The neutral theory is dead. Long live the neutral theory

The neutral theory of molecular evolution has been instrumental in organizing our thinking about the nature of evolutionary forces shaping variation at the DNA level. More importantly, it has provided empiricists with a strong set of testable predictions and hence, a useful null hypothesis against which to test for the presence of selection. Evidence indicates that the neutral theory cannot explain key features of protein evolution nor patterns of biased codon usage in certain species. Whereas we now have a reasonable model of selection acting on synonymous changes in Drosophila, protein evolution remains poorly understood. Despite limitations in the applicability of the neutral theory, it is likely to remain an integral part of the quest to understand molecular evolution.     

DNA and the neutral theory

The neutral theory claims that the great majority of evolutionary changes at the molecular (DNA) level are caused not by Darwinian selection but by random fixation of selectively neutral or nearly neutral mutants. The theory also asserts that the majority of protein and DNA polymorphisms are selectively neutral and that they are maintained in the species by mutational input balanced by random extinction. In conjunction with diffusion models (the stochastic theory) of gene frequencies in finite populations, it treats these phenomena in quantitative terms based on actual observations. Although the theory has been strongly criticized by the 'selectionists', supporting evidence has accumulated over the years. Particularly, the recent outburst of DNA sequence data lends strong support to the theory both with respect to evolutionary base substitutions and DNA polymorphism, including rapid evolutionary base substitutions in pseudogenes. In addition, the observed pattern of synonymous codon choice can now be readily explained in the framework of this theory. I review these recent findings in the light of the neutral theory.     

Biological invasions and the neutral theory

Aim  The invasion of natural communities by alien species represents a serious threat, but creates opportunities to learn about community functions. Neutral theory proposes that the niche concept may not be needed to explain the assemblage and diversity of natural communities, challenging the classical view of community ecology and generating a lasting debate. Biological invasions, when considered as natural experiments, can be used to contrast some of the predictions of neutral and classic niche theories.
Location  Global.
Methods  We use data from biological invasions as natural experiments to contrast some of the fundamental predictions of neutral theory.
Results  Some emerging patterns did not differ from neutral model expectations (e.g. the relationship between native and exotic species richness, invasibility of resource-rich habitats, and the relationship between propagule release and invasion success). Nevertheless, other patterns (e.g. experimental evidence of the relationship between diversity and susceptibility to invasion, the invasion of communities with a low resource availability, invasiveness related to species traits) contrasted with the predictions that can be inferred from neutral theory.
Main conclusions  Neutral theory correctly highlights the need to include randomness in models of community structure. Biological invasion patterns show that neutral forces are important in structuring natural communities, but the patterns differ from those inferred from a complete neutral model. For biodiversity-conservation purposes, the implications of accepting or not accepting neutral theory as a process-based theory are very important.     

Evolutionary constraints and the neutral theory

Summary The neutral theory of molecular evolution postulates that nucleotide substitutions inherently take place in DNA as a result of point mutations followed by random genetic drift. In the absence of selective constraints, the substitution rate reaches the maximum value set by the mutation rate. The rate in globin pseudogenes is about 5 × 10^–9 substitutions per site per year in mammals. Rates slower than this indicate the presence of constraints imposed by negative (natural) selection, which rejects and discards deleterious mutations.We wish to dedicate this paper to the memory of Professor Jack Lester King     

Speciation and the neutral theory of biodiversity

The neutral theory of biodiversity purports that patterns in the distribution and abundance of species do not depend on adaptive differences between species (i.e. niche differentiation) but solely on random fluctuations in population size (“ecological drift”), along with dispersal and speciation. In this framework, the ultimate driver of biodiversity is speciation. However, the original neutral theory made strongly simplifying assumptions about the mechanisms of speciation, which has led to some clearly unrealistic predictions. In response, several recent studies have combined neutral community models with more elaborate speciation models. These efforts have alleviated some of the problems of the earlier approaches, while confirming the general ability of neutral theory to predict empirical patterns of biodiversity. However, the models also show that the mode of speciation can have a strong impact on relative species abundances. Future work should compare these results to diversity patterns arising from non‐neutral modes of speciation, such as adaptive radiations.     

A neutral theory of biogenesis

The selective Darwinian theory of chemical evolution is critically reviewed and the tentative conclusion is reached that neither the theoretical analyses nor the experiments with phages can really prove it. An alternative proposal is put forth which considers the possibility that the biogenetic process has been driven by stochastic forces, e.g. it took place in the absence of Darwinian selection which, in turn, started only when the first protocells came into existence. The dynamics of the early self-organization of living structures should be understood in terms of self-assembly. The complexification of living matter is thus not represented as a gradual phenomenon but as a series of abrupt and relatively fast transitions consisting in the aggregation of pre-systems which had evolved by their own. The shift towards new and variegated states proposed by the bifurcation theory are not considered particularly relevant for reasons reported in the text, nor is it believed that dissipation can entirely account for the order observed in living cells.     

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.     

The neutral theory in the genomic era

A number of tests have been developed to detect positive selection at the molecular level. These tests are based on DNA polymorphism within and divergence between species. Applications of these tests have revealed a large collection of genes that have evolved under positive selection and some general insights into adaptive evolution. Recently, these tests have been applied on a genomic scale and have provided estimates of the frequency of adaptive substitutions and a critical test of the neutral theory.     

Molecular evolutionary clock and the neutral theory

Summary From the standpoint of the neutral theory of molecular evolution, it is expected that a universally valid and exact molecular evolutionary clock would exist if, for a given molecule, the mutation rate for neutral allelesper year were exactly equal among all organisms at all times. Any deviation from the equality of neutral mutation rate per year makes the molecular clock less exact. Such deviation may be due to two causes: one is the change of the mutation rate per year (such as due to change of generation span), and the other is the alteration of the selective constraint of each molecule (due to change of internal molecular environment). A statistical method was developed to investigate the equality of evolutionary rates among lineages. This was used to analyze protein data to demonstrate that these two causes are actually at work in molecular evolution. It was emphasized that departures from exact clockwise progression of molecular evolution by no means invalidates the neutral theory. It was pointed out that experimental studies should be done to settle the issue of whether the mutation rate for nucleotide change is more constant per year or per generation among organisms whose generation spans are very different.     

Sampling Hubbell's neutral theory of biodiversity

In the context of neutral theories of community ecology, a novel genealogy‐based framework has recently furnished an analytic extension of Ewens’ sampling multivariate abundance distribution, which also applies to a random sample from a local community. Here, instead of taking a multivariate approach, we further develop the sampling theory of Hubbell's neutral spatially implicit theory and derive simple abundance distributions for a random sample both from a local community and a metacommunity. Our result is given in terms of the average number of species with a given abundance in any randomly extracted sample. Contrary to what has been widely assumed, a random sample from a metacommunity is not fully described by the Fisher log‐series, but by a new distribution. This new sample distribution matches the log‐series expectation at high biodiversity values (θ > 1) but clearly departs from it for species‐poor metacommunities (θ < 1). Our theoretical framework should be helpful in the better assessment of diversity and testing of the neutral theory by using abundance data.     

群落构建的中性理论和生态位理论

物种共存和生物多样性维持一直是生态学研究的中心论题。基于物种生态位分化的群落构建理论已经发展了近一个世纪, 但我们对群落构建和生物多样性维持的机理仍然不清楚。近年来, 群落中性理论以其简约性和预测能力成为群落生态学研究的焦点, 但由于其“物种在生态功能上等价”的假设与大量研究结果相悖, 同时对自然群落结构的准确预测也只限于少数的生态系统, 因而饱受质疑。如今, 越来越多的生态学家认为群落构建的生态位理论与中性理论之争的最终归宿应该是二者的整合。 在本文中, 我们在简要回顾生态位理论和群落中性理论发展的基础上, 分析二者之间的主要分歧和互补性, 试图梳理二者整合的途径。我们认为, 尽管中性理论的发展极大地丰富了群落构建理论, 但二者的整合尚处于初级阶段; 群落构建零模型假说、中性—生态位连续体假说、随机生态位假说等都不失为有价值的尝试, 今后需要在其他类型的生态系统中进行实验验证, 以更好地理解确定性过程和随机过程在决定群落构建和生物多样性维持中的作用。     

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).     

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.