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.     

Species diversity in local neutral communities

We extend the neutral theory of macroecology by deriving biodiversity models (relative species abundance and species-area relationships) in a local community-metacommunity system in which the local community is embedded within the metacommunity. We first demonstrate that the local species diversity patterns converge to that of the metacommunity as the size (scale) of the embedded local community increases. This result shows that in continuous landscapes no sharp boundaries dividing the communities at the two scales exist; they are an artificial distinction made by the current spatially implicit neutral theory. Second, we remove the artificial restriction that speciation cannot occur in a local community, even if the effects of local speciation are small. Third, we introduce stochasticity into the immigration rate, previously treated as constant, and demonstrate that local species diversity is a function not only of the mean but also of the variance in immigration rate. High variance in immigration rates reduces species diversity in local communities. Finally, we show that a simple relationship exists between the fundamental diversity parameter of neutral theory and Simpson's index for local communities. Derivation of this relationship extends recent work on diversity indices and provides a means of evaluating the effect of immigration on estimates of the fundamental diversity parameter derived from relative species abundance data on local communities.     

A comment on Hubbell's zero-sum ecological drift model

In Hubbell's model of zero-sum ecological drift, loss of species from communities by stochastic change in population size is balanced by the production of new species by processes analogous to mutation or to the fission of populations. Large regional metacommunities contain so many individuals that species are lost slowly and infrequent speciation events can maintain high diversity. However, validation of Hubbell's model requires that community size, diversity, and species life spans match up, and this is shown to be a problem with both the mutation and fission mechanisms of speciation. In the first case, most species are rare and ephemeral and would fail to be recognized by traditional taxonomic practices. In the second case, species life spans are so long that diversity builds to unrealistic levels. Thus, the problem confronting community drift probably is not the maintenance of diversity but rather its control, requiring such mechanisms as environmental change or occasional evolution of competitively superior species that sweep the metacommunity. Testing the community drift model will require close attention to community size and species life spans.     

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.     

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。     

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.     

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.     

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.     

Dynamics of neutral biodiversity

Hubbell's neutral model has become a major paradigm in ecology. Whereas the steady-state structure is well understood, results about the dynamical aspects of the model are scarce. Here we derive dynamical equations for the Simpson diversity index. Both mean and variance of the diversity are proven to satisfy stable linear system dynamics. We show that in the stationary limit we indeed recover previous results, and we supplement this with numerical simulations to validate the dynamical part of our analytical computations. These findings are especially relevant for experiments in microbial ecology, where the Simpson diversity index can be accurately measured as a function of time.     

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.     

Effects of neutrality and productivity on mammal richness and evolutionary history in Australia

Explaining how heterogeneous spatial patterns of species diversity emerge is one of the most fascinating questions of biogeography. One of the great challenges is revealing the mechanistic effect of environmental variables on diversity. Correlative analyses indicate that productivity is associated with taxonomic, phylogenetic, and functional diversity of communities. Surprisingly, no unifying body of theory have been developed to understand the mechanism by which spatial variation of productivity affects the fundamental processes of biodiversity. Based on widely discussed verbal models in ecology about the effect of productivity on species diversity, we developed a spatially explicit neutral model that incorporates the effect of primary productivity on community size and confronted our model's predictions with observed patterns of species richness and evolutionary history of Australian terrestrial mammals. The imposed restrictions on community size create larger populations in areas of high productivity, which increases community turnover and local speciation, and reduces extinction. The effect of productivity on community size modeled in our study causes higher accumulation of species diversity in productive regions even in the absence of niche‐based processes. However, such a simple model is not capable of reproducing spatial patterns of mammal evolutionary history in Australia, implying that more complex evolutionary mechanisms are involved. Our study demonstrates that the overall patterns of species richness can be directly explained by changes in community sizes along productivity gradients, supporting a major role of processes associated with energetic constraints in shaping diversity patterns.     

A novel genealogical approach to neutral biodiversity theory

Current neutral theory in community ecology views local biodiversity as a result of the interplay between speciation, extinction and immigration. Simulations and a mean‐field approximation have been used to study this neutral theory. As simulations have limitations of convergence and the mean‐field approximation ignores dependencies between species’ abundances when applied to species‐abundance data, there is still no final conclusion whether the neutral theory or the traditional lognormal model describes community structure best. We present a novel analytical framework, based on the genealogy of individuals in the local community, to overcome the problems of previous approaches, and show, using Bayesian statistics, that the lognormal model provides a slightly better fit to the species‐abundance distribution of a much‐discussed tropical tree community. A key feature of our approach is that it shows the tight link between genetic and species diversity, which creates important perspectives to future integration of evolutionary and community ecological theory.     

Generalized aphid population growth models with immigration and cumulative-size dependent dynamics

Mechanistic models in which the per-capita death rate of a population is proportional to cumulative past size have been shown to describe adequately the population size curves for a number of aphid species. Such previous cumulative-sized based models have not included immigration. The inclusion of immigration is suggested biologically as local aphid populations are initiated by migration of winged aphids and as reproduction is temperature-dependent. This paper investigates two models with constant immigration, one with continuous immigration and the other with restricted immigration. Cases of the latter are relatively simple to fit to data. The results from these two immigration models are compared for data sets on the mustard aphid in India.     

Coexistence and invasibility in a two-species competition model with habitat-preference

The outcome of competition among species is influenced by the spatial distribution of species and effects such as demographic stochasticity, immigration fluxes, and the existence of preferred habitats. We introduce an individual-based model describing the competition of two species and incorporating all the above ingredients. We find that the presence of habitat preference—generating spatial niches—strongly stabilizes the coexistence of the two species. Eliminating habitat preference—neutral dynamics—the model generates patterns, such as distribution of population sizes, practically identical to those obtained in the presence of habitat preference, provided an higher immigration rate is considered. Notwithstanding the similarity in the population distribution, we show that invasibility properties depend on habitat preference in a non-trivial way. In particular, the neutral model results more invasible or less invasible depending on whether the comparison is made at equal immigration rate or at equal distribution of population size, respectively. We discuss the relevance of these results for the interpretation of invasibility experiments and the species occupancy of preferred habitats.     

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.     

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.     

Extinction–immigration dynamics lag behind environmental filtering in shaping the composition of tropical dry forests within a changing landscape

The impact of rapid habitat loss and fragmentation on biodiversity is a major issue. However, we still lack an integrative understanding of how these changes influence biodiversity dynamics over time. In this study, we investigate the effects of these changes in terms of both niche-based and neutral dynamics. We hypothesize that habitat loss has delayed effects on neutral immigration–extinction dynamics, while edge effects and environmental heterogeneity in habitat patches have rapid effects on niche-based dynamics. We analyzed taxonomic and functional composition of 100 tree communities in a tropical dry forest landscape of New-Caledonia subject to habitat loss and fragmentation. We designed an original, process-based simulation framework, and performed Approximate Bayesian Computation to infer the influence of niche-based and neutral processes. Then, we performed partial regressions to evaluate the relationships between inferred parameter values of communities and landscape metrics (distance to edge, patch area, and habitat amount around communities), derived from either recent or past (65 yr ago) aerial photographs, while controlling for the effect of soil and topography. We found that landscape structure influences both environmental filtering and immigration. Immigration rate was positively related to past habitat amount surrounding communities. In contrast, environmental filtering was mostly affected by present landscape structure and mainly influenced by edge vicinity and topography. Our results highlight that landscape changes have contrasting spatio-temporal influences on niche-based and neutral assembly dynamics. First, landscape-level habitat loss and community isolation reduce immigration and increase demographic stochasticity, resulting in slow decline of local species diversity and extinction debt. Second, recent edge creation affects environmental filtering, incurring rapid changes in community composition by favoring species with edge-adapted strategies. Our study brings new insights about temporal impacts of landscape changes on biodiversity dynamics. We stress that landscape history critically influences these dynamics and should be taken into account in conservation policies.