Duke University Program in Ecology, Duke University, Durham, North Carolina.
Department of Evolutionary Anthropology, Duke University, Durham, North Carolina.
Am J Primatol. 2019 Oct;81(10-11):e22974. doi: 10.1002/ajp.22974. Epub 2019 Apr 1.
Research on animal microbiomes is increasingly aimed at determining the evolutionary and ecological factors that govern host-microbiome dynamics, which are invariably intertwined and potentially synergistic. We present three empirical studies related to this topic, each of which relies on the diversity of Malagasy lemurs (representing a total of 19 species) and the comparative approach applied across scales of analysis. In Study 1, we compare gut microbial membership across 14 species in the wild to test the relative importance of host phylogeny and feeding strategy in mediating microbiome structure. Whereas host phylogeny strongly predicted community composition, the same feeding strategies shared by distant relatives did not produce convergent microbial consortia, but rather shaped microbiomes in host lineage-specific ways, particularly in folivores. In Study 2, we compare 14 species of wild and captive folivores, frugivores, and omnivores, to highlight the importance of captive populations for advancing gut microbiome research. We show that the perturbational effect of captivity is mediated by host feeding strategy and can be mitigated, in part, by modified animal management. In Study 3, we examine various scent-gland microbiomes across three species in the wild or captivity and show them to vary by host species, sex, body site, and a proxy of social status. These rare data provide support for the bacterial fermentation hypothesis in olfactory signal production and implicate steroid hormones as mediators of microbial community structure. We conclude by discussing the role of scale in comparative microbial studies, the links between feeding strategy and host-microbiome coadaptation, the underappreciated benefits of captive populations for advancing conservation research, and the need to consider the entirety of an animal's microbiota. Ultimately, these studies will help move the field from exploratory to hypothesis-driven research.
对动物微生物组的研究越来越侧重于确定控制宿主-微生物组动态的进化和生态因素，这些因素总是相互交织且可能协同作用。我们提出了三项与该主题相关的实证研究，每项研究都依赖于马达加斯加狐猴（共代表 19 个物种）的多样性和应用于跨分析尺度的比较方法。在研究 1 中，我们比较了 14 种野生狐猴的肠道微生物组成，以检验宿主系统发育和摄食策略在调节微生物组结构方面的相对重要性。尽管宿主系统发育强烈预测了群落组成，但亲缘关系较远的相同摄食策略并没有产生趋同的微生物群落，而是以宿主谱系特异性的方式塑造了微生物组，尤其是在食叶动物中。在研究 2 中，我们比较了 14 种野生和圈养的食叶动物、食果动物和杂食动物，以强调圈养种群对推进肠道微生物组研究的重要性。我们表明，圈养的扰动效应是由宿主的摄食策略介导的，并且可以通过改变动物管理在一定程度上减轻。在研究 3 中，我们在野外或圈养的三个物种中检查了各种气味腺微生物组，并发现它们因宿主物种、性别、身体部位和社会地位的替代物而有所不同。这些罕见的数据为嗅觉信号产生中的细菌发酵假说提供了支持，并暗示类固醇激素是微生物群落结构的介导者。最后，我们讨论了规模在比较微生物研究中的作用、摄食策略和宿主-微生物组共适应之间的联系、圈养种群在推进保护研究方面的未被充分认识的益处，以及考虑动物全部微生物组的必要性。最终，这些研究将帮助该领域从探索性研究向假设驱动的研究转变。
