Global warming has become a hot topic among people all over the world (Hansen et al., 1999; Comiso, 2006; Morice et al., 2021). According to statistics, the global temperature has shown a significant upward trend since the industrial revolution, and it increased at a rate of 0.2°C/10 years in the past 30 years (Hansen et al., 2006). With the further intensification of human activities, the global temperature has risen even faster in the past decade than in previous decades, experts predicted that the next century could be the most “rampant” century of global warming (Cox et al., 2000; Hansen et al., 2010; Betts et al., 2011; Wang et al., 2017). Climate change had a significant impact on ecosystems and organisms (Walther et al., 2002; Peñuelas et al., 2013; Antão et al., 2020), such as coral reefs, one of the most significant indicators of climate change, were currently experiencing large-scale bleaching, and it was estimated that more coral reefs in the world have died (Hughes et al., 2017). Persistent climate change not only increased the impact of abiotic stress on organisms (Erasmus et al., 2002), but also make some key species decline rapidly or even die out, resulting in rapid reduction of global species diversity and genetic diversity, there was no doubt that this trend would affect every living organisms on the earth in the future (Thomas et al., 2004).

Animals adjusted their physiological changes to meet the challenge of global warming, and energetics adaptation is one of the most important aspects (Parmesan, 2006; Pörtner and Farrell, 2008; Huey et al., 2012). In the process of coping with climate shocks, whether animals can reach a new balance in energetics is crucial to their survival, and whether they can effectively use energy is related to the predation risk caused by animals going out for food (Hanna and Acclimat, 2015; Kordas et al., 2022). Shortly, it was very important to research the energy adaptation strategies in mammals to cope with global warming. This can not only clarify the energy adaptation mechanism of biological response to climate change, but also help to judge the fate of animals in the future global warming (Pörtner, 2002). Nevertheless, our understanding and research on this problem were still in the initial stage, the research on some important and typical species is very important, with the gradual deepening of these studies, an effective way to solve this problem will eventually be provided. It has been found that warm domesticated animals had a phenomenon of reducing thermogenic capacity (Tan et al., 2016). Moreover, it was found that higher temperature exposure during lactation would hinder the growth of offspring and reduce the reproductive performance in females (Bao et al., 2020).

Liver is one of the important organs for animal heat production, liver energy metabolism often changes to adapt to the environmental variations. In previous studies, we also found that the liver mass and metabolic intensity of the tree shrew increased when it adapted to the cold temperature (Zhang et al., 2012). Brown adipose tissue (BAT) is also an energy metabolism organ of animals (Cannon and Nedergaard, 2004). BAT mainly exists in scapular space of animals (Nedergaard et al., 2007), because of the large amount of uncoupling protein 1 (UCP1) contained in the mitochondrial inner membrane, it plays a role of uncoupling in the transmission of respiratory chain, therefore, thermogenic capacity of BAT is very important for animals to adapt to complex climate change (Kozak and Harper, 2000). For example, the tree shrew increased its BAT mass and UCP1 content when adapting to the cold environment (Zhang et al., 2012). Metabolic rate is the most direct evidence of animal energy expenditure, resting metabolic rate (RMR) is an important indicator of energy consumption, and it is an important indicator to evaluate the ability of animals to adapt to the environment. Finally, body temperature is very important for energy regulation and it also a core physiological indicator in animal energetics (Ayres, 2020). Analysis of animal temperature can also reflect the energy adaptation of animals from the perspective of heat dissipation. For example, body temperature of birds raised 0.22°C for every 1°C increase in ambient temperature (Nilsson et al., 2016). In brief, liver, BAT, RMR and body temperature together constitute the central issue in studying the energy adaptation strategies of animals to adapt to the environment. Furthermore, metabonomics is a new discipline following genomics, transcriptomics and proteomics. Because it can provide terminal information to reflect the changes of all metabolites and metabolic pathways in organisms, it has become an important research technology to explore the energy adaptation mechanism of organisms.

Tupaia belangeri belongs to Scandentia, Tupaiidae, Tupaia. It originally originated from Borneo and was a specific small mammal to the Oriental realm (Roberts et al., 2011), which is believed to be the closest relative of primates, therefore, it had a unique position in the research of evolution, and has been widely studied as a model for the early stage of primate evolution (Janecka et al., 2007; Fan et al., 2013). Moreover, T. belangeri had the characteristics of small size, easy feeding, short breeding cycle, lower maintenance cost and higher brain body mass ratio; it has been developed as an important medical model and widely used in a variety of human disease models (Cao et al., 2003). Such as tumor animal model (Yang et al., 2005), virus infection model (Feng et al., 2017), pulmonary fibrosis animal model (Che et al., 2021), and depression model, etc. (Fuchs, 2005). Furthermore, it was worth noting that T. belangeri is also a valuable model for studying brain function and neurodegenerative diseases, because it had a large ratio of brain to body mass, the results of brain slices showed that the degree of differentiation of its brain structure is consistent with that of primates (Wong and Kaas, 2009; Römer et al., 2018). In the general trend that the use of primates is limited increasingly, T. belangeri showed great development prospects and had been introduced by many laboratories. In general, in view of the key role of T. belangeri in evolutionary issues and various human disease models, it had become an extremely important animal resource. In the previously study, our research team found that the proportion of non shivering thermogenesis (NST) in the total heat production in T. belangeri decreased with the extension of cold acclimation time, while the proportion of RMR increased, indicating that the liver metabolism played a very important role in the process of spreading from south to north (Zhang et al., 2012). In order to clarify the energetics strategies in T. belangeri to adapt to warmer temperature, the present study captured 10 and 11 T. belangeri in two regions with different annual average temperatures respectively, Pianma (PM, annual average temperature is 15.01°C, low temperature region) and Tengchong (TC, annual average temperature is 20.32°C, warm temperature region). We first analyzed the liver metabonomics from the two regions, and screened the energy related differentially expressed metabolites to analyze the differences in energy metabolism pathways. Secondly, we further studied the energy related indicators of the two regions, such as RMR, body temperature, UCP1, etc. Finally, we clarify the energy adaptation strategies in T. belangeri to warmer temperature under the climate pattern of global warming. The research results not only involve the understanding of the internal mechanism of animal adaptation to warmer temperature, but also can preliminarily speculate the possible fate of this important species in the future climate change.

Liver and BAT are two important energy producing organs, and their energy producing status is of great significance for animals to adapt to the environment. For example, Cricetulus barabensis can respond to the impact of the high temperature environment by down regulating the metabolic ability from liver and BAT (Tan et al., 2016). Combined liver and BAT weights, as well as RMR and UCP1 content between the two regions, it showed that T. belangeri adapted to the warmer temperature environment by reducing metabolic intensity and energy consumption. In the warm temperature environment, heat dissipation is more important, the liver does not need to produce more energy, so the liver mass and RMR decreased. Reduction of BAT mass and UCP1 content can reduce the energy producing capacity of BAT, thereby weakening its heat production capacity, which is beneficial for T. belangeri to adapt to warm temperature environment. Decrease of thermogenic capacity in two important organs lead to the decrease of animal metabolic rate (Zhou et al., 2015; Luo et al., 2017). This is a very smart and economical energy adaptation strategy, which not only reduced the heat dissipation pressure under higher temperature, but also reduced energy consumption (Ravussin et al., 2012). Therefore, the metabolic intensity of the liver and BAT would decrease accordingly to adapt to global warming (Padfield et al., 2016; Tan et al., 2016). On the other hand, lower energy consumption means that animals can survive with less basic energy expenditure, which means that animals can survive only by spending less time foraging than before, which not only avoids the increased risk of predation, but also helpful for animals to survive the period of food shortage (Mónus and Barta, 2016; Shiratsuru et al., 2021). In general, T. belangeri adapted to the warm temperature environment by reducing energy consumption. This energy adaptation strategy to deal with climate change is efficient and is a model of physiological adaptation. It can be predicted that the energy adaptation strategy in T. belangeri is conducive to cope with the climate impact of global warming in the future.

Energy metabolites were intermediates in the energy metabolism pathway. Through the analysis of the concentration of intermediates, we can speculate the intensity of the energy metabolism pathway, so as to understand the energy strategy of animals to adapt to the environment. It found that its metabolism reduced through metabonomic analysis of coccinella cyst in cold and dark conditions, and Changchun snail adapted to higher temperature environment through metabolic inhibition (Guo et al., 2021). In our study, we found that the metabolic intensity of the two most important energy metabolism pathways (glycolysis and TCA cycle) of T. belangeri in warm temperature areas decreased, indicating that the basic heat production of the liver in warm temperature environment decreased. The results of metabolome study were consistent with those of liver mass and RMR.

Body temperature is a core physiological indicator of animal energetics (Ayres, 2020). Animals can adapt to environmental changes by changing their body temperature. For example, rats adapt to cold and high-altitude environment through body temperature decreasing (Cadena and Tattersall, 2014), birds coped with the impact of high temperature environment by raising their body temperature (Nilsson et al., 2016). Our research shows that T. belangeri raised body temperature in TC, suggesting that T. belangeri responded to warmer temperature by increasing body temperature, raising body temperature is another effective energetics strategy for adapting to high temperatures (Nilsson et al., 2016), because reasonable increase of body temperature can increase the temperature difference between animals and the external environment, which is conducive to heat dissipation (Vejmělka et al., 2021). But the interesting thing about this conclusion is that maintaining a high body temperature requires more energy, which seems to contradict the above results on reducing energy consumption (Vejmělka et al., 2021). Why is there a waste of energy while saving energy consumption? Because reducing energy consumption is the real and more economical way to adapt to warmer temperature. Why does T. belangeri use this “waste” energy instead of more economical way to achieve its goal? We speculated that this may be related to the fact that T. belangeri were still in the evolutionary process of adapting to warmer temperature. When T. belangeri faced the impact of high temperature, they cannot immediately reduce the metabolic rate to the level of extremely low energy consumption in a short period of time. At this time, it is an efficient energy treatment method to dissipate the excessive energy generated by raising body temperature (Bennett and Lenski, 2007). Although T. belangeri wasted some energy, it can at least survive under the impact of warmer temperature. In the later stage of continuous adaptation to the high-temperature environment, by continuously reducing the metabolic intensity of the production organs, T. belangeri may eventually no longer be necessary to heat up in the “expensive” way of raising body temperature, so as to reduce body temperature and achieve the most perfect use of energy in the high-temperature adaptation strategy (Kordas et al., 2022). In general, high temperature stimulated repeatedly the physiological reaction of T. belangeri to dissipate heat, so as to improve the heat resistance by gradually reducing the physiological pressure, which represented a state in which the ability to improve body temperature. Therefore, thermal adaptation is a process (Somero, 2010; Hoffmann and Sgrò, 2011). Furthermore, how animals mediate high body temperature under obesity is another unresolved issue, because the thermoregulatory center of animals is in the hypothalamus, we speculated that the activity of hypothalamus neurons in TC may have changed. Of course, this needs further study.

In conclusion, we found that T. belangeri adapt to the warm temperature environment by reducing energy consumption, including reducing RMR and differential metabolites, and increasing body temperature, so as to maintain their survival. Moreover, we speculated that T. belangeri may continue to spread northwards under the impact of future global warming.