The divergent effects of moderate climate warming on the gut microbiota and energetic state of cold-climate lizards from open and semi-closed microhabitats

Abstract

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.

Microbial communities are thermally more sensitive in warm-climate lizards compared with their cold-climate counterparts

“…The relative abundances of putative pathogens did not differ significantly among three temperature treatments in L. reevesii , but were enriched in P. przewalskii acclimated to 20°C. The accelerated colonization of pathogenic bacteria in the gut at low temperatures has been observed in other cold-climate vertebrates ( Liu et al, 2022 ; Tong et al, 2023 ). Bacteria of the genus Akkermansia can enhance metabolic homeostasis and anti-inflammatory properties ( Everard et al, 2013 ; Shin et al, 2014 ).…”

Warming effects on lizard gut microbiome depend on habitat connectivity

“…This may result from an investment of the host in the maintenance of particular beneficial members of Firmicutes against heat stress at the expense of others [64]. As certain members of Firmicutes, in particular Ruminococcaceae, have been found promoted by high-fat diet in mice [65], this observation might also suggest an increase of metabolic rate and energetic needs of lizards in warm climates [66].…”

Responses of gut microbiota in crocodile lizards (Shinisaurus crocodilurus) to changes in temperature

“…As a critical environmental factor, temperature significantly influences animal growth, development, and reproduction ( Gillooly et al, 2002 ; Angilletta et al, 2010 ), with global warming posing a particular threat, especially to ambient-temperature reliant reptiles ( Root et al, 2003 ; Xu et al, 2017 ; Leung et al, 2020 ). Notably, in reptiles, temperature can exert substantial effects on various ecological and reproductive factors ( Meiri et al, 2013 ), including digestive performance ( Pafilis et al, 2007 ), offspring sex determination ( Janzen, 1994 ; Warner and Shine, 2008 ), metabolism ( Milsom et al, 2008 ), and athletic ability ( Liu et al, 2022 ). Recent research has also revealed that temperature changes can impact the composition and function of the gut microbiota ( Sepulveda and Moeller, 2020 ; Liu et al, 2022 ).…”

“…Notably, in reptiles, temperature can exert substantial effects on various ecological and reproductive factors ( Meiri et al, 2013 ), including digestive performance ( Pafilis et al, 2007 ), offspring sex determination ( Janzen, 1994 ; Warner and Shine, 2008 ), metabolism ( Milsom et al, 2008 ), and athletic ability ( Liu et al, 2022 ). Recent research has also revealed that temperature changes can impact the composition and function of the gut microbiota ( Sepulveda and Moeller, 2020 ; Liu et al, 2022 ). For example, temperature increases have been shown to reshape the gut microbiota in Eremias argus , leading to altered and destabilized composition in response to adaptive states ( Zhang Z. et al, 2022 ).…”