Neutrality in the Metaorganism

Abstract

Almost all animals and plants are inhabited by diverse communities of microorganisms, the microbiota, thereby forming an integrated entity, the metaorganism. Natural selection should favor hosts that shape the community composition of these microbes to promote a beneficial host-microbe symbiosis. Indeed, animal hosts often pose selective environments, which only a subset of the environmentally available microbes are able to colonize. How these microbes assemble after colonization to form the complex microbiota is less clear. Neutral models are based on the assumption that the alternatives in microbiota community composition are selectively equivalent and thus entirely shaped by random population dynamics and dispersal. Here, we use the neutral model as a null hypothesis to assess microbiata composition in host organisms, which does not rely on invoking any adaptive processes underlying microbial community assembly. We show that the overall microbiota community structure from a wide range of host organisms, in particular including previously understudied invertebrates, is in many cases consistent with neutral expectations. Our approach allows to identify individual microbes that are deviating from the neutral expectation and are therefore interesting candidates for further study. Moreover, using simulated communities, we demonstrate that transient community states may play a role in the deviations from the neutral expectation. Our findings highlight that the consideration of neutral processes and temporal changes in community composition are critical for an in-depth understanding of microbiota-host interactions.

Metacommunity theory for transmission of heritable symbionts within insect communities

“…Modeling metacommunities can also deepen our understanding patterns of diversity of host-associated microbiomes. Previous work on microbiomes has suggested that stochasticity plays a significant role in community assembly, and that the process is inherently hard to predict (see Adair, Wilson, Bost, & Douglas, 2018;Obadia et al, 2017;Sieber et al, 2019;Vega & Gore, 2017), based on findings that are consistent with the neutral theory of biodiversity (Hubbell, 2001). Recent models for metacommunity diversity (e.g., O'Sullivan, Knell, & Rossberg, 2019) can be utilized to answer questions about ecological structural stability influencing microbiome diversity, and whether the microbiome adheres to broad ecological patterns of diversity.…”

Diel patterning in the bacterial community associated with the sea anemone Nematostella vectensis

“…Consistent detection of these two bacterial groups in select anthozoan cnidarians may imply nonrandom associations and conserved taxa, together suggesting some biological importance. However, while differences between the animal-associated bacteria and those in the surrounding environment suggest selection, neutral and stochastic factors may explain how these bacterial communities shift over time and between individuals (Sieber et al, 2019). For example, it is unclear whether the OTUs we identified as cycling may be a result of the anemone, interbacterial interactions independent of the host, or a combination of both factors.…”

“…The small number of OTUs showing 24-hr oscillating abundance could be a result of the subset of differentially expressed immune genes, which could be tissue specific.Complementary to photoperiod-related shifts in cnidarian-associated microbiota we report here, a number of studies have shown that additional rhythmic abiotic factors may affect compositional changes in these symbiont communities(Cai et al, 2018;Sharp, Pratte, Kerwin, Rotjan, & Stewart, 2017; Silveira et al, 2017; Sweet, Brown, Dunne, Singleton, & Bulling, 2017). However, while differences between the animal-associated bacteria and those in the surrounding environment suggest selection, neutral and stochastic factors may explain how these bacterial communities shift over time and between individuals(Sieber et al, 2019). When comparing the bacterial communities of N. vectensis across development, environmental conditions, and geographic locations, Mortzfeld et al (2016) and Domin et al (2018) both detected Rhodobacterales and Alteromonadales.…”

Stochastic colonization of hosts with a finite lifespan can drive individual host microbes out of equilibrium

“…We assume the death of hosts can be approximated as an event occurring each time step with probability τ , given by the probability of host death-birth events per microbial death-birth event. The limiting case τ = 0 corresponds to infinitely living hosts (as in [ 3 , 7 ]), while τ = 1 corresponds to hosts whose lifespan is as short as the average lifespan of a microbe, leading to almost entirely empty hosts.…”

“…Previous applications of neutral models to microbiome data have generally ignored these host-level processes by assuming essentially static hosts with infinite lifespans, allowing convergence to a long-term equilibrium distribution of microbial abundances, see e.g. [ 7 ]. However, any real host species will have a finite lifespan that may not allow for the community to settle down on a potential long-term composition.…”