Reciprocal translocation experiments reveal gut microbiome plasticity and host specificity in a Qinghai-Xizang Plateau lizard

Animal adaptation to environmental challenges is a complex process involving intricate interactions between the host genotype and gut microbiome composition. The gut microbiome, highly responsive to external environmental factors, plays a crucial role in host adaptability and may facilitate local adaptation within species. Concurrently, the genetic background of host populations influences gut microbiome composition, highlighting the bidirectional relationship between host and microbiome. Despite this, our understanding of gut microbiome plasticity and its role in host adaptability remains limited, particularly in reptiles. To clarify this issue, we conducted a reciprocal translocation experiment with gravid females of the Qinghai toad-headed lizards (Phrynocephalus vlangalii) between high-altitude (2 600 m a.s.l.) and superhigh-altitude (3 600 m a.s.l.) environments on Dangjin Mountain of the Qinghai-Xizang Plateau, China. One year later, we assessed the phenotypes and gut microbiomes of their offspring. Results revealed significant plasticity in gut microbiome diversity and structure in response to contrasting elevations. High-altitude conditions increased diversity, and maternal effects appeared to enable high-altitude lizards to maintain elevated diversity when exposed to superhigh-altitude environments. Additionally, superhigh-altitude lizards displayed distinct gut microbiome structures with notable host specificity, potentially linked to their lower growth rates. Overall, these findings underscore the importance of the gut microbiome in facilitating reptilian adaptation to rapid environmental changes across altitudinal gradients. Furthermore, this study provides critical insights into microbial mechanisms underpinning local adaptation and adaptative plasticity, offering a foundation for future research on host-microbiome interactions in evolutionary and ecological contexts.