Ecological Neutral Theory Research Articles

Neutral and niche theory in community ecology: a framework for comparing model realism

Ecological neutral theory has been controversial as an alternative to niche theory for explaining community structure. Neutral theory, which explains community structure in terms of ecological drift, is frequently charged with being unrealistic, but commentators have usually not provided an account of theory or model realism. In this paper, I propose a framework for comparing the “realism” or accuracy of alternative theories within a domain with respect to the extent to which the theories abstract and idealize. Using this framework I argue, contrary to most previous commentators, that neutral and niche theories are similarly realistic. Realism cannot provide a basis for accepting or rejecting either type of theory; instead, community ecologists should continue working with a plurality of models. While theoretical unification may become possible, we should treat a plurality of complementary, partial models as the expected situation within community ecology.

Age-dependent extinction and the neutral theory of biodiversity.

Red Queen (RQ) theory states that adaptation does not protect species from extinction because their competitors are continually adapting alongside them. RQ was founded on the apparent independence of extinction risk and fossil taxon age, but analytical developments have since demonstrated that age-dependent extinction is widespread, usually most intense among young species. Here, we develop ecological neutral theory as a general framework for modeling fossil species survivorship under incomplete sampling. We show that it provides an excellent fit to a high-resolution dataset of species durations for Paleozoic zooplankton and more broadly can account for age-dependent extinction seen throughout the fossil record. Unlike widely used alternative models, the neutral model has parameters with biological meaning, thereby generating testable hypotheses on changes in ancient ecosystems. The success of this approach suggests reinterpretations of mass extinctions and of scaling in eco-evolutionary systems. Intense extinction among young species does not necessarily refute RQ or require a special explanation but can instead be parsimoniously explained by neutral dynamics operating across species regardless of age.

Ecological neutral theory reveals the effect of biases in the fossil record.

Ecological neutral theory reveals the effect of biases in the fossil record.

Abundance does not predict extinction risk in the fossil record of marine plankton

A major premise of ecological neutral theory is that population size is inversely related to extinction risk. This idea is central to modern biodiversity conservation efforts, which often rely on abundance metrics to partially determine species extinction risk. However, limited empirical studies have tested whether extinction is indeed more probable for species with low abundances. Here we use the fossil record of Neogene radiolaria to test the relationship between relative abundance and longevity (time from first to last occurrence). Our dataset includes abundance histories for 189 polycystine radiolarian species from the Southern Ocean, and 101 species from the tropical Pacific. Using linear regression analyses, we show that neither maximum nor average relative abundance are significant predictors of longevity in either oceanographic region. This suggests that neutral theory fails to explain the plankton ecological-evolutionary dynamics we observe. Extrinsic factors are likely more important than neutral dynamics in controlling radiolarian extinction.

The relative abundance of languages: Neutral and non-neutral dynamics.

Credible estimates suggest that a large number of the nearly 7000 languages in the world could go extinct this century, a prospect with profound cultural, socioeconomic, and political ramifications. Despite its importance, we still have little predictive theory for language dynamics and richness. Critical to the language extinction problem, however, is to understand the dynamics of the number of speakers of languages, the dynamics of language abundance distributions (LADs). Many regional LADs are very similar to the bell-shaped distributions of relative species abundance predicted by neutral theory in ecology. Using the tenets of neutral theory, here we show that LADs can be understood as an equilibrium or disequilibrium between stochastic rates of origination and extinction of languages. However, neutral theory does not fit some regional LADs, which can be explained if the number of speakers has grown systematically faster in some languages than others, due to cultural factors and other non-neutral processes. Only the LADs of Australia and the United States, deviate from a bell-shaped pattern. These deviations are due to the documented higher, non-equilibrium extinction rates of low-abundance languages in these countries.

Analysing the distance decay of community similarity in river networks using Bayesian methods

The distance decay of community similarity (DDCS) is a pattern that is widely observed in terrestrial and aquatic environments. Niche-based theories argue that species are sorted in space according to their ability to adapt to new environmental conditions. The ecological neutral theory argues that community similarity decays due to ecological drift. The continuum hypothesis provides an intermediate perspective between niche-based theories and the neutral theory, arguing that niche and neutral factors are at the opposite ends of a continuum that ranges from competitive to stochastic exclusion. We assessed the association between niche-based and neutral factors and changes in community similarity measured by Sorensen’s index in riparian plant communities. We assessed the importance of neutral processes using network distances and flow connection and of niche-based processes using Strahler order differences and precipitation differences. We used a hierarchical Bayesian approach to determine which perspective is best supported by the results. We used dataset composed of 338 vegetation censuses from eleven river basins in continental Portugal. We observed that changes in Sorensen indices were associated with network distance, flow connection, Strahler order difference and precipitation difference but to different degrees. The results suggest that community similarity changes are associated with environmental and neutral factors, supporting the continuum hypothesis.

Worldwide COVID-19 spreading explained: traveling numbers as a primary driver for the pandemic.

The spread of SARS-CoV-2 and the distribution of cases worldwide followed no clear biogeographic, climatic, or cultural trend. Conversely, the internationally busiest cities in all countries tended to be the hardest hit, suggesting a basic, mathematically neutral pattern of the new coronavirus early dissemination. We tested whether the number of flight passengers per time and the number of international frontiers could explain the number of cases of COVID-19 worldwide by a stepwise regression. Analysis were taken by 22 May 2020, a period when one would claim that early patterns of the pandemic establishment were still detectable, despite of community transmission in various places. The number of passengers arriving in a country and the number of international borders explained significantly 49% of the variance in the distribution of the number of cases of COVID-19, and number of passengers explained significantly 14.2% of data variance for cases per million inhabitants. Ecological neutral theory may explain a considerable part of the early distribution of SARS-CoV-2 and should be taken into consideration to define preventive international actions before a next pandemic.

Stochastic Spatial Models in Ecology: A Statistical Physics Approach

Ecosystems display a complex spatial organization. Ecologists have long tried to characterize them by looking at how different measures of biodiversity change across spatial scales. Ecological neutral theory has provided simple predictions accounting for general empirical patterns in communities of competing species. However, while neutral theory in well-mixed ecosystems is mathematically well understood, spatial models still present several open problems, limiting the quantitative understanding of spatial biodiversity. In this review, we discuss the state of the art in spatial neutral theory. We emphasize the connection between spatial ecological models and the physics of non-equilibrium phase transitions and how concepts developed in statistical physics translate in population dynamics, and vice versa. We focus on non-trivial scaling laws arising at the critical dimension D = 2 of spatial neutral models, and their relevance for biological populations inhabiting two-dimensional environments. We conclude by discussing models incorporating non-neutral effects in the form of spatial and temporal disorder, and analyze how their predictions deviate from those of purely neutral theories.

Quantifying the effects of the break up of Pangaea on global terrestrial diversification with neutral theory.

The historic richness of most taxonomic groups increases substantially over geological time. Explanations for this fall broadly into two categories: bias in the fossil record and elevated net rates of diversification in recent periods. For example, the break up of Pangaea and isolation between continents might have increased net diversification rates. In this study, we investigate the effect on terrestrial diversification rates of the increased isolation between land masses brought about by continental drift. We use ecological neutral theory as a means to study geologically complex scenarios tractably. Our models show the effects of simulated geological events that affect all species equally, without the added complexity of further ecological processes. We find that continental drift leads to an increase in diversity only where isolation between continents leads to additional speciation through vicariance, and where higher taxa with very low global diversity are considered. We conclude that continental drift by itself is not sufficient to account for the increase in terrestrial species richness observed in the fossil record.

Predicting community structure in snakes on Eastern Nearctic islands using ecological neutral theory and phylogenetic methods.

Predicting species presence and richness on islands is important for understanding the origins of communities and how likely it is that species will disperse and resist extinction. The equilibrium theory of island biogeography (ETIB) and, as a simple model of sampling abundances, the unified neutral theory of biodiversity (UNTB), predict that in situations where mainland to island migration is high, species-abundance relationships explain the presence of taxa on islands. Thus, more abundant mainland species should have a higher probability of occurring on adjacent islands. In contrast to UNTB, if certain groups have traits that permit them to disperse to islands better than other taxa, then phylogeny may be more predictive of which taxa will occur on islands. Taking surveys of 54 island snake communities in the Eastern Nearctic along with mainland communities that have abundance data for each species, we use phylogenetic assembly methods and UNTB estimates to predict island communities. Species richness is predicted by island area, whereas turnover from the mainland to island communities is random with respect to phylogeny. Community structure appears to be ecologically neutral and abundance on the mainland is the best predictor of presence on islands. With regard to young and proximate islands, where allopatric or cladogenetic speciation is not a factor, we find that simple neutral models following UNTB and ETIB predict the structure of island communities.

Applying ecological models to communities of genetic elements: the case of neutral theory.

A promising recent development in molecular biology involves viewing the genome as a mini-ecosystem, where genetic elements are compared to organisms and the surrounding cellular and genomic structures are regarded as the local environment. Here, we critically evaluate the prospects of ecological neutral theory (ENT), a popular model in ecology, as it applies at the genomic level. This assessment requires an overview of the controversy surrounding neutral models in community ecology. In particular, we discuss the limitations of using ENT both as an explanation of community dynamics and as a null hypothesis. We then analyse a case study in which ENT has been applied to genomic data. Our central finding is that genetic elements do not conform to the requirements of ENT once its assumptions and limitations are made explicit. We further compare this genome-level application of ENT to two other, more familiar approaches in genomics that rely on neutral mechanisms: Kimura's molecular neutral theory and Lynch's mutational-hazard model. Interestingly, this comparison reveals that there are two distinct concepts of neutrality associated with these models, which we dub 'fitness neutrality' and 'competitive neutrality'. This distinction helps to clarify the various roles for neutral models in genomics, for example in explaining the evolution of genome size.

Phanerozoic diversity and neutral theory

AbstractAlthough Phanerozoic increases in the global richness, local richness, and evenness of marine invertebrates are well documented, a common explanation for these patterns has been difficult to identify. Evidence is presented here from marine invertebrate communities that there is a Phanerozoic increase in the fundamental biodiversity number (θ), which describes diversity and relative abundance distributions in neutral ecological theory. If marine ecosystems behave according to the rules of Hubbell’s Neutral Theory of Biodiversity and Biogeography, the Phanerozoic increase inθsuggests three possible mechanisms for the parallel increases in global richness, local richness, and evenness: (1) an increase in the per-individual probability of speciation, (2) an increase in the area occupied by marine metacommunities, and (3) an increase in the density (per-area abundance) of marine organisms. Because speciation rates have declined over time and because there is no clear evidence for an increase in metacommunity area through the Phanerozoic, the most likely of these is an increase in the spatial density of marine invertebrates over the Phanerozoic, an interpretation supported by previous studies of fossil abundance. This, coupled with a Phanerozoic rise in body size, suggests that an increase in primary productivity through time is the primary cause of Phanerozoic increases inθ, global richness, local richness, local evenness, abundance, and body size.

A unified model of species immigration, extinction and abundance on islands

AbstractAimMacArthur and Wilson's theory of island biogeography was revolutionary, and also inspired the more recent unified neutral theory of biodiversity and biogeography. The unified neutral theory has the potential to make predictions about island biogeography that are not well studied. Here we aim to unify the two theories by using an ecological neutral model to study immigration and extinction rates on islands – the cornerstone of MacArthur and Wilson's theory.MethodsWe conduct simulations of a spatially implicit neutral model and measure species abundances, immigration rates and extinction rates. We study the behaviour of the model at dynamic equilibrium and on approach to dynamic equilibrium both from volcanic origin (low initial diversity) and from land bridge origin (high initial diversity). We extend the model to study the effects of clustered immigration and to explicitly account for the distinction between immigration and colonization.ResultsOur model, in accord with the simplest version of MacArthur and Wilson's theory, predicts linear immigration and extinction rates as functions of species richness at dynamic equilibrium. In contrast, the approach to dynamic equilibrium produces rich and unexpected behaviour where immigration and extinction rates are non‐monotonic functions of species richness, at odds with other theory. Once examined, however, this behaviour makes biological sense and results from the influence of the species abundance distribution over immigration and extinction rates. The turnover predicted by our first model appears high, but can be lowered to realistic levels with an alternative model of clustered immigration or by accounting for the difference between the immigration of a new species and its true colonization of the island.Main conclusionsMacArthur and Wilson's theory of island biogeography and ecological neutral theory are different, but there are strong similarities in their assumptions and predictions that should not be overlooked when evaluating them. Our results highlight the importance of species abundances as indicators of immigration and extinction rates; species richness alone is insufficient. In particular, extinction rate and species abundances are unavoidably linked, as rarity usually precedes extinction.

An exactly solvable coarse-grained model for species diversity

We present novel analytical results concerning ecosystem species diversity that stem from a proposed coarse-grained neutral model based on birth–death processes. The relevance of the problem lies in the urgency for understanding and synthesizing both theoretical results from ecological neutral theory and empirical evidence on species diversity preservation. The neutral model of biodiversity deals with ecosystems at the same trophic level, where per capita vital rates are assumed to be species independent. Closed-form analytical solutions for the neutral theory are obtained within a coarse-grained model, where the only input is the species persistence time distribution. Our results pertain to: the probability distribution function of the number of species in the ecosystem, both in transient and in stationary states; the n-point connected time correlation function; and the survival probability, defined as the distribution of time spans to local extinction for a species randomly sampled from the community. Analytical predictions are also tested on empirical data from an estuarine fish ecosystem. We find that emerging properties of the ecosystem are very robust and do not depend on specific details of the model, with implications for biodiversity and conservation biology.

Historical effects on beta diversity and community assembly in Amazonian trees.

We present a unique perspective on the role of historical processes in community assembly by synthesizing analyses of species turnover among communities with environmental data and independent, population genetic-derived estimates of among-community dispersal. We sampled floodplain and terra firme communities of the diverse tree genus Inga (Fabaceae) across a 250-km transect in Amazonian Peru and found patterns of distance-decay in compositional similarity in both habitat types. However, conventional analyses of distance-decay masked a zone of increased species turnover present in the middle of the transect. We estimated past seed dispersal among the same communities by examining geographic plastid DNA variation for eight widespread Inga species and uncovered a population genetic break in the majority of species that is geographically coincident with the zone of increased species turnover. Analyses of these and 12 additional Inga species shared between two communities located on opposite sides of the zone showed that the populations experienced divergence 42,000-612,000 y ago. Our results suggest that the observed distance decay is the result not of environmental gradients or dispersal limitation coupled with ecological drift--as conventionally interpreted under neutral ecological theory--but rather of secondary contact between historically separated communities. Thus, even at this small spatial scale, historical processes seem to significantly impact species' distributions and community assembly. Other documented zones of increased species turnover found in the western Amazon basin or elsewhere may be related to similar historical processes.

Analyzing Tropical Forest Tree Species Abundance Distributions Using a Nonneutral Model and through Approximate Bayesian Inference

The neutral theory of biodiversity challenges the classical niche-based view of ecological communities, where species attributes and environmental conditions jointly determine community composition. Functional equivalence among species, as assumed by neutral ecological theory, has been recurrently falsified, yet many patterns of tropical tree communities appear consistent with neutral predictions. This may mean that neutral theory is a good first-approximation theory or that species abundance data sets contain too little information to reject neutrality. Here we present a simple test of neutrality based on species abundance distributions in ecological communities. Based on this test, we show that deviations from neutrality are more frequent than previously thought in tropical forest trees, especially at small spatial scales. We then develop a nonneutral model that generalizes Hubbell's dispersal-limited neutral model in a simple way by including one additional parameter of frequency dependence. We also develop a statistical method to infer the parameters of this model from empirical data by approximate Bayesian computation. In more than half of the permanent tree plots, we show that our new model fits the data better than does the neutral model. Finally, we discuss whether observed deviations from neutrality may be interpreted as the signature of environmental filtering on tropical tree species abundance distributions.

Do fitness-equalizing tradeoffs lead to neutral communities?

Neutral theory in ecology is aimed at describing communities where species coexist due to similarities rather than the classically posited niche differences. It assumes that all individuals, regardless of species identity, are demographically equivalent. However, Hubbell suggested that neutral theory may describe even niche communities because tradeoffs equalize fitness across species which differ in their traits. In fact, tradeoffs can involve stabilization as well as fitness equalization, and stabilization involves different dynamics and can lead to different community patterns than neutral theory. Yet the important question remains if neutral theory provides a robust picture of all fitness-equalized communities, of which communities with demographic equivalence are one special case. Here, I examine Hubbell’s suggestion for a purely fitness-equalizing interspecific birth–death tradeoff, expanding neutral theory to a theory describing this broader class of fitness-equalized communities. In particular, I use a flexible framework allowing examination of the influence of speciation dynamics. I find that the scaling of speciation rates with birth and death rates, which is poorly known, has large impacts on community structure. In most cases, the departure from the predictions of current neutral models is substantial. This work suggests that demographic and speciation complexities present a challenge to the future development and use of neutral theory in ecology as null model. The framework presented here will provide a starting point for meeting that challenge, and may also be useful in the development of stochastic niche models with speciation dynamics.

How Neutral is Ecology?

Neutral ecological theory comes in two flavors—a two-stage model with space implicit and a spatially explicit version. Reconciliation of the two flavors has proven problematic. Panmixis, an implicit assumption of the two-stage model, is neither realistic for nor supported by tropical forest trees. However, in spatially explicit versions, stochastic species input in local communities is still necessary to retain high species richness. A unified theory of biodiversity must include both stochasticity and relevant ecological mechanisms.

Development, Application and Place of Neutral Theory in Ecology and Biogeography

AbstractClassical ecological theory predicts that ecological communities should only contain as many species as there are resources. Many ecosystems, however, seem to contain many more species than classical theory allows. Understanding this paradox is central to community ecology and biogeography. Niche‐based models consider that differences and trade‐offs between species’ life history traits stabilise species interactions and so allow coexistence. In stark contrast, neutral models assume that individuals at the same trophic level interact identically with conspecifics and heterospecifics (i.e. all species are equivalent), and this equivalence allows coexistence. Despite it seeming unlikely that species are equivalent, neutral models do predict some of the macroscopic properties of ecological communities surprisingly well. Although there are many neutral models, the best‐known neutral model in the context of community ecology is that described by Hubbell (2001) in the Unified Neutral Theory of Biodiversity. We review the development of neutral theory in ecology and biogeography, consider its predictions and how they can be evaluated, and look at how neutral theory may develop in the future. This article focuses on species‐rich plant communities, as they are, for the most part, the test‐bed for the recent development and application of neutral models, but we also consider the application of neutral approaches to other taxonomic groups and ecosystem types.

Using DNA to assess errors in tropical tree identifications: How often are ecologists wrong and when does it matter?

Ecological surveys of tropical tree communities have provided an important source of data to study the forces that generate and maintain tropical diversity. Accurate species identification is central to these studies. Incorrect lumping or splitting of species will distort results, which may in turn affect conclusions. Although ecologists often work with taxonomists, they likely make some identification errors. This is because most trees encountered in the field are not reproductive and must be identified using vegetative characters, while most species descriptions rely on fruit and flower characters. Because every tree has DNA, ecological surveys can incorporate molecular approaches to enhance accuracy. This study reports an extensive ecological and molecular survey of nearly 4000 trees belonging to 55 species in the tree genus Inga (Fabaceae). These trees were sampled in 25 community surveys in the southwestern Amazon. In a process of reciprocal illumination, trees were first identified to species using vegetative characters, and these identifications were revised using phylogenies derived from nuclear and chloroplast DNA sequences.We next evaluated the effects of these revised species counts upon analyses often used to assess ecological neutral theory. The most common morphological identification errors involved incorrectly splitting rare morphological variants of common species and incorrectly lumping geographically segregated, morphologically similar species. Total error rates were significant (6.8–7.6% of all individuals) and had a measurable impact on ecological analyses. The revised identifications increased support for spatially autocorrelated, potentially neutral factors in determining community composition. Nevertheless, the general conclusions of community‐level ecological analyses were robust to misidentifications. Ecological factors, such as soil composition, and potentially neutral factors, such as dispersal limitation, both play important roles in the assembly of Inga communities. In contrast, species‐level analyses of neutrality with respect to habitat were strongly impacted by identification errors. Although this study found errors in morphological identifications, there was also strong evidence that a purely molecular approach to species identification, such as DNA barcoding, would be prone to substantial errors. The greatest accuracy in ecological surveys will be obtained through a synthesis of traditional, morphological and modern, molecular approaches.