Another round in Diamond vs. Simberloff: revisiting the checkerboard pattern debate

Edward F. Connor, Michael D. Collins, and Daniel Simberloff. 2013. "The Chequered History of Checkerboard Distributions." Ecology. http://dx.doi.org/10.1890/12-1471.1.

One of the most vociferous recent debates in community ecology started in the 1970s between Jared Diamond and Dan Simberloff (and colleagues) regarding whether 'checkerboard patterns' of bird distributions provided evidence for interspecific competition. This was an early and particularly heated example of the pattern versus process debate that continues in various forms today. Diamond (1975) proposed that the distribution of birds in the Bismark Archipelago, and particularly the fact that some pairs of bird species did not co-occur on the same islands (producing a checkerboard pattern), was evidence that competition between species limited their distributions. The issue with using this checkerboard pattern as evidence of competition, which Connor and Simberloff (1979) subsequently pointed out, was that a null model was necessary to determine whether it was actually different from random patterns of apparent non-independence between species pairs. Further, other mechanisms (different habitat requirements, speciation, dispersal limitations) could also produce non-independence between species pairs. The original debate may have died down, but the methodology for null models of communities suggested by Connor and Simberloff has greatly influenced modern ecological methods, and continues to be debated and modified to this day.

The original null model of bird distributions in the Bismark Archipelago involved a binary community matrix (rows represent islands, columns represent species) with 0s and 1s representing species presences or absences. Hence, all the 1s in a row represent the species present on the island. The original null model approach involved randomly shuffling the 0s and 1s, maintaining island richness (row sums) and species range sizes (column sums). The authors of a new paper in Ecology admit that the original null models didn’t accurately capture what Diamond meant by a "checkerboard pattern". This is interesting in part because two of the authors (E.F. Connor and Dan Simberloff) lead the debate against Diamond and introduced the binary matrix approach for generating null expectations. So there is a little bit of a ‘mea culpa’ here. The authors note that earlier null models captured patterns of non-overlap between species' distributions but didn’t differentiate between non-overlap between species with overlapping ranges compared to non-overlap between species which simply occurred on sets of geographically distant islands (referred to here as 'regional allopatry'). The original binary matrix approach didn’t consider spatial proximity of species ranges.

With this fact in mind, the authors re-analyzed checkerboard patterns in the Bismark Archipelago, but in such a way as to control for regional allopatry. True checkerboarding was defined as: “a congeneric or within-guild pair with exclusive distribution, co-occurrence in at least one island group, and geographic ranges that overlap more or significantly more than expected under an hypothesis of pairwise independence”. This definition appears closer to Jared Diamond's original definition and so a null model that captures this is probably a better test of the original hypothesis. The authors looked at the overlap of convex hulls defining species’ ranges and when randomizing the binary matrix, added the further restriction that species could occur only within the island groups where they were actually found (instead of being randomly shuffled through any island, as before).

Even with these clarified and more precise null models, the results remain consistent. True checkerboarding appears to rarely occur compared to chance. Of course, this doesn't mean that competition is not important, but “Rather, in echoing what we said many years ago, one can only conclude that, if they do compete, competition does not strongly affect their patterns of distribution among islands.” More generally, the endurance of this particular debate says a lot about the longstanding tension in ecology over the value and wealth of information captured by ecological patterns, and the limitations and caveats that come with such data. There is also a subtle message about the limitations of null models: they are often treated as a magic wand for dealing with observed patterns, but null models are limited by our own understanding (or ignorance) of the processes at play and our interpretation of their meaning. 

Why pattern-based hypotheses fail ecology: the rise and fall of ecological character displacement

Yoel E. Stuart, Jonathan B. Losos, Ecological character displacement: glass half full or half empty?, Trends in Ecology & Evolution, Available online 26 March 2013

Just as ecology is beginning to refocus on integrating evolutionary dynamics and community ecology, a paper from Yoel Stuart and Jonathan Losos (2013) suggests that perhaps the best-known eco-evolutionary hypothesis - Ecological Character Displacement (ECD) – needs to be demoted in popularity. They review the existing evidence for ECD and in the process illustrate the rather typical path that research into pattern-based hypotheses seems to be taking.

ECD developed during that period of ecology when competition was at the forefront of ecological thought. During the 1950s-1960s, Connell, Hutchinson and McArthur produced their influential ideas about competitive coexistence. At the same time, Brown and Wilson (1956) first described ecological character displacement. ECD is defined as involving first, competition for limited resources; second, in response, selection for resource partitioning which drives populations to diverge in resource use. Ecological competition drives adaptive evolution in resource usage – either resulting in exaggerated divergence in sympatry or trait overdispersion. ECD fell in line with a competition-biased worldview, integrated ecology and evolution, and so quickly became entrenched: the ubiquity of trait differences between sympatric species seemed to support its predictions. Pfennig and Pfennig (2012) go so far as to say ‘Character displacement...plays a key, and often decisive, role in generating and maintaining biodiversity.’

One problem was that tests of ECD tended to make it a self-fulfilling prophecy. Differences in resource usage are expected when coexisting species compete; therefore if differences in resource usage are observed, competition is assumed to be the cause. In the ideal test, divergent sympatric species would be found experimentally to compete, and ECD could be used to explain the proximal cause of divergence. But the argument was also made that when divergent sympatric species were not found to compete, this was also evidence of ECD, since “ghosts of competition past” could have lead to complete divergence such that competition no longer occurred. This made it rather difficult to disprove ECD.

There was pushback in the 1970s against these problems, but interestingly, ECD didn’t fall out of favour. A familiar pattern took form: initial ecstatic support, followed by critical papers, which were in turn rebutted by new experimental studies. Theoretical models both supported or rebutted the hypothesis depending on the assumptions involved. In response the large literature, several influential reviews were written (Schluter (2000), Dayan and Simberloff (2005)) that appeared to suggest at least partial support for the ECD from existing data. Rather than dimming interest in ECD, debate kept it relevant for 40+ years. And continued relevance translated to the image of ECD as a longstanding (hence important) idea. Stuart and Losos carry out a new evaluation of the existing evidence for ECD using Schluter and McPhail’s (1992) ‘6 criteria’, using both the papers from the two previous reviews and more recent studies. Their results suggest that strong evidence for ECD is nearly non-existent, with only 5% of all 144 studies meeting all 6 criteria. (Note: this isn't equivalent to suggesting that ECD is nearly non-existent, just that currently support is limited. There's a good discussion as to some of the possible reasons that ECD has been rarely observed, in the paper).

From Stuart and Losos (2013). Fraction of cases from Schluter 2000, Dayan and Simberloff 2005, and this study that meet either 4 or all 6 of the criteria for ECD.

The authors note that there are many explanations for this finding of weak support: the study of evolution in nature is difficult, particularly given the dearth of long term studies. The 6 criteria are very difficult to fulfill. But they also make an important, much more general point: character displacement patterns can result from multiple processes that are not competition, so patterns on their own are not indicative. Patterns that result from legitimate ecological character displacement may not show the predicted trait overdispersion. The story of the rise and fall of ECD is a story with applications to many pattern-driven ecological hypotheses. There are many axiomatic relationships you learn about in introductory courses: productivity-diversity hump shaped relationships, the intermediate disturbance hypothesis, ECD, etc, etc. These have guided hypothesis formation and testing for 40 years and have become entrenched in the literature despite criticism. And similarly, there are recent papers suggesting that long-standing pattern-based hypotheses are actually wrong or at least misguided (e.g. 1, 2, 3, etc). Why? Because pattern-driven hypotheses lack mechanism, usually relying on some sort of common-sense description of a relationship. The truth is that the same pattern may result from multiple processes. Further, a single process can produce multiple patterns. So a pattern means very little without the appropriate context.

So have we wasted 40 years of time, energy and resources jousting at windmills? Probably not, data and knowledge are arrived at in many ways. And observing patterns is important - it is the source of information from natural systems we use to develop hypotheses. But it is hopeful that this is a period where ecology is recognizing that pattern-based hypotheses (and particularly the focus on patterns as proof for these hypotheses) ask the right questions but focus on the wrong answers.

Long-term studies of Darwin's finches have provided strong evidence for ECD.

Ecological interactions and evolutionary relatedness: contrary effects of conserved niches

Over the past several years a multitude of papers linking patterns of evolutionary relatedness to community structure and species coexistence. Much of this work has looked at co-occurrence patterns and looked for non-random patterns of relatedness. The key explanations of patterns has been that communities comprised of more distantly-related species is thought to be structured by competitive interactions, excluding close relatives. Alternatively, communities comprised of species that are closely related, are thought to share some key feature that allows them to persist in a particular set of environmental conditions or stress. This whole area of research is completely predicated on close relatives having more similar niche requirements then two distant relatives. This predication is seldom tested.In a recent paper in the Proceedings of the National Academy of Science, Jean Burns and Sharon Strauss examine the ecological similarity among 32 plant species and tested if evolutionary relationships offered insight into these similarities. The ecological aspects they examined were germination and early survival rates as well as interaction strengths among species. To assess how these were influenced by evolutionary relatedness, they planted each species in the presence of one of four other species varying in time since divergence from a common ancestor, creating a gradient of relatedness for each species. They found that germination and early survival decreased with increasing evolutionary distance. This surprising result means that species germinating near close relatives do better early on then if they are near distant relatives. The explanation could be that they share many of their biotic and abiotic requirements, and these conserved traits influence early success.

Conversely, when they examined interaction strengths over a longer period (measured as relative individual biomass with and without a competitor), they found that negative interactions were stronger among close relatives.

These two results reveal how evolutionary history can offer insight into ecological interactions, and that the mutually exclusive models of competitive exclusion versus environmental filtering do not capture the full and subtle influence of conserved ecologies. Evolutionarily conserved traits can explain both correlated environmental responses and competitive interactions.

Burns, J., & Strauss, S. (2011). More closely related species are more ecologically similar in an experimental test Proceedings of the National Academy of Sciences, 108 (13), 5302-5307 DOI: 10.1073/pnas.1013003108

Reinterpreting phylogenetic patterns in communities

Examining the phylogenetic structure of a community in order to understand patterns of community assembly has become an increasingly popular approach. A quick web search of “community”, “phylogenetics”, and “ecology” finds several hundred papers, most written in the last ten years.

Eco-phylogeneticists examine how patterns of evolutionary relatedness within communities may reflect the processes structuring those communities. In particular, a commonly tested hypothesis is the competition-relatedness hypothesis, which suggests that more closely-related species having more similar niches and therefore stronger competitive interactions, making coexistence between them less likely. As a result, if competition is important, communities may exhibit phylogenetic overdispersion, with species being less related on average than if drawn randomly from the regional species pool. The contrasting pattern, phylogenetic clustering, where species tend to be more closely related than expected, is often interpreted as being the result of strong environmental filtering, such that only a closely related group of species, best adapted to that environment, surviving in the community.

Evidence for the competition-relatedness hypothesis has been mixed, and since most tests of this hypothesis focus on patterns in observed data, conclusions about the underlying mechanism driving community phylogenetic patterns are rarely testable, and yet widely made.

In Mayfield and Levine (2010, Ecology Letters), the authors critique the current ecological justification for the competition-relatedness hypothesis, noting that it does not agree with a more current view of the processes driving species coexistence. As established by Chesson (2000, Annual Review of Ecology and Systematics), coexistence can involve both stabilizing forces (niche differences between species), and equalizing forces (fitness differences between species). In a simplistic example, plants using different soil types (niche differences) may coexist, while plants with similar high growth rates may exclude those species with lower growth rates (fitness differences). The final community should reflect the interplay of both these processes.

The implication of this view of species coexistence is that there is no preconceived phylogenetic pattern which should reflect competition: if species with the highest heights are competitively superior and exclude other species (coexistence driven by fitness differences), and height is a phylogenetically conserved trait, the community will appear to be phylogenetically clustered. Traditionally, a clustered pattern would not be considered to indicate the effects of competition. In fact, Mayfield and Levine show that the expected phylogenetic pattern depends entirely on whether niche and/or fitness differences are important and/or related to phylogenetic distance.

This suggest that conclusions in past studies may need to be reinterpreted. It also adds to the list of assumptions about evolutionary relatedness and ecological function which need to be tested: for example, how do niche and fitness differences tend to change through time? Do they tend to be conserved among closely related species? Does one or the other tend to dominate as a driver of coexistence in different systems? If nothing else, we need to be careful about making generalizations which don’t account for the differing evolutionary history, geographical location, and ecological setting that communities experience, when interpreting observed patterns in those communities.

Competitive coexistence, it's all about individuals.

Understanding how species coexist has been the raison d'etre for many ecologists over the past 100 years. The quest to understand and explain why so many species coexist together has really been a journey of shifting narratives. The major road stops on this journey have included searching for niche differences among species -from single resources to multidimensional niches, elevating the role for non-equilibrial dynamics -namely disturbances, and assessing the possibility that species actually differ little and diversity patterns follow neutral process. Along this entire journey, researchers (especially theoreticians) have reminded the larger community that that coexistence is a product of the balance between interactions among species (interspecific) and interactions among individuals within species (intraspecific). Despite this occasional reminder, ecologists have largely searched for mechanisms dictating the strength of interspecific interactions.

Image used under Flickr creative commons license, taken by Tinken

In order for two species to coexist, intraspecific competition must be stronger than interspecific -so sayeth classic models of competition. While people have consistently looked for niche differences that reduce interspecific competition, no one has really assessed the strength of intraspecific competition. Until now that is. In a recent paper in Science, Jim Clark examines intra- vs interspecific interactions from data following individual tree performances, across multiple species, for up to 18 years. This data set included annual growth and reproduction, resulting in 226,000 observations across 22,000 trees in 33 species!

His question was actually quite simple -what is the strength of intraspecific interactions relative to interspecific ones? There are two alternatives. First, that intraspecific competition is higher, meaning that among species differences only need to be small for coexistence to occur; or secondly, that intraspecific competition is lower, requiring greater species niche differences for coexistence. To answer this he looked at correlations in growth and fecundity between individuals either belonging to the same or different species, living in proximity to one another. He took a strong positive correlation as evidence for strong competition and a negative or weak correlation as evidence for resource or temporal niche partitioning. What he found was that individuals within species were much more likely to show correlated responses to fluctuating environments, than individuals among species.

This paper represents persuasive evidence that within-species competition is generally extremely high, meaning that to satisfy the inequality leading to coexistence: intra > inter, subtle niche differences can be sufficient. These findings should spur a new era of theoretical predictions and empirical tests as our collective journey to understanding coexistence continues.

Clark, J. (2010). Individuals and the Variation Needed for High Species Diversity in Forest Trees Science, 327 (5969), 1129-1132 DOI: 10.1126/science.1183506

Parasite competition enhances host survival

Contracting a parasite is bad. But is getting colonized by multiple parasitic species worse? This is an interesting and important question. The host is a resource, which can support a limited number of parasitic individuals, and so how does competition affect parasitic species and host mortality?
This was the premise of a recent paper by Oliver Balmer and colleagues, studying trypanosome infection of mice hosts. They engineered two transgeneic strains of the protozoan parasite, Trypanosoma brucei (African sleeping sickness), to fluoresce different colors in order to assess infections. They infected mice with each strain separately and together and measured host survival and parasite density.

They found that when both strains were present, they competitively suppressed each other and that the level of suppression depended on the initial density of each strain. One of the strains was more virulent than the other, and infection by both strains reduced mortality by 15% compared to infection by the virulent strain only. This is due to the suppression of the virulent strain by the low virulent strain.

The authors argue that strain source and intraspecific genetic diversity can have an important effect on host mortality. I would also argue that understanding interspecific interactions and within-host niche differences, would also be critical.

What a cool use of molecular technology to test basic hypotheses about disease ecology.

Balmer, O., Stearns, S., Schötzau, A., & Brun, R. (2009). Intraspecific competition between co-infecting parasite strains enhances host survival in African trypanosomes Ecology, 90 (12), 3367-3378 DOI: 10.1890/08-2291.1

Taking below-ground processes seriously: plant coexistence and soil depth

Some of the earliest ecologists, like Eugen Warming and Christen Raunkiaer, were enthralled with the minutia of the differences in plant life forms and how these differences determined where plants lived. They realized that differences in plant growth forms corresponded to how different plants made their way in the world. Since this early era, understanding the mechanisms of plant competition is one of the most widely-studied aspects of ecology. This is such an important aspect of ecology because understanding plant coexistence allows us to understand what controls productivity in the basal trophic level for most terrestrial food webs. There are a plethora of plausible mechanisms for how plants are able to coexist, and most involve above-ground partitioning strategies (such as different leaf shapes) or phenological differences (such as germination or bolting timing). Yet, below-ground interactions among plants as a way to understand competition and coexistence have been making a strong resurgence in the literature lately. This resurgence has been driven by new hypotheses and technologies.In what is probably the best hypothesis test of the role for below-ground niche partitioning, Mathew Dornbush and Brian Wilsey reveal how soil depth can affect coexistence. They seeded 36 tallgrass prairie species into plot that were either shallow, medium or deep soiled, and asked if species richness and diversity were affected after 3 years. They found that species richness significantly increased with increased soil depth, revealing that deeper soils likely had greater niche opportunities for species. Not only did deeper soils harbor greater richness, but compositions were non-random subsets. The species inhabiting shallow soils were a subset of medium soils, and medium a subset of deep. This means that increasing depth opened new niche opportunities, unique from the ones for shallow soils.

This study is the first field-based experiment of soil depth and coexistence, that I know of and the results are compelling. Plant species are segregating below-ground niches, and perhaps we look for other partitioning strategies for species that inhabit the same soil depth.

Dornbush, M., & Wilsey, B. (2009). Experimental manipulation of soil depth alters species richness and co-occurrence in restored tallgrass prairie Journal of Ecology DOI: 10.1111/j.1365-2745.2009.01605.x

Other notable recent papers on below-ground processes:

Bartelheimer, M., Gowing, D., & Silvertown, J. (2009). Explaining hydrological niches: the decisive role of below-ground competition in two closely related species Journal of Ecology DOI: 10.1111/j.1365-2745.2009.01598.x

Cramer, M., van Cauter, A., & Bond, W. (2009). Growth of N-fixing African savanna species is constrained by below-ground competition with grass Journal of Ecology DOI: 10.1111/j.1365-2745.2009.01594.x

Meier, C., Keyserling, K., & Bowman, W. (2009). Fine root inputs to soil reduce growth of a neighbouring plant via distinct mechanisms dependent on root carbon chemistry Journal of Ecology, 97 (5), 941-949 DOI: 10.1111/j.1365-2745.2009.01537.x

Functional traits and trade-offs explain phytoplankton community structure

After attending the presentation by Elena Litchman at the ASLO Aquatic Science Meeting in Nice three weeks ago I came across this paper. Although it was published already two years ago, this works need to be highlighted! Marine phytoplankton is important. It contributes approximately 50% to world primary productivity. Among other factors phytoplankton communities are structured by competition for limiting nutrients (mainly for nitrate and ammonia) in the ocean. Litchman et al. base their paper on the presumption that phytoplankton organisms can achieve higher competitive ability (Tilman’s R*) by different strategies. That is, the organisms can either increase their maximum nutrient uptake and/or growth rate or they decrease the minimum cell quota, the half saturation constant for nutrient uptake and/or their mortality. Litchman et al. tested if they can find constraints and trade-offs on the evolution of better competitive abilities (lower R*) in major phytoplankton groups. Specifically they asked if there is a positive relationship between maximum growth rate and R* which would show a gleaner-opportunist trade-off.
The authors show positive relationships between measurements for growth and nitrate uptake which can constrain the evolution on competitive ability. Indeed major groups of phytoplankton group along these trade-off curves. Whereas coccolithophores e.g. show low nitrate uptake rates and low half-saturation constants, diatoms and dinoflagelates show the opposite nitrate uptake strategy with high uptake rates and high half-saturation constants. A gleaner-opportunist trade-off, i.e. a positive correlation between maximum growth rates and R*which would result in a super species, could not be found across major groups but within the diatoms. The paper gives more results about trait differences among taxonomic groups and allometric scaling relationships. Trade-offs and different strategies in nutrient uptake are discussed in a very concise way either from a mechanistic physiological view as well as from the evolutionary history perspective.


Elena Litchman, Christopher A. Klausmeier, Oscar M. Schofield and Paul G. Falkowski (2009) The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level. Ecology Letters. DOI: 10.1111/j.1461-0248.2007.01117.x