High-Altitude Drives the Convergent Evolution of Alpha Diversity and Indicator Microbiota in the Gut Microbiomes of Ungulates

Abstract

Convergent evolution is an important sector of evolutionary biology. High-altitude environments are one of the extreme environments for animals, especially in the Qinghai Tibet Plateau, driving the inquiry of whether, under broader phylogeny, high-altitude factors drive the convergent evolution of Artiodactyla and Perissodactyla gut microbiomes. Therefore, we profiled the gut microbiome of Artiodactyla and Perissodactyla at high and low altitudes using 16S rRNA gene sequencing. According to cluster analyses, the gut microbiome compositions of high-altitude Artiodactyla and Perissodactyla were not grouped together and were far from those of low-altitude Artiodactyla and Perissodactyla. The Wilcoxon’s test in high-altitude ungulates showed significantly higher Sobs and Shannon indices than in low-altitude ungulates. At the phylum level, Firmicutes and Patescibacteria were significantly enriched in the gut microbiomes of high-altitude ungulates, which also displayed a higher Firmicutes/Bacteroidetes value than low-altitude ungulates. At the family level, Ruminococcaceae, Christensenellaceae, and Saccharimonadaceae were significantly enriched in the gut microbiomes of high-altitude ungulates. Our results also indicated that the OH and FH groups shared two significantly enriched genera, Christensenellaceae_R_7_group and Candidatus_Saccharimonas. These findings indicated that a high altitude cannot surpass the order level to drive the convergent evolution of ungulate gut microbiome composition but can drive the convergent evolution of alpha diversity and indicator microbiota in the gut microbiome of ungulates. Overall, this study provides a novel perspective for understanding the adaptation of ungulates to high-altitude environments.

Convergent evolution of the gut microbiome in marine carnivores

“…We analyzed the gut microbiomes of 108 samples representing 16 species belonging to nine families and 14 genera to explore the convergent evolution of the gut microbiome. 16S rRNA gene data of the gut microbiome of the nine species ( Cuon alpinus [Wu et al, 2016 ], Canis lupus [Wu et al, 2017 ], Vulpes Vulpes [Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ], V. Corsac [Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ], Cervus elaphus [Wang et al, 2019 ], Ovis musimon [Sun et al, 2019 ], Pantholops hodgsonii [Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ], Pseudois nayaur [Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ], and Bos grunniens [Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ]) were obtained by sequencing in our laboratory. Other 16S rRNA gene data ( C. Nippon [Guan et al, 2017 ], Moschus chrysogaster [Sun et al, 2020 ], Halichoerus grypus [Watkins et al, 2022 ], Nyctereutes procyonoides [Ishida‐Kuroki et al, 2020 ], Enhydra lutris nereis [Dudek et al, 2022 ], Balaenoptera physalus , and Physeter microcephalus [Glaeser et al, 2022 ]) were downloaded from the NCBI SRA database ( www.ncbi.nlm.nih.gov ).…”

“…The gut microbiome is an important factor for host adaptations to the environment (Wang et al, 2019 ; Wang, Shang, Wei, et al, 2022 ; Wang, Shang, Wu, et al, 2022 ; Wang, Wu, et al, 2022 ). Wang, Shang, Wu, et al ( 2022 ) found that the gut microbiome function of red and corsac foxes can help hosts adapt to different environmental niches.…”

High-altitude-induced alterations in intestinal microbiota

“…For instance, at an altitude of 4,331 m, the relative abundance of Firmicutes and Bacteroidetes in pikas’ intestines significantly differs from that at 3,694 m and 3,856 m ( Obregon-Tito et al, 2015 ). Studies on wild ungulates at high altitudes (Yaks, Tibetan wild donkeys, Tibetan antelopes, and Bighorn sheep) also reveal that Firmicutes/Bacteroidetes ratios are higher than those in low-altitude ungulates, with Firmicutes and Proteobacteria being the most enriched phyla in the intestinal microbiota of high-altitude ungulates ( Table 1 ; Guo et al, 2014 ; Du et al, 2022 ; Wang et al, 2022 ). In particular, the Firmicutes/Bacteroidetes ratio (F/B ratio) in the intestinal microbiota of high-altitude mammals such as Plateau pikas, Tibetan macaques, Tibetan antelopes, Mouflons, and Blue sheep exceeds that of low-altitude mammals.…”

“…In recent years, there has been increasing recognition of the significant impact of environmental factors on the intestinal microbiota ( Ma et al, 2019 ; Wang et al, 2022 ). Specifically, research has highlighted the role of the high-altitude hypoxic environment in shaping the composition and structure of the intestinal microbial community ( Bai et al, 2022 ; Wang et al, 2022 ). However, our understanding of the precise effects of extreme environments, such as high altitudes, on the intestinal microbiota remains incomplete.…”

Diet and high altitude strongly drive convergent adaptation of gut microbiota in wild macaques, humans, and dogs to high altitude environments

“…The high altitude rumen microbiota of yak and Tibetan sheep exhibited a convergent phenomenon, with significantly lower levels in production of methane and volatile fatty acids (VFAs) (Zhang et al, 2016). The high altitude environments drive the diversity of gut microbiota composition and convergent evolution of indicator microbiota in ungulates (Wang et al, 2022). Studies on a variety of ungulates living in high altitude environments, such as the Tibetan antelope (Pantholops hodgsoni) and Tibetan sheep, also found that they have a similar composition of gut microbiota (Ma et al, 2019).…”