Abstract
The human microbiome project (HMP) has made it possible to test important ecological theories for arguably the most important ecosystem to human health—the human microbiome. Existing limited number of studies have reported conflicting evidence in the case of the neutral theory; the present study aims to comprehensively test the neutral theory with extensive HMP datasets covering all five major body sites inhabited by the human microbiome. Utilizing 7437 datasets of bacterial community samples, we discovered that only 49 communities (less than 1%) satisfied the neutral theory, and concluded that human microbial communities are not neutral in general. The 49 positive cases, although only a tiny minority, do demonstrate the existence of neutral processes. We realize that the traditional doctrine of microbial biogeography “Everything is everywhere, but the environment selects” first proposed by Baas-Becking resolves the apparent contradiction. The first part of Baas-Becking doctrine states that microbes are not dispersal-limited and therefore are neutral prone, and the second part reiterates that the freely dispersed microbes must endure selection by the environment. Therefore, in most cases, it is the host environment that ultimately shapes the community assembly and tip the human microbiome to niche regime.
Highlights
Hubbell’s1 neutral theory presented a null model for testing the mechanisms of species coexistence and biodiversity maintenance in ecological communities
The scarcity is primarily due to the reality that majority of microbes are not cultivable, and their detections were extremely difficult until the invention of the metagenomic technology nearly a decade ago, which revolutionized the techniques for studying microbial community ecology[39,40,41,42,43]
Etienne[57] compared the two sampling formulae using Barro Colorado (BCI) tree dataset[61] and Caño Maraca (CM) fish dataset[62], and the results showed that Etienne sampling formula led to a significantly better fit to the datasets than Ewens sampling formula did
Summary
Hubbell’s1 neutral theory presented a null model for testing the mechanisms of species coexistence and biodiversity maintenance in ecological communities. It offered a simple mechanistic explanation of the species abundance distributions (SAD), which has been extensively studied in community ecology since the 1940s, but still lacks a theoretical consensus for their interpretations[2,3,4,5,6,7,8]. Woodcock[28] performed the first comprehensive testing of the neutral theory in microbial ecology, and presented strong evidence that neutral community models fitted to the microbial communities in tree holes filled by rain water[28,45] conjectured that the scale of regional communities in microbes might be different from that of macro-communities since the dispersal distance of microbes can be more extensive. There were the opposite cases, i.e., neutral effect is more significant (e.g. ref. 48)
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