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.     

Landscape and ecological genomics

Landscape genomics is the modern version of landscape genetics, a discipline that arose approximately 10 years ago as a combination of population genetics, landscape ecology, and spatial statistics. It studies the effects of landscape variables on gene flow and other microevolutionary processes that determine genetic connectivity and variations in populations. In contrast to population genetics, it operates at the level of individual specimens rather than at the level of population samples. Another important difference between landscape genetics and genomics and population genetics is that, in the former, the analysis of gene flow and local adaptations takes quantitative account of landforms and features of the matrix, i.e., hostile spaces that separate species habitats. Landscape genomics is a part of population ecogenomics, which, along with community genomics, is a major part of ecological genomics. One of the principal purposes of landscape genomics is the identification and differentiation of various genome-wide and locus-specific effects. The approaches and computation tools developed for combined analysis of genomic and landscape variables make it possible to detect adaptation-related genome fragments, which facilitates the planning of conservation efforts and the prediction of species’ fate in response to expected changes in the environment.     

Characterizing the post‐recolonization of Antechinus flavipes and its genetic implications in a production forest landscape

Production landscapes, where activities such as timber harvesting, grazing, and resource extraction take place, have considerably reduced the extent of natural habitats. The ecological restoration of these landscapes is, in many cases, the best remaining option to protect biodiversity. However, it is unclear whether restoration designed to avert biodiversity loss in restored landscapes can also maintain genetic diversity in recolonizing faunal populations. We employed core concepts in the field of population genetics to address questions of genetic diversity and gene flow in recolonizing faunal populations, using a small and vagile marsupial (Antechinus flavipes) inhabiting a mined landscape under restoration. We did not detect a disruption of gene flow that led to genetic substructuring, suggesting adequate levels of gene flow across the landscape. Parameters of neutral genetic diversity were high in groups of individuals sampled in both restored and unmined sites. Our results are encouraging as they indicate that ecological restoration has the potential to not just increase available habitat, but also to maintain genetic diversity. However, there is evidence that past anthropogenic disturbances affected the genetics of the population at the regional level. Although restoration at the local level may seem to be successful, it is necessary to manage populations at larger spatial scales than where restoration is conducted, and over long temporal scales, if genetic diversity is to be maintained in restored landscapes. The field of population genetics is an underused tool in ecological restoration yet can provide important insights into how well restoration achieves its goals.     

Understanding ecological change across large spatial,temporal and taxonomic scales: integrating data and methods in light of theory

The difficulty of integrating multiple theories, data and methods has slowed progress towards making unified inferences of ecological change generalizable across large spatial, temporal and taxonomic scales. However, recent progress towards a theoretical synthesis now provides a guiding framework for organizing and integrating all primary data and methods for spatiotemporal assemblage‐level inference in ecology. In this paper, we describe how recent theoretical developments can provide an organizing paradigm for linking advances in data collection and methodological frameworks across disparate ecological sub‐disciplines and across large spatial and temporal scales. First, we summarize the set of fundamental processes that determine change in multispecies assemblages across spatial and temporal scales by reviewing recent theoretical syntheses of community ecology. Second, we review recent advances in data and methods across the main sub‐disciplines concerned with ecological inference across large spatial, temporal and taxonomic scales, and organize them based on the primary fundamental processes they include, rather than the spatiotemporal scale of their inferences. Finally, we highlight how iteratively focusing on only one fundamental process at a time, but combining all relevant spatiotemporal data and methods, may reduce the conceptual challenges to integration among ecological sub‐disciplines. Moreover, we discuss a number of avenues for decreasing the practical barriers to integration among data and methods. We aim to reconcile the recent convergence of decades of thinking in community ecology and macroecology theory with the rapid progress in spatiotemporal approaches for assemblage‐level inference, at a time where a robust understanding of spatiotemporal change in ecological assemblages is more crucial than ever to conserve biodiversity.     

Mechanisms in macroecology: AWOL or purloined letter? Towards a pragmatic view of mechanism

Ecologists often believe the discovery of mechanism to be the central goal of scientific research. While many macroecologists have inherited this view, to date they have been much more efficient at producing patterns than identifying their underlying processes. We discuss several possible attitudes for macroecologists to adopt in this context while also arguing that in fact macroecology already has many mechanisms that are ignored. We briefly describe six of these: central limit theorem, fractals, random sampling and placement, neutral theory (and descendents), concordance of forces, and maximum entropy. We explore why these mechanisms are overlooked and discuss whether they should be. We conclude that macroecology needs to take a more pragmatic, less ideological approach to mechanism. We apply this viewpoint to the recent controversy over maximum entropy and suggest that maximum entropy needs to be viewed more pragmatically and less ideologically.     

Forward from the crossroads of ecology and evolution

Community genetics is a synthesis of community ecology and evolutionary biology. It examines how genetic variation within a species affects interactions among species to change ecological community structure and diversity. The use of community genetics approaches has greatly expanded in recent years and the evidence for ecological effects of genetic diversity is growing. The goal of current community genetics research is to determine the circumstances in which, and the mechanisms by which community genetic effects occur and is the focus of the papers in this special issue. We bring a new group of researchers into the community genetics fold. Using a mixture of empirical research, literature reviews and theoretical development, we introduce novel concepts and methods that we hope will enable us to develop community genetics into the future.     

Neutral theory and community ecology

I review the mathematical and biological aspects of Hubbell's (2001) neutral theory of species abundance for ecological communities, and clarify its historical connections with closely related approaches in population genetics. A selective overview of the empirical evidence for and against this theory is provided, with a special emphasis on tropical plant communities. The neutral theory predicts many of the basic patterns of biodiversity, confirming its heuristic power. The strict assumption of equivalence that defines neutrality, equivalence among individuals, finds little empirical support in general. However, a weaker assumption holds for stable communities, the equivalence of average fitness among species. One reason for the surprising success of the neutral theory is that all the theories of species coexistence satisfying the fitness equivalence assumption, including many theories of niche differentiation, generate exactly the same patterns as the neutral theory. Hubbell's neutral theory represents an important synthesis and a much needed demonstration of the pivotal role of intraspecific variability in ecology. Further improvements should lead to an explicit linking to niche‐based processes. This research programme will depend crucially on forthcoming theoretical and empirical achievements.     

Time-dependent solutions of the spatially implicit neutral model of biodiversity

Previous research into the neutral theory of biodiversity has focused mainly on equilibrium solutions rather than time-dependent solutions. Understanding the time-dependent solutions is essential for applying neutral theory to ecosystems in which time-dependent processes, such as succession and invasion, are driving the dynamics. Time-dependent solutions also facilitate tests against data that are stronger than those based on static equilibrium patterns. Here I investigate the time-dependent solutions of the classic spatially implicit neutral model, in which a small local community is coupled to a much larger metacommunity through immigration. I present explicit general formulas for the eigenvalues, left eigenvectors and right eigenvectors of the models’s transition matrix. The time-dependent solutions can then be expressed in terms of these eigenvalues and eigenvectors. Some of these results are translated directly from existing results for the classic Moran model of population genetics (the Moran model is equivalent to the spatially implicit neutral model after a reparameterization); others of the results are new. I demonstrate that the asymptotic time-dependent solution corresponding to just these first two eigenvectors can be a good approximation to the full time-dependent solution. I also demonstrate the feasibility of a partial eigendecomposition of the transition matrix, which facilitates direct application of the results to a biologically relevant example in which a newly invading species is initially present in the metacommunity but absent from the local community.     

The what,how and why of doing macroecology

Macroecology is a growing and important subdiscipline of ecology, but it is becoming increasingly diffuse, without an organizing principle that is widely agreed upon. I highlight two main current views of macroecology: as the study of large‐scale systems and as the study of emergent systems. I trace the history of both these views through the writings of the founders of macroecology. I also highlight the transmutation principle that identifies serious limitations to the study of large‐scale systems with reductionist approaches. And I suggest that much of the underlying goal of macroecology is the pursuit of general principles and the escape from contingency. I highlight that there are many intertwined aspects of macroecology, with a number of resulting implications. I propose that returning to a focus on studying assemblages of a large number of particles is a helpful view. I propose defining macroecology as “the study at the aggregate level of aggregate ecological entities made up of large numbers of particles for the purposes of pursuing generality”.     

植物群落构建机制研究进展

群落构建研究对于解释物种共存和物种多样性的维持是至关重要的,因此一直是生态学研究的中心论题。尽管近年来关于生态位和中性理论的验证研究已经取得了显著的成果,但对于局域群落构建机制的认识仍存在很大争议。随着统计和理论上的进步使得用功能性状和群落谱系结构解释群落构建机制变为可能,主要是通过验证共存物种的性状和谱系距离分布模式来实现。然而,谱系和功能性状不能相互替代,多种生物和非生物因子同时控制着群落构建,基于中性理论的扩散限制、基于生态位的环境过滤和竞争排斥等多个过程可能同时影响着群落的构建。所以,综合考虑多种方法和影响因素探讨植物群落的构建机制,对于预测和解释植被对干扰的响应,理解生物多样性维持机制有重要意义。试图在简要回顾群落构建理论及研究方法发展的基础上,梳理其最新研究进展,并探讨整合功能性状及群落谱系结构的研究方法,解释群落构建和物种多样性维持机制的可能途径。在结合功能性状和谱系结构研究群落构建时,除了考虑空间尺度、环境因子、植被类型外,还应该关注时间尺度、选择性状的种类和数量、性状的种内变异、以及人为干扰等因素对群落构建的影响。     

Coalescence 2.0: a multiple branching of recent theoretical developments and their applications

Population genetics theory has laid the foundations for genomic analyses including the recent burst in genome scans for selection and statistical inference of past demographic events in many prokaryote, animal and plant species. Identifying SNPs under natural selection and underpinning species adaptation relies on disentangling the respective contribution of random processes (mutation, drift, migration) from that of selection on nucleotide variability. Most theory and statistical tests have been developed using the Kingman coalescent theory based on the Wright‐Fisher population model. However, these theoretical models rely on biological and life history assumptions which may be violated in many prokaryote, fungal, animal or plant species. Recent theoretical developments of the so‐called multiple merger coalescent models are reviewed here (Λ‐coalescent, beta‐coalescent, Bolthausen‐Sznitman, Ξ‐coalescent). We explain how these new models take into account various pervasive ecological and biological characteristics, life history traits or life cycles which were not accounted in previous theories such as (i) the skew in offspring production typical of marine species, (ii) fast adapting microparasites (virus, bacteria and fungi) exhibiting large variation in population sizes during epidemics, (iii) the peculiar life cycles of fungi and bacteria alternating sexual and asexual cycles and (iv) the high rates of extinction‐recolonization in spatially structured populations. We finally discuss the relevance of multiple merger models for the detection of SNPs under selection in these species, for population genomics of very large sample size and advocate to potentially examine the conclusion of previous population genetics studies.     

Eco-evolutionary maintenance of diversity in fluctuating environments

Growing evidence suggests that temporally fluctuating environments are important in maintaining variation both within and between species. To date, however, studies of genetic variation within a population have been largely conducted by evolutionary biologists (particularly population geneticists), while population and community ecologists have concentrated more on diversity at the species level. Despite considerable conceptual overlap, the commonalities and differences of these two alternative paradigms have yet to come under close scrutiny. Here, we review theoretical and empirical studies in population genetics and community ecology focusing on the ‘temporal storage effect’ and synthesise theories of diversity maintenance across different levels of biological organisation. Drawing on Chesson's coexistence theory, we explain how temporally fluctuating environments promote the maintenance of genetic variation and species diversity. We propose a further synthesis of the two disciplines by comparing models employing traditional frequency-dependent dynamics and those adopting density-dependent dynamics. We then address how temporal fluctuations promote genetic and species diversity simultaneously via rapid evolution and eco-evolutionary dynamics. Comparing and synthesising ecological and evolutionary approaches will accelerate our understanding of diversity maintenance in nature.     

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.     

A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation

The detection of adaptive loci in the genome is essential as it gives the possibility of understanding what proportion of a genome or which genes are being shaped by natural selection. Several statistical methods have been developed which make use of molecular data to reveal genomic regions under selection. In this paper, we propose an approach to address this issue from the environmental angle, in order to complement results obtained by population genetics. We introduce a new method to detect signatures of natural selection based on the application of spatial analysis, with the contribution of geographical information systems (GIS), environmental variables and molecular data. Multiple univariate logistic regressions were carried out to test for association between allelic frequencies at marker loci and environmental variables. This spatial analysis method (SAM) is similar to current population genomics approaches since it is designed to scan hundreds of markers to assess a putative association with hundreds of environmental variables. Here, by application to studies of pine weevils and breeds of sheep we demonstrate a strong correspondence between SAM results and those obtained using population genetics approaches. Statistical signals were found that associate loci with environmental parameters, and these loci behave atypically in comparison with the theoretical distribution for neutral loci. The contribution of this new tool is not only to permit the identification of loci under selection but also to establish hypotheses about ecological factors that could exert the selection pressure responsible. In the future, such an approach may accelerate the process of hunting for functional genes at the population level.     

Transmission ratio distortion: review of concept and implications for genetic association studies

Transmission ratio distortion (TRD) occurs when one of the two alleles from either parent is preferentially transmitted to the offspring. This leads to a statistical departure from the Mendelian law of inheritance, which states that each of the two parental alleles is transmitted to offspring with a probability of 0.5. A number of mechanisms are thought to induce TRD such as meiotic drive, gametic competition, and embryo lethality. TRD has been extensively studied in animals, but the prevalence of TRD in humans remains largely unknown. Nevertheless, understanding the TRD phenomenon and taking it into consideration in many aspects of human genetics has potential benefits that have not been sufficiently emphasized in the current literature. In this review, we discuss the importance of TRD in three distinct but related fields of genetics: developmental genetics which studies the genetic abnormalities in zygotic and embryonic development, statistical genetics/genetic epidemiology which utilizes population study designs and statistical models to interpret the role of genes in human health, and population genetics which is concerned with genetic diversity in populations in an evolutionary context. From the perspective of developmental genetics, studying TRD leads to the identification of the processes and mechanisms for differential survival observed in embryos. As a result, it is a genetic force which affects allele frequency at the population, as well as, at the organismal level. Therefore, it has implications on genetic diversity of the population over time. From the perspective of genetic epidemiology, the TRD influence on a marker locus is a confounding factor which has to be adequately dealt with to correctly interpret linkage or association study results. These aspects are developed in this review. In addition to these theoretical notions, a brief summary of the empirical evidence of the TRD phenomenon in human and mouse studies is provided. The objective of our paper is to show the potentially important role of TRD in many areas of genetics, and to create an incentive for future research.     

Microbiology of the phyllosphere: a playground for testing ecological concepts

Many concepts and theories in ecology are highly debated, because it is often difficult to design decisive tests with sufficient replicates. Examples include biodiversity theories, succession concepts, invasion theories, coexistence theories, and concepts of life history strategies. Microbiological tests of ecological concepts are rapidly accumulating, but have yet to tap into their full potential to complement traditional macroecological theories. Taking the example of microbial communities on leaf surfaces (i.e. the phyllosphere), we show that most explorations of ecological concepts in this field of microbiology focus on autecology and population ecology, while community ecology remains understudied. Notable exceptions are first tests of the island biogeography theory and of biodiversity theories. Here, the phyllosphere provides the unique opportunity to set up replicated experiments, potentially moving fields such as biogeography, macroecology, and landscape ecology beyond theoretical and observational evidence. Future approaches should take advantage of the great range of spatial scales offered by the leaf surface by iteratively linking laboratory experiments with spatial simulation models.     

Hubbell's fundamental biodiversity parameter and the Simpson diversity index

Central to Hubbell's neutral theory of biodiversity is a universal, dimensionless fundamental biodiversity parameter that is the product of community size and speciation rate. One of the most important discoveries of Hubbell's theory is that the species‐abundance distribution and the species–area relationship of the neutral metacommunity is completely determined by this fundamental biodiversity parameter, although the diversity patterns of the local community are collectively determined by the biodiversity parameter and migration. Using the relative abundance of species and following the concept of heterozygosity of population genetics, here we developed an analytical relationship between this biodiversity parameter and the well‐known Simpson diversity index. This relationship helps bridge the evolutionary aspect of biodiversity to the ecological and statistical aspect of the diversity. The relationship between these two parameters suggests that diversity patterns of the metacommunity can also be equally described by the Simpson index. This relationship provides an alternative approach to interpret and estimate the fundamental biodiversity parameter for the metacommunity.     

丛枝菌根真菌生物地理学研究进展

丛枝菌根真菌(arbuscular mycorrhizal fungi,AMF)普遍存在于陆地生态系统中,能与绝大多数高等植物形成菌根共生体系。AMF能够促进植物对矿质养分的吸收,增强植物的抗逆能力,在维持生态系统稳定性和生产力中发挥着重要作用。AMF生物地理学主要研究AMF的生物地理分布格局和群落构建机制,对于理解AMF在不同生态系统中的重要性至关重要。总结了AMF生物地理学最新研究进展及研究方法,提出了AMF生物地理学研究理论框架。认为AMF在自然界中并非简单随机分布,宿主植物、地理因子、气候因子和土壤因子共同决定AMF的群落结构,不同尺度下的AMF群落构建符合生态位-中性连续统假说,但在不同尺度下这些驱动因子的相对重要性不同。在全球尺度和区域尺度下,AMF的地理分布格局主要受地理距离和气候因子的影响,中性理论的作用大于生态位理论。随着空间尺度的缩减,宿主植物和环境因子对AMF群落的影响胜过地理距离和扩散限制的作用,生态位理论取代中性理论在AMF群落构建中的主导地位。此外,很多研究发现,同一生境中AMF的群落构建机制并非一成不变,会随环境的变化而发生改变。在未来的研究中,应在野外调查和公共数据库的基础上加强整合分析和数据挖掘工作,从而进一步丰富和完善AMF生物地理学理论。     

The contribution of evening primrose (<Emphasis Type="Italic">Oenothera biennis</Emphasis>) to a modern synthesis of evolutionary ecology

In this review, I consider the contribution that common evening primrose (Oenothera biennis) has made towards integrating the ecology, evolution and genetics of species interactions. Oenothera biennis was among the earliest plant models in genetics and cytogenetics and it played an important role in the modern synthesis of evolutionary biology. More recently, population and ecological genetics approaches have provided insight into the patterns of genetic variation within and between populations, and how a combination of abiotic and biotic factors maintain and select on heritable variation within O. biennis populations. From an ecological perspective, field experiments show that genetic variation and evolution within populations can have cascading effects throughout communities. Plant genotype affects the preference and performance of individual arthropod populations, as well as the composition, biomass, total abundance and diversity of arthropod species on plants. A combination of experiments and simulation models show that natural selection on specific plant traits can drive rapid ecological changes in these same community variables. At the patch level, increasing genotypic diversity leads to a greater abundance and diversity of omnivorous and predaceous arthropods, which is also associated with increased biomass and fecundity of plants in genetically diverse patches. Finally, in questioning whether a community genetics perspective is needed in biology, I review several multifactorial experiments which show that plant genotype often explains as much variation in community variables as other ecological factors typically identified as most important in ecology. As a whole, research in the O. biennis system has contributed to a more complete understanding of the dynamic interplay between ecology, evolution and genetics.