James Rosindell

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.

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.

A unified model of island biogeography sheds light on the zone of radiation

Islands acquire species through immigration and speciation. Models of island biogeography should capture both processes; however quantitative island biogeography theory has either neglected speciation or treated it unrealistically. We introduce a model where the dominance of immigration on small and near islands gives way to an increasing role for speciation as island area and isolation increase. We examine the contribution of immigration and speciation to the avifauna of 35 archipelagoes and find, consistent with our model, that the zone of radiation comprises two regions: endemic species diverged from mainland sister-species at intermediate isolation and from insular sister-species at higher levels of isolation. Our model also predicts species-area curves in accord with existing research and makes new predictions about species ages and abundances. We argue that a paucity of data and theory on species abundances on isolated islands highlights the need for island biogeography to be reconnected with mainstream ecology.

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.

OneZoom: A Fractal Explorer for the Tree of Life

An intuitively simple zooming interface offers a visually appealing way to explore very large phylogenetic trees with metadata.

The Neutral—Niche Debate: A Philosophical Perspective

Ecological communities around the world are under threat while a consensus theory of community structure remains elusive. In the last decade ecologists have struggled with two seemingly opposing theories: niche-based theory that explains diversity with species’ differences and the neutral theory of biodiversity that claims that much of the diversity we observe can be explained without explicitly invoking species’ differences. Although ecologists are increasingly attempting to reconcile these two theories, there is still much resistance against the neutral theory of biodiversity. Here we argue that the dispute between the two theories is a classic example of the dichotomy between philosophical perspectives, realism and instrumentalism. Realism is associated with specific, small-scale and detailed explanations, whereas instrumentalism is linked to general, large-scale, but less precise accounts. Recognizing this will help ecologists get both niche-based and neutral theories in perspective as useful tools for understanding biodiversity patterns.

The Spatial Limitations of Current Neutral Models of Biodiversity

The unified neutral theory of biodiversity and biogeography is increasingly accepted as an informative null model of community composition and dynamics. It has successfully produced macro-ecological patterns such as species-area relationships and species abundance distributions. However, the models employed make many unrealistic auxiliary assumptions. For example, the popular spatially implicit version assumes a local plot exchanging migrants with a large panmictic regional source pool. This simple structure allows rigorous testing of its fit to data. In contrast, spatially explicit models assume that offspring disperse only limited distances from their parents, but one cannot as yet test the significance of their fit to data. Here we compare the spatially explicit and the spatially implicit model, fitting the most-used implicit model (with two levels, local and regional) to data simulated by the most-used spatially explicit model (where offspring are distributed about their parent on a grid according to either a radially symmetric Gaussian or a ‘fat-tailed’ distribution). Based on these fits, we express spatially implicit parameters in terms of spatially explicit parameters. This suggests how we may obtain estimates of spatially explicit parameters from spatially implicit ones. The relationship between these parameters, however, makes no intuitive sense. Furthermore, the spatially implicit model usually fits observed species-abundance distributions better than those calculated from the spatially explicit models simulated data. Current spatially explicit neutral models therefore have limited descriptive power. However, our results suggest that a fatter tail of the dispersal kernel seems to improve the fit, suggesting that dispersal kernels with even fatter tails should be studied in future. We conclude that more advanced spatially explicit models and tools to analyze them need to be developed.

Unifying ecology and macroevolution with individual-based theory

A contemporary goal in both ecology and evolutionary biology is to develop theory that transcends the boundary between the two disciplines, to understand phenomena that cannot be explained by either field in isolation. This is challenging because macroevolution typically uses lineage-based models, whereas ecology often focuses on individual organisms. Here, we develop a new parsimonious individual-based theory by adding mild selection to the neutral theory of biodiversity. We show that this model generates realistic phylogenies showing a slowdown in diversification and also improves on the ecological predictions of neutral theory by explaining the occurrence of very common species. Moreover, we find the distribution of individual fitness changes over time, with average fitness increasing at a pace that depends positively on community size. Consequently, large communities tend to produce fitter species than smaller communities. These findings have broad implications beyond biodiversity theory, potentially impacting, for example, invasion biology and paleontology.

Can clade age alone explain the relationship between body size and diversity

One of the most striking patterns observed among animals is that smaller-bodied taxa are generally much more diverse than larger-bodied taxa. This observation seems to be explained by the mere fact that smaller-bodied taxa tend to have an older evolutionary origin and have therefore had more time to diversify. A few studies, based on the prevailing null model of diversification (i.e. the stochastic constant-rate birth–death model), have suggested that this is indeed the correct explanation, and body-size dependence of speciation and extinction rates does not play a role. However, there are several potential shortcomings to these studies: a suboptimal statistical procedure and a relatively narrow range of body sizes in the analysed data. Here, we present a more coherent statistical approach, maximizing the likelihood of the constant-rate birth–death model with allometric scaling of speciation and extinction rates, given data on extant diversity, clade age and average body size in each clade. We applied our method to a dataset compiled from the literature that includes a wide range of Metazoan taxa (range from midges to elephants). We find that the higher diversity among small animals is indeed, partly, caused by higher clade age. However, it is also partly caused by the body-size dependence of speciation and extinction rates. We find that both the speciation rate and extinction rate decrease with body size such that the net diversification rate is close to 0. Even more interestingly, the allometric scaling exponent of speciation and extinction rates is approximately −0.25, which implies that the per generation speciation and extinction rates are independent of body size. This suggests that the observed relationship between diversity and body size pattern can be explained by clade age alone, but only if clade age is measured in generations rather than years. Thus, we argue that the most parsimonious explanation for the observation that smaller-bodied taxa are more diverse is that their evolutionary clock ticks faster.

Integrating ecology into macroevolutionary research.

On 9 March, over 150 biologists gathered in London for the Centre for Ecology and Evolution spring symposium, ‘Integrating Ecology into Macroevolutionary Research’. The event brought together researchers from London-based institutions alongside others from across the UK, Europe and North America for a day of talks. The meeting highlighted methodological advances and recent analyses of exemplar datasets focusing on the exploration of the role of ecological processes in shaping macroevolutionary patterns.