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 which 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, ; Obadia et al, ; Sieber et al, ; Vega & Gore, ), based on findings that are consistent with the neutral theory of biodiversity (Hubbell, ). Recent models for metacommunity diversity (e.g., O'Sullivan, Knell, & Rossberg, ) can be utilized to answer questions about ecological structural stability influencing microbiome diversity, and whether the microbiome adheres to broad ecological patterns of diversity.…”

Common structuring principles of the Drosophila melanogaster microbiome on a continental scale and between host and substrate

“…These processes comprise ecological drift, dispersal and colonization history. It appears plausible for diverse species (Sieber et al ., ), including Drosophila (Adair et al ., ) that neutral processes dominate microbiome assembly.…”

Environmental conditions and neutral processes shape the skin microbiome of European catfish (Silurus glanis) populations of Southwestern France

“…Besides such deterministic processes, recent work has demonstrated a variable contribution of neutral processes (i.e., stochastic microbes immigration and extinction from the local microbial pool) in shaping microbiomes of various animals, including fishes (Jeraldo et al ., ; Levy and Borenstein, ; Burns et al ., ; Sieber et al ., ). However, knowledge about the relative roles of deterministic ( endogenous and exogenous host's factors) and neutral processes shaping fish skin microbiome remains limited to a restricted number of host species.…”