Department of Ecology & Evolutionary Biology, Brown University, Providence, RI 02912;
Department of Ecology & Evolutionary Biology, Princeton University, Princeton, NJ 08544.
Proc Natl Acad Sci U S A. 2019 Nov 19;116(47):23588-23593. doi: 10.1073/pnas.1905666116. Epub 2019 Nov 4.
A major challenge in biology is to understand how phylogeny, diet, and environment shape the mammalian gut microbiome. Yet most studies of nonhuman microbiomes have relied on relatively coarse dietary categorizations and have focused either on individual wild populations or on captive animals that are sheltered from environmental pressures, which may obscure the effects of dietary and environmental variation on microbiome composition in diverse natural communities. We analyzed plant and bacterial DNA in fecal samples from an assemblage of 33 sympatric large-herbivore species (27 native, 6 domesticated) in a semiarid East African savanna, which enabled high-resolution assessment of seasonal variation in both diet and microbiome composition. Phylogenetic relatedness strongly predicted microbiome composition ( = 0.91) and was weakly but significantly correlated with diet composition ( = 0.20). Dietary diversity did not significantly predict microbiome diversity across species or within any species except kudu; however, diet composition was significantly correlated with microbiome composition both across and within most species. We found a spectrum of seasonal sensitivity at the diet-microbiome nexus: Seasonal changes in diet composition explained 25% of seasonal variation in microbiome composition across species. Species' positions on (and deviations from) this spectrum were not obviously driven by phylogeny, body size, digestive strategy, or diet composition; however, domesticated species tended to exhibit greater diet-microbiome turnover than wildlife. Our results reveal marked differences in the influence of environment on the degree of diet-microbiome covariation in free-ranging African megafauna, and this variation is not well explained by canonical predictors of nutritional ecology.
生物学的一个主要挑战是了解系统发育、饮食和环境如何塑造哺乳动物的肠道微生物组。然而,大多数非人类微生物组的研究依赖于相对粗糙的饮食分类,并且要么侧重于单个野生种群,要么侧重于免受环境压力影响的圈养动物,这可能掩盖了饮食和环境变化对不同自然群落中微生物组组成的影响。我们分析了在东非半干旱草原上 33 种共生大型食草动物(27 种本地,6 种驯化)的粪便样本中的植物和细菌 DNA,这使得对饮食和微生物组组成的季节性变化进行高分辨率评估成为可能。系统发育关系强烈预测微生物组组成(=0.91),与饮食组成(=0.20)呈弱但显著相关。饮食多样性并没有显著预测除大角斑羚外的所有物种的微生物多样性,也没有预测任何物种的微生物多样性;然而,饮食组成与大多数物种的微生物组成在种间和种内都呈显著相关。我们在饮食-微生物组交汇点发现了一个季节性敏感性的范围:饮食组成的季节性变化解释了种间微生物组组成季节性变化的 25%。物种在(和偏离)这个光谱上的位置不是由系统发育、体型、消化策略或饮食组成驱动的;然而,驯化物种往往比野生动物表现出更大的饮食-微生物组周转率。我们的研究结果揭示了环境对自由放养的非洲巨型动物中饮食-微生物组协变程度的影响存在显著差异,这种差异不能用营养生态学的典型预测因子很好地解释。
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