Linking Statistical and Ecological Theory: Hubbell's Unified Neutral Theory of Biodiversity as a Hierarchical Dirichlet Process

Abstract

Neutral models which assume ecological equivalence between species provide null models for community assembly. In Hubbell's Unified Neutral Theory of Biodiversity (UNTB), many local communities are connected to a single metacommunity through differing immigration rates. Our ability to fit the full multi-site UNTB has hitherto been limited by the lack of a computationally tractable and accurate algorithm. We show that a large class of neutral models with this mainland-island structure but differing local community dynamics converge in the large population limit to the hierarchical Dirichlet process. Using this approximation we developed an efficient Bayesian fitting strategy for the multi-site UNTB. We can also use this approach to distinguish between neutral local community assembly given a non-neutral metacommunity distribution and the full UNTB where the metacommunity too assembles neutrally. We applied this fitting strategy to both tropical trees and a data set comprising 570,851 sequences from 278 human gut microbiomes. The tropical tree data set was consistent with the UNTB but for the human gut neutrality was rejected at the whole community level. However, when we applied the algorithm to gut microbial species within the same taxon at different levels of taxonomic resolution, we found that species abundances within some genera were almost consistent with local community assembly. This was not true at higher taxonomic ranks. This suggests that the gut microbiota is more strongly niche constrained than macroscopic organisms, with different groups adopting different functional roles, but within those groups diversity may at least partially be maintained by neutrality. We also observed a negative correlation between body mass index and immigration rates within the family Ruminococcaceae. This provides a novel interpretation of the impact of obesity on the human microbiome as a relative increase in the importance of local growth versus external immigration within this key group of carbohydrate degrading organisms.

Microbial ecosystems are dominated by specialist taxa

“…Recent work (Harris et al . ) in statistical ecology looking at the fit of neutral models (Hubbell ) to human gut microbiota reach similar conclusions: neutrality is rejected from abundance data at all but low taxonomic ranks (genus). Overall, habitat filtering selects specialist taxa, probably based on markedly different metabolic and functional roles (Fierer et al .…”

Latent Dirichlet Allocation reveals spatial and taxonomic structure in a DNA‐based census of soil biodiversity from a tropical forest

“…Another popular and slightly different version of LDA consists of adding a Dirichlet prior also on the taxonomic composition of assemblages (Griffiths & Steyvers, ; Valle et al, ). In an ecological context, this assumption is reminiscent of Hubbell's neutral model prediction that taxa‐abundance distributions are, to a good approximation, dispersal‐biased realizations of a Dirichlet distribution (Harris et al, ; Sloan, Woodcock, Lunn, Head, & Curtis, ). The linkage between the neutral theory of biodiversity and inferential methods based on the Dirichlet process is an interesting and possibly promising avenue of research (Harris et al, ).…”

A general sampling formula for community structure data

“…Harris et al . () circumvented the latter problem, but their approach is based on Bayesian computation rather than on a simple likelihood formula.…”