REVIEWS

Advances and prospects of the gut microbiome in non-human primate

  • Qiuyan GUO ,
  • Xiao WEI ,
  • Meijing LU ,
  • Penglai FAN ,
  • Qihai ZHOU
Expand
  • 1.Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection, Monistry of Education, Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin 541006, China
    2.Terrestrial Wildlife Rescue and Epidemic Diseases Surveillance Center of Guangxi, Nanning 530000, China

Received date: 2022-03-20

  Accepted date: 2022-07-05

  Online published: 2023-01-10

Abstract

The gut microbiome is the second set of animal genomes and interacts with hosts in development, nutrition metabolism, physiological function, and immunity. Non-human primates (NHPs) are close to humans in terms of ecological niche, social structure, geographical distribution and evolution. The research of NHPs gut microbiome not only contributes to understanding primate ecology, conservation, and evolution but has also important reference value for in-depth understanding of the role of the gut microbiome in human evolution. This paper summarizes the factors influencing the composition of the gut microbiome in NHPs, including host species and phylogeny, diet, habitat fragmentation, age/sex, captivity, and community life. We also explore the application of gut microbiome research in NHPs ecology, behavior, conservation, and adaptive evolution. Future studies of the gut microbiome of NHPs will offer new insight into primate ecology and evolution as well as human health. They will also provide a new theoretical basis and means for primate conservation.

Cite this article

Qiuyan GUO , Xiao WEI , Meijing LU , Penglai FAN , Qihai ZHOU . Advances and prospects of the gut microbiome in non-human primate[J]. ACTA THERIOLOGICA SINICA, 2023 , 43(1) : 69 -81 . DOI: 10.16829/j.slxb.150669

References

null Adriansjach J, Baum S T, Lefkowitz E J, Van Der Pol W J, Buford T W, Colman R J. 2020. Age?related differences in the gut microbiome of Rhesus macaques. The Journals of Gerontology: Series A, 75 (7): 1293-1298.
null Aiello L C, Wells J C K. 2002. Energetics and the evolution of the genus Homo . Annual Review of Anthropology, 31 (1): 323-338.
null Altmann J, Samuels A. 1992. Costs of maternal care: Infant?carrying in baboons. Behavioral Ecology Sociobiology, 29 (6): 391-398.
null Amaral W Z, Lubach G R, Proctor A, Lyte M, Phillips G J, Coe C L. 2017. Social influences on Prevotella and the gut microbiome of young monkeys. Psychosomatic Medicine, 79 (8): 888-897.
null Amato K R, Belle S V, Fiore A D, Estrada A, Stumpf R, White B, Nelson K E, Knight R, Leigh S R. 2017. Patterns in gut microbiota similarity associated with degree of sociality among sex classes of a neotropical primate. Microbial Ecology, 74 (1): 250-258.
null Amato K R, Clayton J B, Hale V L. 2022. Colobine gut microbiota: new perspectives on the nutrition and health of a specialized subfamily of primates. In: Matsuda I, Grueter C C, Teichroeb J A eds. The Colobines: Nature History, Behavior and Ecological Diversity. Cambridge University Press, 78-93.
null Amato K R, Leigh S R, Kent A, Mackie R I, Yeoman C J, Stumpf R M, Wilson B A, Nelson K E, White B A, Garber P A. 2015. The gut microbiota appears to compensate for seasonal diet variation in the wild black howler monkey (Alouatta pigra). Microbial Ecology, 69 (2): 434-443.
null Amato K R, Leigh S R, Kent A, Mackie R I, Yeoman C J, Stumpf R M, Wilson B A, Nelson K E, White B A, Garber P A. 2014.The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild, black howler monkeys (Alouatta pigra). American Journal of Physical Anthropology, 155 (4): 652-664.
null Amato K R, Martinez?Mota R, Righini N, Raguet?Schofield M, Corcione F P, Marini E, Humphrey G, Gogul G, Gaffney J, Lovelace E, Williams L, Luong A, Dominguez?Bello M G, Stumpf R M, White B, Nelson K E, Knight R, Leigh S R. 2016. Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species. Oecologia, 180 (3): 717-733.
null Amato K R, Sanders J G, Song S J, Nute M, Metcalf J L, Thompson L R, Morton J T, Amir A, Mckenzie V J, Humphrey G, Gogul G, Gaffney J, Baden A L, Britton G A O, Cuozzo F P, Fiore A D, Dominy N J, Goldberg T L, Gomez A, Kowalewski M M, Lewis R J, Link A, Sauther M L, Tecot S, White B A, Nelson K E, Stumpf R M, Knight R, Leigh S R. 2019. Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. The ISME Journal, 13: 576-587.
null Amato K R, Yeoman C J, Kent A, Righini N, Carbonero F, Estrada A, Gaskins H R, Stumpf R M, Yildirim S, Torralba M, Gillis M, Wilson B A, Nelson K E, White B A, Leigh S R. 2013. Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal, 7 (7): 1344-1353.
null Antwis R E, Edwards K L, Unwin B, Walker S L, Shultz S. 2019. Rare gut microbiota associated with breeding success, hormone metabolites and ovarian cycle phase in the critically endangered eastern black rhino. Microbiome, 7 (1): 27.
null Baniel A, Amato K R, Beehner J C, Bergman T J, Mercer A, Perlman R F, Petrullo L, Reitsema L, Sams S, Lu A, Snyder?Mackler N. 2020. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas. Microbiome, 9 (1): 26.
null Baranga D, Chapman C A, Mucunguzi P, Reyna?Hurtabo R. 2013. Fragments and food: red?tailed monkey abundance in privately owned forest fragments of central Uganda. Primates in Fragments, 15: 213-225.
null Barbican H J, Li Y Y, Ramirez M, Klase Z, Lipende I, Mjungu D, Moeller A H, Wilson M L, Pusey A E, Lonsdorf E V, Bushman F D, Hahn B H. 2018. Destabilization of the gut microbiome marks the end?stage of simian immunodeficiency virus infection in wild Chimpanzees. American Journal of Primatology, 80 (1): e22515.
null Barelli C, Albanese D, Stumpf R M, Asangba A E, Donati C, Rovero F, Hauffe H C. 2020. The gut microbiota communities of wild arboreal and ground?feeding tropical primates are affected differently by habitat disturbance. mSystems, 5 (3): e00061-20.
null Barton W, Cronin O, Garcia?Perez I, Whiston R, Holmes E, Woods T, Molloy C B, Molloy M G, Shanahan F, Cotter P D, O’Sullivan O. 2020. The effects of sustained fitness improvement on the gut microbiome: a longitudinal, repeated measures case?study approach. Translation Sports Medicine, 4 (2): 174-192.
null Bauchop T, Martucci R W. 1968. Ruminant-like digestion of the langur monkey. Science, 161 (3842): 698-700.
null Becker F, Gavins F N E, Fontenot J, Fontenot J, Jordan P, Yun J Y, Scott R, Polk P R, Friday R E, Boktor M, Musso M, Romero E, Boudreaux S, Simmons J, Hasselschwert D L, Goetzmann J E, Vanchiere J, Cvek U, Trutschl M, Kilgore P, Alexander J S. 2019. Dynamic gut microbiome changes following regional intestinal lymphatic obstruction in primates. Pathophysiology, 26 (3-4): 253-261.
null Benavidez K M, Iruri?Tucker A, Steiniche T, Wasserman M D. 2019. Primate microbial endocrinology: an uncharted frontier. American Journal of Primatology, 81: e23053.
null Bennett G, Malone M, Sauther M L, Cuozzo F P, White B, Nelson K E, Stumpf R M, Knight R, Leigh S R, Amato K R . 2016. Host age, social group, and habitat type influence the gut microbiota of wild ring?tailed lemurs (Lemur catta).American Journal of Primatology, 78 (8): 883-892.
null Bj?rk J R, Dasari M, Grieneisen L, Archie E A. 2019. Primate microbiomes over time: longitudinal answers to standing questions in microbiome research. American Journal of Primatology, 81 (12): e22970.
null Bonaz B, Bazin T, Pellissier S. 2018. The vagus nerve at the interface of the microbiota-gut-brain axis. Frontiers in Neuroscience, 12: 49.
null Bronikowski A M, Cords M, Alberts S C, Altmann J, Brockman D K, Fedigan L M, Pusey A, Stoinski T, Strier K B, Morris W F. 2016. Female and male life tables for seven wild primate species. Scientific Data, 3 (1): 160006.
null Brooks A W, Kohl K D, Brucher R M, van Opstal E J, Bordenstein S R. 2016. Phylosymbiosis: relationships and functional effects of microbial commnunities across host evolutionary history. PLoS Biology, 14 (11): e2000225.
null Bublitz D C, Wright P C, Rasambainarivo F T, Arrigo?Nelson S J, Bodager J R, Gillespie T G. 2015. Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance. American Journal of Primatology, 77 (3): 330-337.
null Chen L M, Wang D M, Garmaeva S, Kurilshikov A, Vila V A, Gacesa R, Sinha T, Study L C, Segal E, Weersma R K, Wijmenga C, Zhernakova A, Fu J Y. 2021. The long?term genetic stability and individual specificity of the human gut microbiome. Cell, 184 (9): 2302-2315.
null Chi L D, Khan I, Lin Z B, Zhang J W, Lee M Y S, Leong W, Hsiao W L W, Zheng Y. 2020. Fructo-oligosaccharides from Morinda officinalis remodeled gut microbiota and alleviated depression features in a stress rat mode. Phytomedicine, 67: 153457.
null Clarke S F, Murphy E F, O’Sullivan O, Lucey A, Humphreys M, Hogan A, Hayes P, O’Reilly M, Jeffery I B, Wood?Martin R, Kerins D M, Quigley E M, Ross R P, O’Toole P W, Molloy M G, Falvey E C, Shanahan F, Cotter P. 2014. Exercise and associated dietary extremes impact on gut microbial diversity. Gut, 63 (12): 1913-1920.
null Clayton J B, Al?Ghalith G A, Long H T, Tuan B V, Cabana F, Huang H, Vangay P, Ward T, Minh V V, Tam N A, Dat N T, Travis D A, Murtaugh M P, Covert H, Glander K E, Nadler T, Toddes B, Sha J C M, Singer R, Knights D, Johnson T J. 2018a. Associations between nutrition, gut microbiome, and health in a novel nonhuman primate model. Scientific Reports, 8 (1): 11159.
null Clayton J B, Gomez A, Amato K, Knights D, Travis D A, Blekhman R, Knight R, Leigh S, Stumpf R, Wolf T, Glander K E, Cabana F, Johnson T J. 2018b. The gut microbiome of nonhuman primates: lessons in ecology and evolution. American Journal of Primatology, 80 (6): e22867.
null Clayton J B, Vangay P, Huang H, Ward T, Hillmann B M, Al?Ghalith G A, Travis D A, Long H T, Tuan B V, Minh V V, Cabana F, Nadler T, Toddes B, Murphy T, Glander K E, Johnson T J, Knights D. 2016. Captivity humanizes the primate microbiome. Proceedings of the National Academy of Sciences, 113 (37): 10376-10381.
null Corlett R T. 2016. Plant diversity in a changing world: status, trends, and conservation needs. Plant Divers, 38 (1): 10-16.
null Cui Z W, Holmes A J, Zhang W J, Hu D L, Shao Q, Wang Z L, Lu J Q, Raubenheimer D. 2022. Seasonal diet and microbiome shifts in wild rhesus macaques are better correlated at the level of nutrient components than food items. Integrative Zoology, 17: 1147-1161.
null Dantzer R. 1991. Stress, stereotypies and welfare. Behavioural Processes, 25 (2-3): 95-102.
null Lugano S D, Nyerere K A, Kariuki W K, Samuel K, Joseph K, Apondi O J. 2018. Gastrointestinal microbial flora in wild and captive olive baboons (Papio anubis). American Journal of Infectious Diseases and Microbiology, 6 (1): 30-37.
null Degnan P H, Pusey A E, Lonsdorf E V, Goodall J, Wroblewski E E, Wilson M L, Rudicell R S, Hahn B H, Ochman H. 2012. Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Biological Sciences, 109 (32): 13034-13039.
null den Besten G, van Eunen K, Groen A K, Venema K, Reijngoud D J, Bakker B M. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota and host energy metabolism. Journal of Lipid Research, 54 (9): 2325-2340.
null Dillon R J, Vennard C T, Buckling A, Charnley A K. 2005. Diversity of locust gut bacteria protects against pathogen invasion. Ecology Letters, 8 (12): 1291-1298.
null Ding Y, Bu F, Chen T, Shi G P, Yuan X M, Feng Z Y, Duan Z L, Wang R, Zhang S M, Wang R, Zhang S M, Wang Q, Zhou J Y, Chen Y G. 2021. A next-generation probiotic: Akkermansia muciniphila ameliorates chronic stress-induced depressive-like behavior in mice by regulating gut microbiota and metabolites. Applied Microbiology and Biotechnology, 105 (21-22): 8411-8426.
null Ding Y, Wu Q, Hu Y B, Wang X, Nie Y G, Wu X P, Wei F W. 2017. Advances and prospects of gut microbiome in wild mammals. Acta Theriologica Sinaca, 37 (4): 399-406. (in Chinese)
null Donohue M E, Asangba A E, Ralainirina J, Weisrock D W, Stumpf R M, Wright P C. 2019. Extensive variability in the gut microbiome of a highly?specialized and critically endangered lemur species across sites. American Journal of Primatology, 81 (10-11): e23046.
null Dunbar R, Fleagle J G. 1999. Primate adaptation and evolution. The Journal of the Royal Anthropological Institute, 5: 650.
null Eckermann H A, Ou Y, Lahti L, Weerth C. 2022. Can gut microbiota throughout the first 10 years of life predict executive functioning in childhood? Developmental Psychobiology, 64 (3): e22226.
null Ezenwa V O, Gerardo N M, Inouye D W, Medina M, Xavier J B. 2012. Animal behavior and the microbiome. Science, 338 (6140): 198-199.
null Ezenwa V O, Ghai R R, McKay A F, Williams A E. 2016. Group living and pathogen infection revisited. Current Opinion in Behavioral Sciences, 12: 66-72.
null Fackelmann G, Gillingham M A F, Schmid J, Heni A C, Wilhelm K, Schwensow N, Sommer S. 2021. Human encroachment into wildlife gut microbiomes. Communications Biology, 4 (1): 800.
null Farzi A, Fr?hlich E E, Holzer P. 2018. Gut microbiota and the neuroendocrine system. Neurotherapeutics, 15: 5-22.
null Frankel J S, Mallott E K, Hopper L M, Ross S R, Amato K R. 2019. The effect of captivity on the primate gut microbiome varies with host dietary niche. American Journal of Primatology, 81 (12): e23061.
null Friswell M K, Gika H, Stratford I J, Theodoridis G, Telfer B, Wilson I D, Mcbain A J. 2010. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS ONE, 5 (1): e8584.
null Goldberg T L, Gillespie T R, Rwego I B, Estoff E L, Chapman C A. 2008. Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerging Infectious Diseases, 14 (9): 1375-1382.
null Gomez A, Petrzelkova K, Yeoman C J, Vlckova K, Mrázek J, Koppova I, Carbonero F, Ulanov A, Modry D, Todd A, Torralba M, Nelson K E, Gaskins H R, Wilson B, Stumpf R M, White B A, Leigh S R. 2015. Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology. Molecular Ecology, 24 (10): 2551-2565.
null Gomez A, Rothman J M, Petrzelkova K, Yeoman C J, Vlckova K, Uma?a J D, Carr M, Modry D, Todd A, Torralba M, Nelson K E, Stumpf R M, Wilson B A, Blekhman R, White B A, Leigh S R. 2016. Temporal variation selects for diet?microbe co?metabolic traits in the gut of Gorilla spp. The ISME Journal, 10: 514-526.
null Grassotti T T, Kothe C I, Prichula J, Mohellibi N, Mann M B, Wagner P G C, Campos F S, Campos A A S, Frazzon J, Frazzon A P G. 2021. Fecal bacterial communities of wild black capuchin monkeys (Sapajus nigritus) from the Atlantic Forest biome in Southern Brazil are divergent from those of other non?human primates. Current Research in Microbial Sciences, 2: 100048.
null Grieneisen L E, Livermore J, Alberts S, Tung J, Archie E A. 2017. Group living and male dispersal predict the core gut microbiome in wild baboons. Integrative and Comparative Biology, 57 (4): 770-785.
null Guan Y, Yang H T, Han S Y, Feng L M, Wang T M, Ge J P. 2017. Comparison of the gut microbiota composition between wild and captive sika deer (Cervus nippon hortulorum) from feces by high?throughput sequencing. AMB Express, 7 (1): 212.
null Hale V L, Tan C L, Niu K F, Yang Y Q, Knight R, Zhang Q K, Cui D Y, Amato K R. 2017. Diet versus phylogeny: a comparison of gut microbiota in captive colobine monkey species. Mirobial Ecology, 75: 515-527.
null Hale V L, Tan C L, Niu K F, Yang Y Q, Zhang Q K, Knight R, Amato K R. 2019. Gut microbiota in wild and captive Guizhou snub-nosed monkeys, Rhinopithecus brelichi . American Journal of Primatology, 81 (10-11): e22989.
null Hennessy M B, Mccowan B, Jiang J, Capitanio J P. 2014. Depressive-like behavioral response of adult male rhesus monkeys during routine animal husbandry procedure. Frontiers in Behavioral Neuroscience, 8 (8): 309.
null Hicks A L, Lee K J, Couto?Rodriguez M, Patel J, Sinha R, Guo C, Olson S H, Seimon A, Seimon T A, Ondzie A U, Karesh W B, Reed P, Cameron K N, Lipkin W L, Williams B L. 2018. Gut microbiomes of wild great apes fluctuate seasonally in response to diet. Nature Communications, 9 (1): 1789.
null Ja?arevi? E, Morrison K E, Bale T L. 2016. Sex differences in the gut microbiome-brain axis across the lifespan. Philosophical Transactions of the Royal Society B, 371: 20150122.
null Kalkeri R, Walters K, Pol W V D, Mcfarland B C, Fisher N, Koide F, Morrow C D, Singh V K. 2021. Changes in the gut microbiome community of nonhuman primates following radiation injury. BMC Microbiology, 21 (1): 93.
null Kummrow M. 2021. Diagnostic and therapeutic guidelines to abnormal behavior in captive nonhuman primates. Veterinary Clinics of North America: Exotic Animal Practice, 24 (1): 253-266.
null Kuthyar S, Manus M B, Amato K R. 2019. Leveraging non?human primates for exploring the social transmission of microbes. Current Opinion in Microbiology, 50: 8-14.
null Langille M G I, Zaneveld J, Caporaso J G, Mcdonald D, Knights D, Reyes J A, Clemente J C, Burkepile D E, Thurber R L V, Knight R, Beiko R G, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA maker gene sequences. Nature Biotechnology, 31: 814-821.
null Lee W, Hayakawa T, Kiyono M, Yamabata N, Hanya G. 2019. Gut microbiota composition of Japanese macaques associates with extent of human encroachment. American Journal of Primatology, 81 (12): e23072.
null Levy M, Thaiss C A, Elinav E. 2016. Metabolites: messengers between the microbiota and the immune system. Genes & Development, 30 (14): 1589-1597.
null Ley R E, Hamady M, Lozupone C, Turnbaugh P J, Ramey R R, Bircher S, Schlegel M L, Tucker T A, Schrenzel M D, Knight R, Gordon J I. 2008. Evolution of mammals and their gut microbes. Science, 320 (5883): 1647-1651.
null Li Y H, Chen T, Li Y B, Tang Y, Huang Z H. 2021. Gut microbiota are associated with sex and age of host: Evidence from semi‐provisioned rhesus macaques in southwest Guangxi, China. Ecology and Evolution, 11 (12): 8096-8122.
null Liu R, Amato K, Hou R, Gomez A, Dunn D W, Zhang J, Garber P A, Chapman C A, Righini N, He G, Fang G, Li Y H, Li B G, Guo S T. 2022. Specialized digestive adaptations within the hindgut of a colobine monkey. The Innovation, 2: 103-109.
null Liu S H, Guo R J, Liu F, Yuan Q J, Yu Y, Ren F F. 2020. Gut microbiota regulates depression-like behavior in rats through the neuroendocrine-immune-mitochondrial pathway. Neuropsychiatric Disease and Treatment, 16: 859-869.
null Ma J, Prince A L, Bader D, Hu M, Ganu R, Baquero K, Blundell P, Harris R A, Frias A E, Grove K L, Aagaard K M. 2014. High?fat maternal diet during pregnancy persistently alters the offspring microbiome in a primate model. Nature Communications, 5: 3889-3900.
null Mallott E K, Amato K R, Garber P A, Malhi R S. 2018. Influence of fruit and invertebrate consumption on the gut microbiota of wild white?faced capuchins (Cebus capucinus). American Journal of Physical Anthropology, 165 (3): 576-588.
null Marshall A R. 2008. Ecological report on Magombera forest. Worldwide Fund For Nature Tanzania Programme Office.
null Mckenney E A, Ashwell M, Lambert J E, Fellner V. 2014. Fecal microbial diversity and putative function in captive western lowland gorillas (Gorilla gorilla gorilla), common chimpanzees (Pan troglodytes), hamadryas baboons (Papio hamadryas) and binturongs (Arctictis binturong). Integrative Zoology, 9 (5): 557-569.
null Mckenney E A, O’Connell T M, Rodrigo A, Yoder A D. 2018a. Feeding strategy shapes gut metagenomic enrichment and functional specialization in captive lemurs, Gut Microbes, 9 (3): 202-217.
null Mckenney E A, Koelle K, Dunn R R, Yoder A D. 2018b. The ecosystem services of animal microbiomes. Molecular Ecology, 27 (8): 2164-2172.
null Moeller A H, Foerster S, Wilson M L, Pusey A E, Hahn B H, Ochman H.2016.Social behavior shapes the chimpanzee pan?microbiome. Science Advances, 2: 372-379.
null Moreno?Indias I, Sánchez?Alcoholado L, Sánchez?Garrido M á, Martín?Nú?ez G M, Pérez?Jiménez F, Tena?Sempere M, Tinahones F J, Queipo?Ortu?o M I. 2016. Neonatal androgen exposure causes persistent gut microbiota dysbiosis related to metabolic disease in adult female rats. Endocrinology, 157 (12): 4888-4898.
null Nagpal R, Shively C A, Register T C, Craft S, Yadav H. 2019. Gut microbiome Mediterranean diet interactions in improving host health. F1000Research, 8: 699.
null Nakamura N, Amato K R, Garber P, Estrada A, Mackie R I, Gaskins H R. 2011. Analysis of the hydrogenotrophic microbiota of wild and captive black howler monkeys (Alouatta pigra) in palenque national park, Mexico. American Journal of Primatology, 73 (9): 909-919.
null Namasivayam S, Kauffman K D, Mcculloch J A, Yuan W X, Thovarai V, Mittereder L R, Trinchieri G, Barber D L, Sher A. 2019. Correlation between disease severity and the intestinal microbiome in Mycobacterium tuberculosis?Infected Rhesus Macaques. mBio, 10 (3): e01018-e01019.
null Neufeld K M, Kang N, Bienenstock J, Foster J A. 2011. Reduced anxiety-like behavior and central neurochemical change in germ?free mice. Neurogastroenterology & Motility, 23 (3): 255-264.
null Noguera J C, Aira M, Pérez?Losada M, Domínguez J, Velando A. 2018. Glucocorticoids modulate gastrointestinal microbiome in a wild bird. Royal Society Open Science, 5 (4): 171743.
null Ochman H, Worobey M, Kuo C H, Ndjango J B N, Peeters M, Hahn B H, Hugenholtz P. 2010. Evolutionary relationships of wild hominids recapitulated by gut microbial communities. PLoS Biology, 8 (11): e1000546.
null Oftedal O T, Whiten A, Southgate D A T, Soest P V. 1991. The nutritional consequences of foraging in primates: the relationship of nutrient intakes to nutrient requirements. Philisophical Transaction of The Royal Sociey B: Biological Sciences, 334: 161-170.
null Orkin J D, Campos F A, Myers M S, Hernandez S E C, Guadamuz A, Melin A D. 2019a. Seasonality of the gut microbiota of free?ranging white?faced capuchins in a tropical dry forest. The ISME Journal, 13 (1): 183-196.
null Orkin J D, Webb S E, Melin A D. 2019b. Small to modest impact of social group on the gut microbiome of wild Costa Rican capuchins in a seasonal forest. American Journal of Primatology, 81(10-11): e22985.
null Perofsky A C, Lewis R J, Abondano L A, Fiore A D, Meyers L A. 2017. Hierarchical social networks shape gut microbial composition in wild Verreaux’s sifaka. The Royal Society, 284 (1868): 20172274.
null Perofsky A C, Mayers L A, Abondano L A, Fiore A D, Lewis R J. 2021. Social groups constrain the spatiotemporal dynamics of wild sifaka gut microbiomes. Molecular Ecology, 30 (24): 6759-6775.
null Qi X Y, Yun C Y, Pang Y L, Qiao J. 2021. The impact of the gut microbiota on the reproductive and metabolic endocrine system. Gut Microbes, 13 (1): 21.
null Reese A T, Phillips S R, Owens L A, Venable E M, Langergraber K E, Machanda Z P, Mitani J C, Muller M N, Watts D P, Wrangham R W, Goldberg T L, Thompson M E, Carmody R N. 2021. Age patterning in wild chimpanzee gut microbiota diversity reveals differences from humans in early life. Current Biology, 31 (3): 613-620.
null Reveles K R, Patel S, Forney L, Ross C N. 2019. Age?related changes in the marmoset gut microbiome. American Journal of Primatology, 81 (2): e22960.
null Rudolph K, Schneider D, Fichtel C, Daniel R, Heistermann M, Kappeler P M. 2022. Drivers of gut microbiome variation within and between groups of a wild Malagasy primate. Microbiome, 10 (1): 28.
null Sarkar A, Lehto S M, Harty S, Dinan T G, Cryan J F, Burnet P W J. 2016. Psychobiotics and the manipulation of bacteria?gut?brain signals. Trends in Neurosciences, 39: 763-781.
null Savage D C. 1977. Microbial ecology of the gastrointestinal tract. Annual Reviews in Microbiology, 31 (1): 107-133.
null Sender R, Fuchs S, Milo R. 2016. Revised estimates for the number of human and bacteria cells in the body. PLoS Biology, 14 (8): e1002533.
null Shigeno Y, Toyama M, Nakamura M, Niimi K, Takahashi E, Benno Y. 2018. Comparison of gut microbiota composition between laboratory?bred marmosets (Callithrix jacchus) with chronic diarrhea and healthy animals using terminal restriction fragment length polymorphism analysis. Microbiology and Immunology, 62(11): 702-710.
null Shively C A, Willard S L. 2012. Behavioral and neurobiological characteristics of social stress versus depression in nonhuman primates. Experimental Neurology, 233 (1): 87-94.
null Sun B H, Wang X, Bernstein S, Huffman M A, Xia D P, Gu Z Y, Chen R, Sheeran L K, Wagner R S, Li J H. 2016. Marked variation between winter and spring gut microbiota in free?ranging Tibetan macaques (Macaca thibetana). Scientific Reports, 6: 26035.
null Trosvik P, de Muinck E J, Rueness E K, Fashing P J, Beierschmitt E C, Callingham K R, Kraus J B, Trew T H, Moges A, Mekonnen A, Venkataraman V V, Nguyen N. 2018a. Multilevel social structure and diet shape the gut microbiota of the gelada monkey, the only grazing primate. Microbiome, 6 (1): 84.
null Trosvik P, Rueness E K, de Muinck E J, Moges A, Mekonnen A. 2018b. Ecological plasticity in the gastrointestinal microbiomes of Ethiopian Chlorocebus monkeys. Scientific Reports, 8 (1): 20.
null Tung J, Barreiro L B, Burns M B, Grenier J C, Lynch J, Grieneisen L E, Altmann J, Alberts S C, Blekhman R, Archie E A. 2015. Social networks predict gut microbiome composition in wild baboons. eLife, 4 (4): e05224.
null Uenishi G, Fujita S, Ohashi G, Kato A, Yamauchi S, Matsuzawa T, Ushida K. 2007. Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity. American Journal of Primatology, 69 (4): 367-376.
null Unwin T, Smith A. 2010. Behavioral differences between provisioned and non?provisioned Barbary macaques (Macaca sylvanus). Anthrozo?s, 23 (2): 109-118.
null Wang L, Beier U H, Akimova T, Dahiya S, Han R, Samanta A, Levine M H, Hancock W W. 2018. Histone/protein deacet-ylase inhibitor therapy for enhancement of Foxp3+ T-regulatory cell function posttransplantation. American Journal of Transplantation, 18: 1596-1603.
null Wei F W, Shan L, Hu Y B, Nie Y G. 2019. Conservation evolutionary biology: a new branch of conservation biology. Science China life Sciences, 49 (4): 498-508. (in Chinese)
null Wei Z Y, Rao J H, Tang M T, Zhao G A, Li Q C, Wu L M, Liu S Q, Li B H, Xiao B Q, Liu X Y, Chen J H. 2022. Characterization of changes and driver microbes in gut microbiota during healthy aging using a captive monkey model. Genomics, Proteomics & Bioinformatics, 20 (2): 350-365.
null Wikberg E C, Christie D, Sicotte P, Ting N. 2020. Interactions between social groups of colobus monkeys (Colobus vellerosus) explain similarities in their gut microbiomes. Animal Behaviour, 163: 17-31.
null Wu X Y, Wei X B, Shang Y Q, Zhang H H. 2021. Evolutionary and dietary relationships of wild mammals based on the gut microbiome. Gene, 808: 145999.
null Xia W C, Liu G Q, Wang D L, Chen H, Zhu L F, Li D Y. 2022. Functional convergence of Yunnan snub?nosed monkey and bamboo?eating panda gut microbiomes revealing the driving by dietary flexibility on mammal gut microbiome. Computational and Structural Biotechnology Journal, 20: 685-699.
null Xie T Q, Wang Y C, Zou Z J, He J, Yu Y, Liu Y Q, Bai J B. 2020. Environmental tobacco smoke exposure and breastfeeding duration influence the composition and dynamics of gut microbiota in young children aged 0-2 years. Biological Research For Nursing, 23 (3): 1099800420975129.
null Yang S Z, Liu Y, Yang N, Lan Y, Lan Y, Feng J Y, Yue B S, He M, Zhang L, Zhang A Y, Price M, Li J, Fan Z X. 2022. The gut microbiome and antibiotic resistome of chronic diarrhea rhesus macaques (Macaca mulatta) and its similarity to the human gut microbiome. Microbiome, 10 (1): 29.
null Yang Y, Li Q H, Garber P A, Grueter C C, Ren G P, Wang X W, Huang Z P, Xiang Z F, Xiao W, Behie A. 2020. Cafeteria: style feeding trials provide new insights into the diet and nutritional strategies of the black snub?nosed monkey (Rhinopithecus strykeri): implications for conservation. American Journal of Primatology, 82 (3): e23108.
null Yasuda K, Oh K, Ren B, Tickle T L, Franzosa E A, Wachtman L M, Miller A D, Westmoreland S V, Mansfield K G, Vallender E J, Miller G M, Rowlett J K, Gevers D, Huttenhower C, Morgan X C. 2015. Biogeography of the intestinal mucosal and luminal microbiome in the rhesus macaque. Cell Host & Microbe, 17 (3): 385-391.
null Yi L N. 2019. Gut microbiota of wild snub-nosed monkeys (Rhinopithecus roxellana) in Shennongjia: variation in relation to seasonality, age, and gender. Master thesis.Beijing: University of Chinses Academy of Sciences. (in Chinese)
null Yildirim S, Yeoman C J, Sipos M, Torralba M, Wilson B A, Goldberg T L, Stumpf R M, Leigh S R, White B A, Nelson K E. 2010. Characterization of the fecal microbiome from non?human wild primates reveals species specific microbial communities. PLoS ONE, 5 (11): e13963.
null Zeng Y, Pu Y, Niu L L, Deng J B, Zeng D, Amato K R, Li Y, Zhou Y, Lin Y C, Wang J, Wu L Q, Chen B H, Pan K C, Jing B, Ni X Q. 2022. Comparison of gastrointestinal microbiota in golden snub-nosed monkey (Rhinopithecus roxellanae), green monkey (Chlorocebus aethiops sabaeus), and ring?tailed lemur (Lemur catta) by high throughput sequencing. Global Ecology and Conservation, 33: e01946.
null Zhan J, Ma X R, Liu D H, Liang Y R, Li P Z, Cui J N, Zhou Z Q, Wang P. 2020. Gut microbiome alterations induced by tributyltin exposure are associated with increased body weight, impaired glucose and insulin homeostasis and endocrine disruption in mice. Environmental Pollution, 266 (Pt 3): 115276.
null Zhang Z G, Xu D M, Wang L, Hao J J, Wang J F, Zhou X, Wang W W, Qiu Q, Huang X D, Zhou J W, Long R J, Zhao F Q, Shi P. 2016. Convergent evolution of rumen microbiomes in high?altitude mammals. Current Biology, 26 (14): 1873-1879.
null Zhao Q, Elson C O. 2018. Adaptive immune education by gut microbiota antigens. Immunology, 154 (1): 28-37.
null Zheng P, Wu J, Zhang H P, Perry S W, Yin B M, Tan X M, Chai T J, Liang W W, Huang Y, Li Y F, Duan J J, Wong M L, Licinio J, Xie P. 2020. The gut microbiome modulates gut-brain axis glycerophospholipid metabolism in a region-specific manner in a nonhuman primate model of depression. Molecular Psychiatry, 26 (6): 2380-2392.
null Zhu L F, Suhr Van Haute M J, Hassenstab H R, Smith C, Rose D J, Mustoe A C, Benson A K, French J A. 2020. Fecal short?chain fatty acid concentrations increase in newly paired male marmosets (Callithrix jacchus). mSphere, 5 (5): e00794-20.
null 丁赟, 吴琦, 胡义波, 王潇, 聂永刚, 吴小平, 魏辅文. 2017. 野生哺乳动物肠道微生物组成研究进展与展望. 兽类学报, 37 (4): 399-406.
null 伊丽娜. 2019. 神农架野生川金丝猴肠道菌群不同季节、年龄、性别差异的研究. 北京: 中国科学院大学硕士学位论文.
null 魏辅文, 单磊, 胡义波, 聂永刚. 2019. 保护演化生物学—保护生物学的新分支. 中国科学: 生命科学, 49 (4): 498-508.
Outlines

/

〈 〉