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).     

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.     

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.     

The unified neutral theory of biodiversity and biogeography at age ten

A decade has now passed since Hubbell published The Unified Neutral Theory of Biodiversity and Biogeography. Neutral theory highlights the importance of dispersal limitation, speciation and ecological drift in the natural world and provides quantitative null models for assessing the role of adaptation and natural selection. Significant advances have been made in providing methods for understanding neutral predictions and comparing them with empirical data. In this review, we describe the current state-of-the-art techniques and ideas in neutral theory and how these are of relevance to ecology. The future of neutral theory is promising, but its concepts must be applied more broadly beyond the current focus on species-abundance distributions.     

Relaxing the zero-sum assumption in neutral biodiversity theory

The zero-sum assumption is one of the ingredients of the standard neutral model of biodiversity by Hubbell. It states that the community is saturated all the time, which in this model means that the total number of individuals in the community is constant over time, and therefore introduces a coupling between species abundances. It was shown recently that a neutral model with independent species, and thus without any coupling between species abundances, has the same sampling formula (given a fixed number of individuals in the sample) as the standard model [Etienne, R.S., Alonso, D., McKane, A.J., 2007. The zero-sum assumption in neutral biodiversity theory. J. Theor. Biol. 248, 522-536]. The equilibria of both models are therefore equivalent from a practical point of view. Here we show that this equivalence can be extended to a class of neutral models with density-dependence on the community-level. This result can be interpreted as robustness of the model, i.e. insensitivity of the model to the precise interaction of the species in a neutral community. It can also be interpreted as a lack of resolution, as different mechanisms of interactions between neutral species cannot be distinguished using only a single snapshot of species abundance data.     

Understanding how biodiversity unfolds through time under neutral theory

Theoretical predictions for biodiversity patterns are typically derived under the assumption that ecological systems have reached a dynamic equilibrium. Yet, there is increasing evidence that various aspects of ecological systems, including (but not limited to) species richness, are not at equilibrium. Here, we use simulations to analyse how biodiversity patterns unfold through time. In particular, we focus on the relative time required for various biodiversity patterns (macroecological or phylogenetic) to reach equilibrium. We simulate spatially explicit metacommunities according to the Neutral Theory of Biodiversity (NTB) under three modes of speciation, which differ in how evenly a parent species is split between its two daughter species. We find that species richness stabilizes first, followed by species area relationships (SAR) and finally species abundance distributions (SAD). The difference in timing of equilibrium between these different macroecological patterns is the largest when the split of individuals between sibling species at speciation is the most uneven. Phylogenetic patterns of biodiversity take even longer to stabilize (tens to hundreds of times longer than species richness) so that equilibrium predictions from neutral theory for these patterns are unlikely to be relevant. Our results suggest that it may be unwise to assume that biodiversity patterns are at equilibrium and provide a first step in studying how these patterns unfold through time.     

Slight differences among individuals and the unified neutral theory of biodiversity

The unified neutral theory of biodiversity provides a very simple and counterintuitive explanation of species diversity patterns. By specifying speciation, community size and dispersal, and completely ignoring differences among individual organisms and species, it generates biodiversity patterns that remarkably resemble natural ones. Here I show that adding even slight differences among organisms generates very different patterns and predictions. In large communities with widespread dispersal, heritable differences in viability among individual organisms lead to biodiversity patterns characterised by the overdominance of a single species comprising organisms with relatively high fitness. In communities with local dispersal, the same differences produce rapid community extinction. I conclude that the unified neutral theory is not robust to slight deviations from its most controversial assumption.     

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.     

The role of sex separation in neutral speciation

Neutral speciation mechanisms based on isolation by distance and assortative mating, termed topopatric, has recently been shown to describe the observed patterns of abundance distributions and species–area relationships. Previous works have considered this type of process only in the context of hermaphroditic populations. In this work, we extend a hermaphroditic model of topopatric speciation to populations where individuals are explicitly separated into males and females. We show that for a particular carrying capacity, speciation occurs under similar conditions, but the number of species generated is lower than in the hermaphroditic case. As a consequence, the species–area curve has lower exponents, especially at intermediate scales. Evolution results in fewer species having more abundant populations.     

The merits of neutral theory

Hubbell's neutral theory of biodiversity has challenged the classic niche-based view of ecological community structure. Although there have been many attempts to falsify Hubbell's theory, we argue that falsification should not lead to rejection, because there is more to the theory than neutrality alone. Much of the criticism has focused on the neutrality assumption without full appreciation of other relevant aspects of the theory. Here, we emphasize that neutral theory is also a stochastic theory, a sampling theory and a dispersal-limited theory. These important additional features should be retained in future theoretical developments of community ecology.     

Dispersal, edaphic fidelity and speciation in species-rich Western Australian shrublands: evaluating a neutral model of biodiversity

Over evolutionary time, the number of species in a community reflects the balance between the rate of speciation and the rate of extinction. Over shorter time‐scales local species richness is also affected by how often species move into and out of the local community. These processes are at the heart of Hubbell's ‘unified neutral theory of biodiversity’ ( Hubbell 2001 ). Hubbell's spatially implicit, dispersal‐limited neutral model is the most widely used of the many implementations of neutral theory and it provides an estimate of the rate of speciation in a metacommunity (if metacommunity size is known) and the rate at which species migrate into the local community from the wider metacommunity. Recently, this neutral model has been used to compare rates of speciation and migration in the species‐rich fynbos of South Africa and in neotropical forests. Here we use new analytical methods for estimating the neutral model's parameters to infer speciation and dispersal rates for three sites in species‐rich sclerophyll shrublands (equivalent to fynbos) in Western Australia (WA). Our estimates suggest that WA shrublands are intermediate between fynbos and tropical rainforest in terms of speciation and dispersal. Although a weak test, the model predicts species abundance distributions and species accumulation curves similar to those observed at the three sites. The neutral model's predictions also remain plausible when confronted with independent data describing: (1) known edaphic relationships between sites, (2) estimates of metacommunity species richness and (3) rates of speciation among resprouters and nonsprouters. Two of the site pairs, however, show species turnovers significantly different from those predicted by the spatially implicit form of the neutral model that we use. This suggests that non‐neutral processes, in this case probably edaphic specialisation, are important in the WA shrubland metacommunity. The neutral model predicts similar rates of speciation in resprouter and sprouter taxa, a finding supported by recent molecular phylogenies. Finally, when converted into temporally scaled speciation rates and species longevities, the estimates produced by the neutral model seem implausible. The apparent departure from neutrality in the turnover of species between some sites and the implausible temporal dynamics may be due to the particular model chosen and does not reduce the significance of our other results, which confirm that local dispersal limitation, coupled with broader scale edaphic fidelity, combine to structure this biodiverse metacommunity.     

Conservation: losing biodiversity by reverse speciation

A large fraction of the world's species diversity is of recent evolutionary origin, and has evolved as a by-product of divergent adaptation in heterogeneous environments. Recent research provides a dire warning that homogenizing environments may cause the rapid loss of such species through a reversal of the speciation process.     

Diploid versus haploid models of neutral speciation

Neutral models of speciation based on isolation by distance and assortative mating, termed topopatric, have shown to be successful in describing abundance distributions and species–area relationships. Previous works have considered this type of process in the context of haploid genomes. Here we discuss the implementation of two schemes of dominance to analyze the effects of diploidy: a complete dominance model in which one allele dominates over the other and a perfect codominant model in which heterozygous genotypes give rise to a third phenotype. In the case of complete dominance, we observe that speciation requires stronger spatial inbreeding in comparison to the haploid model. For perfect codominance, instead, speciation demands stronger genetic assortativeness. Nevertheless, once speciation is established, the three models predict the same abundance distributions even at the quantitative level, revealing the robustness of the original mechanism to describe biodiversity features.     

Lineages-through-time plots of neutral models for speciation

Drawing inferences about macroevolutionary processes from phylogenetic trees is a fundamental challenge in evolutionary biology. Understanding stochastic models for speciation is an essential step in solving this challenge. We consider a neutral class of stochastic models for speciation, the constant rate birth-death process. For trees with n extant species - which might be derived from bigger trees via random taxon sampling - we calculate the expected time of the kth speciation event (k=1,...,n-1). Further, for a tree with n extant species, we calculate the density and expectation for the number of lineages at any time between the origin of the process and the present. With the developed methods, expected lineages-through-time (LTT) plots can be drawn analytically. The effect of random taxon sampling on LTT plots is discussed.