Metabolic and microbial changes in light-vented bulbul during recent northward range expansion

Abstract

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. The light-vented bulbul Pycnonotus sinensis represents one such species. It used to be restricted to the Oriental realm but expanded its distribution range north to the Palearctic areas during the past few decades. Here, we explored the seasonal dynamics of the resting metabolic rate (RMR) and microbiota for local and newly colonized populations of the species. Our results showed that the mass-adjusted RMR and body mass were positively correlated with latitude variations in both seasons. Consistently, the gut microbiota showed a corresponding variation to the northern cold environments. In the two northern populations, the alpha diversity decreased compared with those of the two southern populations. Significant differences were detected in dominant phyla, such as Firmicutes, Bacteroidetes, Proteobacteria, and Desulfobacterota in both seasons. The core microbiota showed geographic differences in the winter, including the elevated relative abundance of 5 species in northern populations. Finally, to explore the link between microbial communities and host metabolic thermogenesis, we conducted a correlation analysis between microbiota and mass-adjusted RMR. We found that more genera were significantly correlated with mass-adjusted RMR in the wintering season compared to the breeding season (71 vs. 23). These results suggest that microbiota of the lighted-vented bulbul linked with thermogenesis in diversity and abundance under northward expansion.

Keywords: RMR; bird; body mass; gut microbiota; season.

Figure 1.

Map of study sites (Downloaded from Standard Map Service System http://bzdt.ch.mnr.gov.cn/).

Figure 2.

Changes of mass-adjusted RMR and body mass in different latitudes in light-vented bulbul. (A) Pearson correlation analysis between latitude and mass-adjusted RMR (A) as well as body mass (B) during the breeding and wintering seasons. Seasonal differences of mass-adjusted RMR (C) and body mass (D) in the same geographic population using the t test. (* represents P < 0.05, ** represents P < 0.01).

Figure 3.

The gut microbiome diversity of light-vented bulbul in the breeding season. (A) Alpha diversity (ASVs and Shannon index) of bacterial communities in four groups using the Kruskal–Wallis test. (B) PCoA plot based on Bray-Curtis distance metrics depicting the differences in microbial community structure of four groups. (C) Relative abundances of bacterial phyla among groups (Kruskal–Wallis test). (D) The core microbiomes present in > 50% of individuals of light-vented bulbul in the breeding season. The relative abundance differences of genera between southern (GL and NC) and northern populations (DH and BJ) use the Wilcoxon test (* represents FDR < 0.05).

Figure 4.

The gut microbiome diversity of light-vented bulbul in the wintering season. (A) Alpha diversity (ASVs and Shannon index) of bacterial communities in four groups using the Kruskal–Wallis test. (B) PCoA plot based on Bray-Curtis distance metrics depicting the differences in microbial community structure of four groups. (C) Relative abundances of bacterial phyla among groups (Kruskal–Wallis test). (D) The core microbiomes present in >50% of individuals of light-vented bulbul in wintering season. The relative abundance differences of genera between southern (GL and NC) and northern populations (DH and BJ) use the Wilcoxon test (* represents FDR < 0.05).

Figure 5.

The compositions of the genera level were significantly correlated with mass-adjusted RMR of light-vented bulbul in the breeding season (A) and wintering season (B). Color gradient and circle size denote Pearson’s correlation coefficients. The color of the line represents the significance of the difference. The size of the line represents Pearson’s correlation coefficients.

Figure 6.

Different microbiota in the breeding and wintering seasons of light-vented bulbul. (A) Venn diagram of common and specific amplicon sequence variants (ASVs). (B) PCoA plots based on Bray-Curtis distance metrics depict the differences in microbial community structure between two groups.