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.     

Modes of speciation and the neutral theory of biodiversity

Hubbell's neutral theory of biodiversity has generated much debate over the need for niches to explain biodiversity patterns. Discussion of the theory has focused on its neutrality assumption, i.e. the functional equivalence of species in competition and dispersal. Almost no attention has been paid to another critical aspect of the theory, the assumptions on the nature of the speciation process. In the standard version of the neutral theory each individual has a fixed probability to speciate. Hence, the speciation rate of a species is directly proportional to its abundance in the metacommunity. We argue that this assumption is not realistic for most speciation modes because speciation is an emergent property of complex processes at larger spatial and temporal scales and, consequently, speciation rate can either increase or decrease with abundance. Accordingly, the assumption that speciation rate is independent of abundance (each species has a fixed probability to speciate) is a more natural starting point in a neutral theory of biodiversity. Here we present a neutral model based on this assumption and we confront this new model to 20 large data sets of tree communities, expecting the new model to fit the data better than Hubbell's original model. We find, however, that the data sets are much better fitted by Hubbell's original model. This implies that species abundance data can discriminate between different modes of speciation, or, stated otherwise, that the mode of speciation has a large impact on the species abundance distribution. Our model analysis points out new ways to study how biodiversity patterns are shaped by the interplay between evolutionary processes (speciation, extinction) and ecological processes (competition, dispersal).     

Demographic analysis of Hubbell's neutral theory of biodiversity

Hubbell's neutral model is increasingly applied in both theoretical and empirical studies but so far little attention has been paid to the ecological mechanisms that determine species diversity in neutral communities. In this contribution we use a stochastic individual-based Markovian model to provide an explicit derivation of Hubbell's local community model from the fundamental processes of reproduction, mortality, and immigration, and show that such derivation provides important insights on the mechanisms regulating species diversity that cannot be obtained from the original model and its previous extensions. One important insight is that the basic parameters of Hubbell's model, community size (J) and the probability that a dying individual will be replaced by an immigrant (m), cannot be considered independent and that their interdependency leads to a counterintuitive trade-off between community size and species diversity. We further demonstrate that Hubbell's treatment of community size as a free parameter hides fundamental mechanisms that influence species diversity through their effect on the size of the community. For example, while in Hubbell's model immigration can only increase species diversity by promoting colonization rates, the demographic derivation shows that immigration can also promote species diversity by reducing extinction rates. Our demographic derivation also unifies previous contrasting predictions about the effect of reproduction on species diversity by showing that both positive and negative effects are possible, and that the balance between the two effects depends on the size of the community. The demographic derivation also reconciles an apparent contradiction between Hubbell's theory and patch occupancy theory, and integrates three previously proposed mechanisms of species diversity, the More Individuals Hypothesis, the rescue effect, and the dilution effect, within a single, unified framework.     

When and why do non-neutral metacommunities appear neutral?

Hubbell's neutral theory assumes that all species in a community have the same per capita fitness. Despite the overwhelming evidence against this assumption in most communities the neutral theory has often been, though not always, successful at predicting patterns of diversity in nature. I analyze a non-neutral model in order to suggest conditions under which observed species-abundance distributions (SADs) could be expected to resemble neutral distributions. The non-neutral model consists of two guilds of species such that (1) individuals between guilds do not interact, (2) dynamics within guilds follow Hubbell's model and (3) neutral parameters between guilds differ. This two-guild model generates SADs that appear neutral in some cases and clearly non-neutral in other cases. This result suggests that SADs may be more informative about niche structure than previously thought. The two-guild model could be tested in communities composed of fairly well-defined guilds or functional groups.     

A sampling theory for asymmetric communities

We introduce the first analytical model of asymmetric community dynamics to yield Hubbell's neutral theory in the limit of functional equivalence among all species. Our focus centers on an asymmetric extension of Hubbell's local community dynamics, while an analogous extension of Hubbell's metacommunity dynamics is deferred to an appendix. We find that mass-effects may facilitate coexistence in asymmetric local communities and generate unimodal species abundance distributions indistinguishable from those of symmetric communities. Multiple modes, however, only arise from asymmetric processes and provide a strong indication of non-neutral dynamics. Although the exact stationary distributions of fully asymmetric communities must be calculated numerically, we derive approximate sampling distributions for the general case and for nearly neutral communities where symmetry is broken by a single species distinct from all others in ecological fitness and dispersal ability. In the latter case, our approximate distributions are fully normalized, and novel asymptotic expansions of the required hypergeometric functions are provided to make evaluations tractable for large communities. Employing these results in a Bayesian analysis may provide a novel statistical test to assess the consistency of species abundance data with the neutral hypothesis.     

Linking dispersal, immigration and scale in the neutral theory of biodiversity

In the classic spatially implicit formulation of Hubbell's neutral theory of biodiversity a local community receives immigrants from a metacommunity operating on a relatively slow timescale, and dispersal into the local community is governed by an immigration parameter m . A current problem with neutral theory is that m lacks a clear biological interpretation. Here, we derive analytical expressions that relate the immigration parameter m to the geometry of the plot defining the local community and the parameters of a dispersal kernel. Our results facilitate more rigorous and extensive tests of the neutral theory: we conduct a test of neutral theory by comparing estimates of m derived from fits to empirical species abundance distributions to those derived from dispersal kernels and find acceptable correspondence; and we generate a new prediction of neutral theory by investigating how the shapes of species abundance distributions change theoretically as the spatial scale of observation changes. We also discuss how our main analytical results can be used to assess the error in the mean-field approximations associated with spatially implicit formulations of neutral theory.     

The impact of neutrality, niche differentiation and species input on diversity and abundance distributions

We present a spatially-explicit generalization of Hubbell's model of community dynamics in which the assumption of neutrality is relaxed by incorporating dispersal limitation and habitat preference. In simulations, diversity and species abundances were governed by the rate at which new species were introduced (usually called 'speciation') and nearly unaffected by dispersal limitation and habitat preference. Of course, in the absence of species input, diversity is maintained solely by niche differences. We conclude that the success of the neutral model in predicting the abundance distribution has nothing to do with neutrality, but rather with the species-introduction process: when new species enter a community regularly as singletons, the typical J-shaped abundance distribution, with a long tail of rare species, is always observed, whether species differ in habitat preferences or not. We suggest that many communities are indeed driven by the introduction process, accounting for high diversity and rarity, and that species differences may be largely irrelevant for either.     

Neutral theory in community ecology

One of the central goals of community ecology is to understand the forces that maintain species diversity within communities. The traditional niche-assembly theory asserts that species live together in a community only when they differ from one another in resource uses. But this theory has some difficulties in explaining the diversity often observed in specie-rich communities such as tropical forests. As an alternative to the niche theory, Hubbell and other ecologists introduced a neutral model. Hubbell argues that the number of species in a community is controlled by species extinction and immigration or speciation of new species. Assuming that all individuals of all species in a trophically similar com-munity are ecologically equivalent, Hubbell's neutral theory predicts two important statistical distributions. One is the asymptotic log-series distribution for the metacommunities under point mutation speciation, and the other is the zero-sum multinomial distribution for both local communities under dispersal limitation and metacommunities under random fission speciation. Unlike the niche-assembly theory, the neutral theory takes similarity in species and individuals as a starting point for investigating species diversity. Based on the fundamental processes of birth, death, dispersal and spe-ciation, the neutral theory provided the first mechanistic explanation of species abundance distribution commonly observed in natural communities. Since the publication of the neutral theory, there has been much discussion about it, pro and con. In this paper, we summarize recent progress in the assumption, prediction and speciation mode of the neutral theory, including progress in the theory itself, tests about the assumption of the theory, prediction and speciation mode at the metacommunity level. We also suggest that the most important task in the future is to bridge the niche-assembly theory and the neutral theory, and to add species differences to the neutral theory and more stochasticity to the niche theory.     

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.     

群落生态学的中性理论

生物多样性的分布格局和维持机制一直是群落生态学研究的核心问题,其中的关键是物种的共存机制。长期以来,生态位分化的思想在这一研究领域占据着主导地位。然而这一理论在解释热带雨林很高的物种多样性时遇到了困难。而以Hubbell为代表提出的群落中性漂变理论则假定在同一营养级物种构成的群落中不同物种的不同个体在生态学上可看成是完全等同的;物种的多度随机游走,群落中的物种数取决于物种灭绝和物种迁入/新物种形成之间的动态平衡。在这一假定之下,该理论预言了两种统计分布。一种是集合群落在点突变形成新物种的模式下其各个物种相对多度服从对数级数分布,而受扩散限制的局域群落以及按照随机分裂为新物种模式形成的集合群落则服从零和多项式分布。与生态位理论相反,中性理论不以种间生态位差异作为研究群落结构的出发点,而是以物种间在个体水平上的对等性作为前提。该理论第一次从基本生态学过程(出生、死亡、迁移、物种分化)出发,给出了群落物种多度分布的机理性解释,同时其预测的物种多度分布格局在实际群落中也得到了广泛的印证。因此,中性理论自诞生以来便在生态学界引发了极大的反响,也包括一些反对的声音。该文重点综述了关于中性理论的假设、预测和物种形成模式等方面的最新研究进展,包括中性理论本身的发展、关于中性理论的假设和预测的合理性检验以及在集合群落尺度上物种分化模式的讨论;并指出未来发展方向可能是在生态位理论和中性理论之间架起一座桥梁,同时发展包含随机性的群落生态位模型,以及允许种间差异的近中性模型。     

A mathematical synthesis of niche and neutral theories in community ecology

The debate between niche-based and neutral community theories centers around the question of which forces shape predominantly ecological communities. Niche theory attributes a central role to niche differences between species, which generate a difference between the strength of intra- and interspecific interactions. Neutral theory attributes a central role to migration processes and demographic stochasticity. One possibility to bridge these two theories is to combine them in a common mathematical framework. Here we propose a mathematical model that integrates the two perspectives. From a niche-based perspective, our model can be interpreted as a Lotka-Volterra model with symmetric interactions in which we introduce immigration and demographic stochasticity. From a neutral perspective, it can be interpreted as Hubbell's local community model in which we introduce a difference between intra- and interspecific interactions. We investigate the stationary species abundance distribution and other community properties as functions of the interaction coefficient, the immigration rate and the strength of demographic stochasticity.     

A general framework for neutral models of community dynamics

Neutral models of community dynamics are a powerful tool for ecological research, but their applications are currently limited to unrealistically simple types of dynamics and ignore much of the complexity that characterize natural ecosystems. Here, we present a new analytical framework for neutral models that unifies existing models of neutral communities and extends the applicability of existing models to a much wider spectrum of ecological phenomena. The new framework extends the concept of neutrality to fitness equivalence and in spite of its simplicity explains a wide spectrum of empirical patterns of species diversity including positive, negative and unimodal productivity–diversity relationships; gradual and highly delayed declines in species diversity with habitat loss; and positive and negative responses of species diversity to habitat heterogeneity. Surprisingly, the abundance distribution in all of these cases is given by the dispersal limited multinomial (DLM), the abundance distribution in Hubbell's zero-sum model, showing DLM's robustness and demonstrating that it cannot be used to infer the underlying community dynamics. These results support the hypothesis that ecological communities are regulated by a limited set of fundamental mechanisms much simpler than could be expected from their immense complexity.     

Demographic trade-offs determine species abundance and diversity

Aims Much recent theory has focused on the role of neutral processes in assembling communities, but the basic assumption that all species are demographically identical has found little empirical support. Here, we show that the framework of the current neutral theory can easily be generalized to incorporate species differences so long as fitness equivalence among individuals is maintained through trade-offs between birth and death.Methods Our theory development is based on a careful reformulation of the Moran model of metacommunity dynamics in terms of a non-linear one-step stochastic process, which is described by a master equation.Important findings We demonstrate how fitness equalization through demographic trade-offs can generate significant macroecological diversity patterns, leading to a very different interpretation of the relation between Fisher's α and Hubbell's fundamental biodiversity number. Our model shows that equal fitness (not equal demographics) significantly promotes species diversity through strong selective sieving of community membership against high-mortality species, resulting in a positive association between species abundance and per capita death rate. An important implication of demographic trade-off is that it can partly explain the excessively high speciation rates predicted by the neutral theory of the stronger symmetry. Fitness equalization through demographic trade-offs generalizes neutral theory by considering heterospecific demographic difference, thus representing a significant step toward integrating the neutral and niche paradigms of biodiversity.     

Neutral theory in macroecology and population genetics

Current neutral theory in macroecology has many parallels with neutral theory in population genetics, but it also has many distinct features that arise because it focuses mainly on questions at the community level rather than at the population level. Here we highlight the similarities and differences between these two bodies of theories from the aspects of the operational units, definitions of neutrality, basic parameters, driving forces, spatial structure and community assembly rules. Compared with neutral theory in population genetics, whose development spans more than 40 years, neutral theory in ecology, which is only a few years old, is still immature and under-developed. There are many opportunities for major theoretical contributions, some of which can be adopted directly from population genetics, while others will require new theoretical work. We critically discuss these opportunities and theoretical challenges in neutral macroecology, particularly in regard to effective community size, ecological drift, community differentiation and ecological dominance.     

The zero-sum assumption in neutral biodiversity theory

The neutral theory of biodiversity as put forward by Hubbell in his 2001 monograph has received much criticism for its unrealistic simplifying assumptions. These are the assumptions of functional equivalence among different species (neutrality), the assumption of point mutation speciation, and the assumption that resources are continuously saturated, such that constant resource availability implies constant community size (zero-sum assumption). Here we focus on the zero-sum assumption. We present a general theory for calculating the probability of observing a particular species-abundance distribution (sampling formula) and show that zero-sum and non-zero-sum formulations of neutral theory have exactly the same sampling formula when the community is in equilibrium. Moreover, for the non-zero-sum community the sampling formula has this same form, even out of equilibrium. Therefore, the term "zero-sum multinomial (ZSM)" to describe species abundance patterns, as coined by Hubbell [2001. The Unified Neutral Theory of Biodiversity and Biogeography, Princeton University Press, Princeton, NJ], is not really appropriate, as it also applies to non-zero-sum communities. Instead we propose the term "dispersal-limited multinomial (DLM)", thus making explicit one of the most important contributions of neutral community theory, the emphasis on dispersal limitation as a dominant factor in determining species abundances.     

Environmental heterogeneity affects the location of modelled communities along the niche–neutrality continuum

The continuum hypothesis has been proposed as a means to reconcile the contradiction between the niche and neutral theories. While past research has shown that species richness affects the location of communities along the niche–neutrality continuum, there may be extrinsic forces at play as well. We used a spatially explicit continuum model to quantify the effects of environmental heterogeneity, comprising abundance distribution and spatial configuration of resources, on the degree of community neutrality. We found that both components of heterogeneity affect the degree of community neutrality and that species'' dispersal characteristics affect the neutrality–heterogeneity relationship. Narrower resource abundance distributions decrease neutrality, while spatial configuration, which is manifested by spatial aggregation of resources, decreases neutrality at higher aggregation levels. In general, the degree of community neutrality was affected by complex interactions among spatial configuration of resources, their abundance distributions and the dispersal characteristics of species in the community. Our results highlight the important yet overlooked role of the environment in dictating the location of communities along the hypothesized niche–neutrality continuum.     

How dispersal limitation shapes species-body size distributions in local communities

A critical but poorly understood pattern in macroecology is the often unimodal species-body size distribution (also known as body size-diversity relationship) in a local community (embedded in a much larger regional species pool). Purely neutral community models that assume functional equivalence among species are incapable of explaining this pattern because body size is the key determinant of functional differences between species. Several niche-based explanations have been offered, but none of them is completely satisfactory. Here we develop a simple model that unites a neutral community model with niche-based theory to explain the relationship. In the model, species of similar size are assumed to belong to the same size guild. Within a size guild, all individuals are equivalent in their competition for resources, sensu Hubbell's neutral community model; they have the same speciation rate and dispersal capacities. Between size guilds, however, the total number of individuals, the speciation rate, and the dispersal capacities differ, but using known allometric scaling laws for these properties, we can describe the differences between size guilds. Our model predicts that species richness reaches an optimum at an intermediate body size, in agreement with observations. The optimum at intermediate body size is basically the result of a trade-off between, on the one hand, allometric scaling laws for the number of individuals and the speciation rate that decrease with body size and, on the other hand, the scaling law for active dispersal that increases with body size.     

Neutral theory and the species abundance distribution: recent developments and prospects for unifying niche and neutral perspectives

Published in 2001, The Unified Neutral Theory of Biodiversity and Biogeography (UNTB) emphasizes the importance of stochastic processes in ecological community structure, and has challenged the traditional niche‐based view of ecology. While neutral models have since been applied to a broad range of ecological and macroecological phenomena, the majority of research relating to neutral theory has focused exclusively on the species abundance distribution (SAD). Here, we synthesize the large body of work on neutral theory in the context of the species abundance distribution, with a particular focus on integrating ideas from neutral theory with traditional niche theory. First, we summarize the basic tenets of neutral theory; both in general and in the context of SADs. Second, we explore the issues associated with neutral theory and the SAD, such as complications with fitting and model comparison, the underlying assumptions of neutral models, and the difficultly of linking pattern to process. Third, we highlight the advances in understanding of SADs that have resulted from neutral theory and models. Finally, we focus consideration on recent developments aimed at unifying neutral‐ and niche‐based approaches to ecology, with a particular emphasis on what this means for SAD theory, embracing, for instance, ideas of emergent neutrality and stochastic niche theory. We put forward the argument that the prospect of the unification of niche and neutral perspectives represents one of the most promising future avenues of neutral theory research.     

Community differentiation on landscapes: drift, migration and speciation

Theories of the differentiation of ecological communities on landscapes have typically not considered evolutionary dynamics. Here we analytically study the expected differentiation among local communities in a large metacommunity, undergoing speciation, ecological drift and intercommunity dispersal, in the context of neutral theory. We demonstrate that heterogeneity in species diversity and abundance arises among communities when local communities are small and intercommunity migration is infrequent. We propose a new measure to describe community differentiation, defined as the average correlation or the average probability (C_st) that two randomly sampled individuals of the same species within local communities are from the same ancestor. The effects of driving forces (migration, mutation, and ecological drift) are incorporated into the two-level hierarchical community structure in a finite island model of neutral communities. Community differentiation can increase the effective metacommunity size or the Hubbell's fundamental species diversity in the metacommunity by a factor (1−C_st)⁻¹. Significant community differentiation arises when C_st≠0. Intercommunity migration promotes species diversity in local communities but reduce species diversity in the metacommunity. In either the finite or infinite island case, one can estimate the number of intercommunity migrants by using multiple local community datasets when the speciation is negligible in the neutral local communities, or by using the metacommunity dataset when the speciation is included in the local neutral communities. These results highlight the significance of the evolutionary mechanisms in generating heterogeneous communities in the absence of complicated ecological processes on large landscapes.