure & Schtickzelle, 2013; Levy et al ., 2015; Carlo et al ., 2018; Sun et al ., 2021). More broadly, the phenotypic plasticity of offspring phenotypes induced by embryo–environment interactions needs to be integrated with community ecology, to enhance our ability to predict community responses to global environmental change (Warne, Baer & Boyles, 2019).…”