Specialized digestive adaptations within the hindgut of a colobine monkey

Rui Liu, Katherine Amato, Rong Hou, Andres Gomez, Derek W. Dunn, Jun Zhang, Paul A. Garber, Colin A. Chapman, Nicoletta Righini, Gang He, Gu Fang, Yuhang Li, Baoguo Li, Songtao Guo

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Abstract

In mammal herbivores, fiber digestion usually occurs predominantly in either the foregut or the hindgut. Reports of mechanisms showing synergistic function in both gut regions for the digestion of fiber and other nutrients in wild mammals are rare because it requires integrative study of anatomy, physiology, and gut microbiome. Colobine monkeys (Colobinae) are folivorous, with high-fiber foods fermented primarily in their foreguts. A few colobine species live in temperate regions, so obtaining energy from fiber during the winter is essential. However, the mechanisms enabling this remain largely unknown. We hypothesized that such species possess specialized mechanisms to enhance fiber digestion in the hindgut and studied microbial and morphological digestive adaptations of golden snub-nosed monkeys (GSMs), Rhinopithecus roxellana. which is a temperate forest colobine from central China that experiences high-thermal-energy demands while restricted to a fibrous, low-energy winter diet. We tested for synergistic foregut and hindgut fiber digestion using comparisons of morphology, microbiome composition and function, and digestive efficiency. We found that the GSM colon has a significantly greater volume than that of other foregut-fermenting colobines. The microbiomes of the foregut and hindgut differed significantly in composition and abundance. However, while digestive efficiency and the expression of microbial gene functions for fiber digestion were higher in the foregut than in the hindgut, both gut regions were dominated by microbial taxa producing enzymes to enable active digestion of complex carbohydrates. Our data suggest that both the GSM foregut and hindgut facilitate fiber digestion and that an enlarged colon is likely an adaptation to accommodate high throughput of fiber-rich food during winter.

Original languageEnglish (US)
Article number100207
JournalThe Innovation
Volume3
Issue number2
DOIs
StatePublished - Mar 29 2022

Bibliographical note

Funding Information:
We thank Professors Fuwen Wei and Rebecca Stumpf for constructive comments on previous versions of this paper, Professors Quanwei Zhongyang and Lifeng Zhu for their help in data analysis of 16S rRNA, and Professor Fu Dongjing for drawing the sketch of GI tract anatomy. P.A.G. wishes to thank Chrissie, Sara, Jenni, and Dax for their support. This work was supported by National Natural Science Foundation of China ( 31730104 , 31872247 , 31870396 , 32000297 , 32070450 , and 32070453 ); Strategic Priority Research Program of the Chinese Academy of Sciences ( XDB31020302 ); key program of Forestry Science Research of Shaanxi ( SHLY-2018-07 ); and Natural Science Foundation of Shaanxi Province in China, 2018JC-022 , 2016JZ009 . D.W.D. is supported by a Talents 1000 Fellowship of Shaanxi Province .

Publisher Copyright:
© 2022 The Author(s)

Keywords

  • comparative morphology
  • fiber-protein digestion
  • golden snub-nosed monkeys
  • gut microbiota
  • nutrition

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