Synchronized Metabolic and Microbial Changes in Light-vented Bulbul during Recent Northward Range Expansion

Abstract

Abstract Background Endotherms recently expanding to cold environments generally exhibit strong physiological acclimation to sustain high body temperature. During this process, gut microbes likely play a considerable role in host physiological functions, including digestion and thermogenesis. Light-vented bulbul (Pycnonotus sinensis) represents one of such a species. It used to be restricted to the Oriental realm, and expanded its range to the Palearctic during the past few decades. Results We explored the seasonal dynamics of the resting metabolic rate (RMR) and gut microbiota for local and newly colonized populations of light-vented bulbul. Our results showed that light-vented bulbul exhibited physiological changes during northern expansion. Specifically, the RMR was positively correlated with latitude in the winter (p = 0.0011, r = 0.33). Body mass showed a significant positive correlation with latitude in the breeding (p = 0.045, r = 0.27) and wintering seasons (p = 0.012, r = 0.25), corresponding to Bergmann’s rule. Consistently, the gut microbiota showed corresponding variation to the northern cold environments. In the two northern populations, the alpha diversity decreased compared with those of two southern populations. Significant differences were detected in dominant phyla, such as Firmicutes, Bacteroidetes, Proteobacteria and Desulfobacterota in the breeding and wintering seasons (p < 0.05). The core microbiota showed geographic differences in the winter, including the elevated relative abundance of 5 species (Alistipes shahii, Bacteroides stercoris, Bacteroides vulgatus, Parabacteroides merdae and Bacteroides spp.) in northern populations. Finally, to explore the link between microbial communities and host metabolic thermogenesis, we conducted a correlation analysis between microbiota and RMR. We found that more genera were significantly correlated with RMR in the wintering season than that in the breeding season (71 versus 23). Conclusions This study suggested that key microbiota linked with thermogenesis to push lighted-vented bulbul on a path toward the north.