Warming temperatures caused by climate change are predicted to vary temporally and spatially. For mid‐ and high‐latitude reptiles, the seasonal variation in warming temperatures experienced by embryos and hatchlings may determine offspring fitness, yet this has remained largely unexplored. To evaluate the independent and interactive influence of seasonal variation in warming temperatures on embryonic and hatchling development, we incubated eggs and reared hatchlings of a cold‐climate oviparous ectothermic species, the Heilongjiang grass lizard (Takydromus amurensis), following a 2 × 2 factorial design (present climate versus warming climate for embryos × present climate versus warming climate for hatchlings). We then evaluated embryonic and hatchling development, including hatching success, incubation period, initial hatchling body size, hatchling metabolic rate, growth rate and survival in the mesocosms. We found that warming temperatures shortened the incubation period and produced hatchlings with higher survival rates than those incubated under the present climate conditions. Similarly, hatchlings reared under a warming climate had similar growth rates and resting metabolic rates, but higher survival rates than those reared under the present climate. Hatchlings that experienced both warming incubation and warming growth conditions had the highest survival rates. This study revealed that moderate warming temperatures (Representative Concentration Pathway, RCP 4.5, 1.1–2.6°C) experienced by embryos and hatchlings interact to benefit hatchling fitness in cold‐climate oviparous ectotherms. Our study also highlighted the importance of integrating seasonal variation in warming temperatures when evaluating the responses to climate warming in multiple developmental stages in oviparous ectotherms.

IntroductionUnderstanding the physiological responses to warming temperatures is critical for evaluating the vulnerabilities of animals to climate warming. The physiological responses are increasingly affected by gut microbiota. However, the interactions between physiological responses and the gut microbiota of sympatric animals from various microhabitats in the face of climate change remain largely unknown.MethodsTo evaluate the effects of warming temperatures on animals from different microhabitats, we compared locomotor performance, metabolic rate, growth, survival, and gut microbiota of two sympatric ectothermic species (Eremias argus and Takydromus amurensis) from open and semi-closed microhabitats under present and moderate warming climate conditions, respectively.Results and discussionWe found that locomotor performance and growth rates of snout-vent length (SVL) were enhanced in both lizard species by warming climate. Interestingly, warming temperatures enhanced resting metabolic rates (RMR) in the open-habitat lizard, E. argus, but depressed them in the semi-closed habitat lizard, T. amurensis. Reversely, the metabolism-related gut microbiota was not affected by warming in E. argus, whereas it was significantly enhanced by warming in T. amurensis, indicating a plausible compensatory effect of the gut microbiota on the metabolic regulation of T. amurensis. Furthermore, warming likely improved immunity in both lizard species by significantly reducing pathogenic bacteria while increasing probiotics. This study found that high-latitude sympatric lizards from both open and semi-closed habitats were beneficial to warming temperatures by physiological modification and regulation of the gut microbiota and highlighted the importance of integrating the physiology and gut microbiota in evaluating the vulnerability of animals to climate warming.

The effects of warming temperatures on embryonic and hatchling development are critical for determining the vulnerability of species to climate warming. However, these effects have rarely been investigated in high-latitude oviparous species, particularly in their low-latitude margin populations. This study investigated the embryonic and hatchling development and fitness-related traits of a low-latitude margin population of a high-latitude lizard (Lacerta agilis). These traits were examined under present (24°C), moderate warming (27 and 30°C), and severe warming scenarios (33°C). Based on embryonic and hatchling responses to thermal variation, this study aimed to predict the vulnerability of the early life stages of low-latitude margin population of Lacerta agilis to climate warming. The incubation period of the low-latitude margin population of Lacerta agilis decreased as the temperature increased from 24 to 33°C. Hatching success was similar at 24, 27, and 30°C but decreased significantly at 33°C. No differences with temperature were observed for hatchling snout-vent length and hatchling body mass. The sprint speed was higher for hatchlings from temperatures of 24 and 33°C. The growth rate of hatchlings was highest at 30°C; however, the survival rate of hatchlings was not affected by the thermal environment. This study demonstrated that even for a low-latitude margin population of the high-latitude lizard, Lacerta agilis, moderate warming (i.e., 27 and 30°C) would benefit embryonic and hatchling development. This was indicated by the results showing higher hatching success, growth rate, and survival rate. However, if temperatures increase above 33°C, development and survival would be depressed significantly. Thus, low-latitude margin population of high-latitude species Lacerta agilis would benefit from climate warming in the near future but would be under stress if the nest temperature exceeded 30°C.