Rampal S. Etienne

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.

Diversity-dependence brings molecular phylogenies closer to agreement with the fossil record

The branching times of molecular phylogenies allow us to infer speciation and extinction dynamics even when fossils are absent. Troublingly, phylogenetic approaches usually return estimates of zero extinction, conflicting with fossil evidence. Phylogenies and fossils do agree, however, that there are often limits to diversity. Here, we present a general approach to evaluate the likelihood of a phylogeny under a model that accommodates diversity-dependence and extinction. We find, by likelihood maximization, that extinction is estimated most precisely if the rate of increase in the number of lineages in the phylogeny saturates towards the present or first decreases and then increases. We demonstrate the utility and limits of our approach by applying it to the phylogenies for two cases where a fossil record exists (Cetacea and Cenozoic macroperforate planktonic foraminifera) and to three radiations lacking fossil evidence (Dendroica, Plethodon and Heliconius). We propose that the diversity-dependence model with extinction be used as the standard model for macro-evolutionary dynamics because of its biological realism and flexibility.

The case for ecological neutral theory

Ecological neutral theory has elicited strong opinions in recent years. Here, we review these opinions and strip away some unfortunate problems with semantics to reveal three major underlying questions. Only one of these relates to neutral theory and the importance of ecological drift, whereas the others involve the link between pattern and process, the tradeoff between simplicity and complexity in modeling, and the role of stochasticity and drift in ecology. We explain how neutral theory cannot be simultaneously used both as a null hypothesis and as an approximation. However, we also show how neutral theory always has a valuable use in one of these two roles, even though the real world is not neutral.

Experimental evidence for a phylogenetic Janzen–Connell effect in a subtropical forest

Observational evidence increasingly suggests that the Janzen-Connell effect extends beyond the species boundary. However, this has not been confirmed experimentally. Herein, we present both observational and experimental evidence for a phylogenetic Janzen-Connell effect. In a subtropical forest in Guangdong province, China, we observed that co-occurring tree species are less phylogenetically related than expected. The inhibition effects of neighbouring trees on seedling survival decreased with increasing phylogenetic distance between them. In a shade-house experiment, we studied seedling survival of eight species on soil collected close to Castanopsis fissa relative to their survival on soil close to their own adult trees, and found that this relative survival rate increased with phylogenetic distance from C. fissa. This phylogenetic signal disappeared when seedlings were planted in fungicide-treated soil. Our results clearly support negative effects of phylogenetically similar neighbouring trees on seedling survival and suggest that these effects are caused by associated host-specific fungal pathogens.

Interactions between macroparasites and microparasites drive infection patterns in free-ranging African buffalo

Epidemiological studies typically focus on single-parasite systems, although most hosts harbor multiple parasite species; thus, the potential impacts of co-infection on disease dynamics are only beginning to be recognized. Interactions between macroparasites, such as gastrointestinal nematodes, and microparasites causing diseases like TB, AIDS, and malaria are particularly interesting because co-infection may favor transmission and progression of these important diseases. Here we present evidence for strong interactions between gastrointestinal worms and bovine tuberculosis (TB) in free-ranging African buffalo (Syncerus caffer). TB and worms are negatively associated at the population, among-herd, and within-herd scales, and this association is not solely the result of demographic heterogeneities in infection. Combining data from 1362 buffalo with simple mechanistic models, we find that both accelerated mortality of co-infected individuals and TB transmission heterogeneity caused by trade-offs in immunity to the two types of parasites likely contribute to observed infection patterns. This study is one of the first to examine the relevance of within-host immunological trade-offs for understanding parasite distribution patterns in natural populations.

A dispersal-limited sampling theory for species and alleles

The importance of dispersal for biodiversity has long been recognized. However, it was never advertised as vigorously as Stephen Hubbell did in the context of his neutral community theory. After his book appeared in 2001, several scientists have sought and found analytical expressions for the effect of dispersal limitation on community composition, still in the neutral context. This has been done along two relatively independent lines of research that have a different mathematical approach and focus on different, yet related, types of results. Here, we study both types in a new framework that makes use of the sampling nature of the theory. We present sampling distributions that contain binomial or hypergeometric sampling on the one hand, and dispersal limitation on the other, and thus views dispersal limitation as ubiquitous as sampling effects. Further, we express the results of one line of research in terms of the other and vice versa, using the concept of subsamples. A consequence of our findings is that metacommunity size does not independently affect the outcome of neutral models in contrast to a previous assertion (Ecol. Lett., 7, 2004, p. 904) based on an incorrect formula (Phys. Rev. E, 68, 2003, p. 061902, eqns 11-14). Our framework provides the basis for development of a dispersal-limited non-neutral community theory and applies in population genetics as well, where alleles and mutation play the roles of species and speciation respectively.

Hidden Consequences of Living in a Wormy World : Nematode-Induced Immune Suppression Facilitates Tuberculosis Invasion in African Buffalo

Most hosts are infected with multiple parasites, and responses of the immune system to co‐occurring parasites may influence disease spread. Helminth infection can bias the host immune response toward a T‐helper type 2 (Th2) over a type 1 (Th1) response, impairing the host’s ability to control concurrent intracellular microparasite infections and potentially modifying disease dynamics. In humans, immune‐mediated interactions between helminths and microparasites can alter host susceptibility to diseases such as HIV, tuberculosis (TB), and malaria. However, the extent to which similar processes operate in natural animal populations and influence disease spread remains unknown. We used cross‐sectional, experimental, and genetic studies to show that gastrointestinal nematode infection alters immunity to intracellular microparasites in free‐ranging African buffalo (Syncerus caffer). Buffalo that were more resistant to nematode infection had weaker Th1 responses, there was significant genotypic variation in nematode resistance, and anthelminthic treatment enhanced Th1 immunity. Using a disease dynamic model parameterized with empirical data, we found that nematode‐induced immune suppression can facilitate the invasion of bovine TB in buffalo. In the absence of nematodes, TB failed to invade the system, illustrating the critical role nematodes may play in disease establishment. Our results suggest that helminths, by influencing the likelihood of microparasite invasion, may influence patterns of disease emergence in the wild.

Prolonging the past counteracts the pull of the present : Protracted speciation can explain observed slowdowns in diversification

Abstract Phylogenetic trees show a remarkable slowdown in the increase of number of lineages towards the present, a phenomenon which cannot be explained by the standard birth–death model of diversification with constant speciation and extinction rates. The birth–death model instead predicts a constant or accelerating increase in the number of lineages, which has been called the pull of the present. The observed slowdown has been attributed to nonconstancy of the speciation and extinction rates due to some form of diversity dependence (i.e., species-level density dependence), but the mechanisms underlying this are still unclear. Here, we propose an alternative explanation based on the simple concept that speciation takes time to complete. We show that this idea of “protracted” speciation can be incorporated in the standard birth–death model of diversification. The protracted birth–death model predicts a realistic slowdown in the rate of increase of number of lineages in the phylogeny and provides a compelling fit to four bird phylogenies with realistic parameter values. Thus, the effect of recognizing the generally accepted fact that speciation is not an instantaneous event is significant; even if it cannot account for all the observed patterns, it certainly contributes substantially and should therefore be incorporated into future studies.

Testing the metabolic theory of ecology

The metabolic theory of ecology (MTE) predicts the effects of body size and temperature on metabolism through considerations of vascular distribution networks and biochemical kinetics. MTE has also been extended to characterise processes from cellular to global levels. MTE has generated both enthusiasm and controversy across a broad range of research areas. However, most efforts that claim to validate or invalidate MTE have focused on testing predictions. We argue that critical evaluation of MTE also requires strong tests of both its theoretical foundations and simplifying assumptions. To this end, we synthesise available information and find that MTEs original derivations require additional assumptions to obtain the full scope of attendant predictions. Moreover, although some of MTEs simplifying assumptions are well supported by data, others are inconsistent with empirical tests and even more remain untested. Further, although many predictions are empirically supported on average, work remains to explain the often large variability in data. We suggest that greater effort be focused on evaluating MTEs underlying theory and simplifying assumptions to help delineate the scope of MTE, generate new theory and shed light on fundamental aspects of biological form and function.

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.