Significance Across ecology, and particularly within microbial ecology, there is limited understanding of the mechanisms governing the relative influences of stochastic and deterministic processes. ...Filling this knowledge gap is a major challenge that requires the development of novel conceptual paradigms, experiments, and ecological models. Here we ( i ) present a conceptual model that couples the stochastic/deterministic balance to primary and secondary ecological succession, thereby integrating previously isolated conceptual domains; ( ii ) evaluate this model over 105 years of ecosystem development, revealing a systematic shift in the type and strength of ecological selection; and ( iii ) couple empirical data with a new simulation model to elucidate underlying mechanisms and characterize their scale dependency. The insights and conceptual framework provided here represent a nexus for cross-system integration.
Ecological succession and the balance between stochastic and deterministic processes are two major themes within microbial ecology, but these conceptual domains have mostly developed independent of each other. Here we provide a framework that integrates shifts in community assembly processes with microbial primary succession to better understand mechanisms governing the stochastic/deterministic balance. Synthesizing previous work, we devised a conceptual model that links ecosystem development to alternative hypotheses related to shifts in ecological assembly processes. Conceptual model hypotheses were tested by coupling spatiotemporal data on soil bacterial communities with environmental conditions in a salt marsh chronosequence spanning 105 years of succession. Analyses within successional stages showed community composition to be initially governed by stochasticity, but as succession proceeded, there was a progressive increase in deterministic selection correlated with increasing sodium concentration. Analyses of community turnover among successional stages—which provide a larger spatiotemporal scale relative to within stage analyses—revealed that changes in the concentration of soil organic matter were the main predictor of the type and relative influence of determinism. Taken together, these results suggest scale-dependency in the mechanisms underlying selection. To better understand mechanisms governing these patterns, we developed an ecological simulation model that revealed how changes in selective environments cause shifts in the stochastic/deterministic balance. Finally, we propose an extended—and experimentally testable—conceptual model integrating ecological assembly processes with primary and secondary succession. This framework provides a priori hypotheses for future experiments, thereby facilitating a systematic approach to understand assembly and succession in microbial communities across ecosystems.
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 multisite 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 multisite UNTB. We can also use this approach to distinguish between neutral local community assembly given a nonneutral 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.
Ecological community assembly is governed by a combination of (i) selection resulting from among-taxa differences in performance; (ii) dispersal resulting from organismal movement; and (iii) ...ecological drift resulting from stochastic changes in population sizes. The relative importance and nature of these processes can vary across environments. Selection can be homogeneous or variable, and while dispersal is a rate, we conceptualize extreme dispersal rates as two categories; dispersal limitation results from limited exchange of organisms among communities, and homogenizing dispersal results from high levels of organism exchange. To estimate the influence and spatial variation of each process we extend a recently developed statistical framework, use a simulation model to evaluate the accuracy of the extended framework, and use the framework to examine subsurface microbial communities over two geologic formations. For each subsurface community we estimate the degree to which it is influenced by homogeneous selection, variable selection, dispersal limitation, and homogenizing dispersal. Our analyses revealed that the relative influences of these ecological processes vary substantially across communities even within a geologic formation. We further identify environmental and spatial features associated with each ecological process, which allowed mapping of spatial variation in ecological-process-influences. The resulting maps provide a new lens through which ecological systems can be understood; in the subsurface system investigated here they revealed that the influence of variable selection was associated with the rate at which redox conditions change with subsurface depth.
In this perspective, we evaluate the explanatory power of the neutral theory of molecular evolution, 50 years after its introduction by Kimura. We argue that the neutral theory was supported by ...unreliable theoretical and empirical evidence from the beginning, and that in light of modern, genome-scale data, we can firmly reject its universality. The ubiquity of adaptive variation both within and between species means that a more comprehensive theory of molecular evolution must be sought.
Spatial turnover in the composition of biological communities is governed by (ecological) Drift, Selection and Dispersal. Commonly applied statistical tools cannot quantitatively estimate these ...processes, nor identify abiotic features that impose these processes. For interrogation of subsurface microbial communities distributed across two geologically distinct formations of the unconfined aquifer underlying the Hanford Site in southeastern Washington State, we developed an analytical framework that advances ecological understanding in two primary ways. First, we quantitatively estimate influences of Drift, Selection and Dispersal. Second, ecological patterns are used to characterize measured and unmeasured abiotic variables that impose Selection or that result in low levels of Dispersal. We find that (i) Drift alone consistently governs ∼25% of spatial turnover in community composition; (ii) in deeper, finer-grained sediments, Selection is strong (governing ∼60% of turnover), being imposed by an unmeasured but spatially structured environmental variable; (iii) in shallower, coarser-grained sediments, Selection is weaker (governing ∼30% of turnover), being imposed by vertically and horizontally structured hydrological factors;(iv) low levels of Dispersal can govern nearly 30% of turnover and be caused primarily by spatial isolation resulting from limited exchange between finer and coarser-grain sediments; and (v) highly permeable sediments are associated with high levels of Dispersal that homogenize community composition and govern over 20% of turnover. We further show that our framework provides inferences that cannot be achieved using preexisting approaches, and suggest that their broad application will facilitate a unified understanding of microbial communities.
A recent article reassessing the Neutral Theory of Molecular Evolution claims that it is no longer as important as is widely believed. The authors argue that “the neutral theory was supported by ...unreliable theoretical and empirical evidence from the beginning, and that in light of modern, genome-scale data, we can firmly reject its universality.” Claiming that “the neutral theory has been overwhelmingly rejected,” they propose instead that natural selection is the major force shaping both between-species divergence and within-species variation. Although this is probably a minority view, it is important to evaluate such claims carefully in the context of current knowledge, as inaccuracies can sometimes morph into an accepted narrative for those not familiar with the underlying science. We here critically examine and ultimately reject Kern and Hahn’s arguments and assessment, and instead propose that it is now abundantly clear that the foundational ideas presented five decades ago by Kimura and Ohta are indeed correct.
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 multisite 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 multisite UNTB. We can also use this approach to distinguish between neutral local community assembly given a nonneutral 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.
This study addressed the selection of the rhizospheric microbial community from the bulk soil reservoir under agricultural management of soybean in Amazon forest soils. We used a shotgun metagenomics ...approach to investigate the taxonomic and functional diversities of microbial communities in the bulk soil and in the rhizosphere of soybean plants and tested the validity of neutral and niche theories to explain the rhizosphere community assembly processes. Our results showed a clear selection at both taxonomic and functional levels operating in the assembly of the soybean rhizosphere community. The taxonomic analysis revealed that the rhizosphere community is a subset of the bulk soil community. Species abundance in rhizosphere fits the log-normal distribution model, which is an indicator of the occurrence of niche-based processes. In addition, the data indicate that the rhizosphere community is selected based on functional cores related to the metabolisms of nitrogen, iron, phosphorus and potassium, which are related to benefits to the plant, such as growth promotion and nutrition. The network analysis including bacterial groups and functions was less complex in rhizosphere, suggesting the specialization of some specific metabolic pathways. We conclude that the assembly of the microbial community in the rhizosphere is based on niche-based processes as a result of the selection power of the plant and other environmental factors.
Approximately 2-4% of genetic material in human populations outside Africa is derived from Neanderthals who interbred with anatomically modern humans. Recent studies have shown that this Neanderthal ...DNA is depleted around functional genomic regions; this has been suggested to be a consequence of harmful epistatic interactions between human and Neanderthal alleles. However, using published estimates of Neanderthal inbreeding and the distribution of mutational fitness effects, we infer that Neanderthals had at least 40% lower fitness than humans on average; this increased load predicts the reduction in Neanderthal introgression around genes without the need to invoke epistasis. We also predict a residual Neanderthal mutational load in non-Africans, leading to a fitness reduction of at least 0.5%. This effect of Neanderthal admixture has been left out of previous debate on mutation load differences between Africans and non-Africans. We also show that if many deleterious mutations are recessive, the Neanderthal admixture fraction could increase over time due to the protective effect of Neanderthal haplotypes against deleterious alleles that arose recently in the human population. This might partially explain why so many organisms retain gene flow from other species and appear to derive adaptive benefits from introgression.
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