A general expectation for the paradox of coexistence

There are several popular approaches to the goal of finding generalities in ecology. One is essentially top down, searching for generalities across ecological patterns in multiple places and at multiple scales and then attempting to understand the underlying mechanisms (e.g. metabolic scaling theory and allometric approaches). Alternatively, the approach can be bottom up. It may consider multiple models or multiple individual mechanisms and find generalities in the patterns or relationships they predict. 

A great example of generalities from multiple models is in a recent paper published in PNAS (from Sakavara et al. 2018). It relies on, links together, and adds to, our understanding of community assembly and the effects of competition on the distribution of niches in communities. In particular, it adds additional support to the assertion that both combinations of either highly similar or highly divergent species can coexist, across a wide variety of models.

Work published in 2006 by Scheffer and van Nes played an important early role towards a reconciliation of neutral theory and niche-based approaches. They used a Lotka-Volterra model to highlight that communities could assemble with clusters of coexisting, similar species evenly spaced along a niche axis (Figure 1). Neutrality, or at least near-neutrality, could result even when dynamics were determined by niche differences. [Scheffer, van Nes, and Remi Vergnon also provide a nice commentary on the Sakavara et al. paper found here].

Fig. 1: From Scheffer and van Nes, emergent 'lumpiness' in communities.

One possibility is that Scheffer and van Nes's results might be due to the specifics of the L-V model rather than representing a general and biologically realistic expectation. Sakavara et al. address this issue using a mechanistic consumer-resource model in "Lumpy species coexistence arises robustly in fluctuating resource environments". Under this model, originally from Tilman's classic work with algae, coexistence is limited by the number of resources that limit a species' growth. For 2 species, for example, 2 resources must be present that limit species growth, and further the species must experience a tradeoff in their competitive abilities for the 2 resources. Coexistence can occur when each species is limited more by the resource on which it is most competitive (Figure 2). Such a model– in which resources limit coexistence—leads to an expectation that communities will assemble to maximize the dissimilarity of species.

Fig 2. From Sakavara et al. (2017).

Such a result occurs when resources are provided constantly, but in reality the rates of resource supply may well be cyclical or unpredictable. Will community assembly be similar (resulting in patterns of limiting similarity) when resources are variable in their supply? Or will clumps of similar species be able to coexist? Sakavara et al. considered this question using consumer-resource models of competition, where there are two fluctuating limiting resources. They simulated the dynamics of 300 competing species, which were assigned different trait values along a trait gradient. Here the traits were the half-saturation coefficients for the 2 limiting resources: these were related via a tradeoff between the half saturation constants for each resource.

What they found is strikingly similar to the results from Scheffer and van Nes and dissimilar to the the results that emerge when resources are constant. Clumps of coexisting species emerged along the trait axis. When resource fluctuations occurred rapidly, only fairly specialized species survived in these clumps (R* values that were high for either resource 1, or resource 2, rather than intermediate). But when fluctuations were less frequent, clusters of species also survived at intermediate points along the trait axis. However, in all cases the community organized into clumps composed of very similar species that were coexisting (see Figure 3). It appears that this occurs because the fluctuating resources result in the system having non-stationary conditions. That is, similar sets of species can coexist because the system varies between those species' requirements for persistence and growth. 

Fig. 3. "Lumpy species coexistence". The y-axis shows the trait value (here, the R*) of species present under 360 day periodicity of resource supply.  

Using many of the dominant models of competition in ecology, it is clearly possible to explain the coexistence of both similar or dissimilar species. This is true across approaches from the Lotka-Volterra results of Scheffer and van Nes, to Tilman's R* resource competition, to Chessonian coexistence (2000). It provides a unifying expectation upon which further research can build. Perhaps the paradox of the planktons is not really a paradox anymore?

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Reference:
Athanasia Sakavara, George Tsirtsis, Daniel L. Roelke, Rebecca Mancy, and Sofie Spatharis. Lumpy species coexistence arises robustly in fluctuating resource environments. PNAS 2017; published ahead of print December 20, 2017, doi:10.1073/pnas.1705944115

What do we mean when we talk about the niche?

The niche concept is a good example of an idea in ecology that is continually changing. It is probably the most important idea in ecology that no one has yet nailed down. As most histories of the niche mention, the niche has developed from its first mention by Grinnell (in 1917) to Hutchinson’s multi-dimensional niche space, to mechanistic descriptions of resource usage and R*s (from MacArthur’s warblers to Tilman’s algae). Its most recent incarnation can be found in what has been called modern coexistence theory, as first proposed by Peter Chesson in his seminal 2000 paper.

Chesson’s mathematical framework has come to dominate a lot of discussion amongst community ecologists, with good reason. It provides a clear way to understand stable coexistence amongst local populations in terms of their ability to recover from low densities, and further by noting that those low density growth rates are the outcome of two types of processes: those driven by fitness differences and those driven by stabilizing effects that reduce interspecific competition relative to intraspecific competition. Many of the different specific mechanisms of coexistence can be classified in terms of this framework of equalizing and stabilizing effects. “Niche” differences between species in this framework can be defined as those differences that increase negative intraspecific density dependence compared to interspecific effects. If, as a simplistic example, two plant species have different rooting depths and so access different depths of the water table, then this increases competition for water between similar root-depth conspecifics relative to interspecific competition. Thus, this is a niche difference. Extensions on modern niche theory have offered insights into everything from invasion success, restoration, and eco-phylogenetic analyses.

But it seems as though the rise of 'modern coexistence theory' is changing the language that ecologists use to discuss the niche concept. When Thomas Kuhn talks about paradigm shifts, he notes that it is not only theory that changes but also the worldview organized around a given idea. At least amongst community ecologists, it seems as though this had focused the discussion of the niche to an increasingly local scale, particularly in terms of stabilizing and equalizing terms measured as fixed quantities made under homogenous, local conditions. A recognition of the role of spatial and temporal conditions in altering these variables seems less common, compared to the direction of earlier, Hutchinsonian-type discussions of the niche.

Note that this was not Chesson's original definition, since he is explicit that: “The theoretical literature supports the concept that stable coexistence necessarily requires important ecological differences between species that we may think of as distinguishing their niches and that often involve tradeoffs, as discussed above. For the purpose of this review, niche space is conceived as having four axes: resources, predators (and other natural enemies), time, and space.”

On a recent manuscript, an editor commented that the term 'niche processes' shouldn't be used to refer to environmental filtering since (paraphrased) “when ecologists refer to niche processes, they are usually thinking of processes that constrain species’ abundances locally, confer an advantage on rare species...” But is it fair to say that this is the only thing we mean (or should mean) when we discuss niches? I’ve had discussions with other people who’ve had this kind of response – e.g., reviewers asking for simulations to be reframed from niches defined in terms of environmental tolerances to things that fit more clearly into equalizing and stabilizing terms. That is a good description of a stabilizing process, which is termed a 'niche difference' in the modern coexistence literature. But there is still a lot of grey space we have yet to address in terms of how to integrate (e.g.) the effects of the environment (including over larger scales) into local 'niche processes' or stabilizing effects. It's a subtle argument - that we can use the framework established by Chesson, but we should try to do so without dismissing too-quickly the concepts that don't fit easily within it. In addition, elsewhere the niche is still conceptualized in varying ways from comparative evolutionary biologists who talk about niche conservatism and mean the maintenance of ancestral trait values or environmental tolerances; to functional ecologists who may refer to multidimensional differences in trait space; to species distribution modellers who thinks of large-scale environmental correlates or physiological determinants of species’ distributions. 

The niche is probably the most fundamental, yet vaguely–defined and poorly understood idea in ecology. So, formalizing the definition and constraining it is a necessary idea. And modern coexistence theory has provided great deal of insight into local coexistence and thus has allowed for a better understanding of the niche concept. But there is also a need to be careful in how quickly and how much we restrict our discussion of the niche. It's possible to gain both the strengths of modern coexistence theory as well as appreciate its current limitations. Modern coexistence theory isn’t yet complete or sufficient. It’s currently easier to estimate stabilizing and equalizing terms from experimental data in which conditions are controlled and homogenous, and this can inadvertently focus future research and discussion on those types of conditions. Models which consider larger scale processes and the impacts of changing abiotic conditions through space in time exist, but across different literatures, and these need continued synthesis. There is still a need to understand how to most realistically incorporating and understand the complex interactions between multiple species (e.g. Levine et al. 2017). The application of modern coexistence theory to observational data in particular is still limited, and such data is essential when species are slow lived or experimentally unwieldy. Further, when quantities of interest (particularly traits or phylogenetic differences) contribute to both equalizing and stabilizing effects, its still not clear how to partition their contributions meaningfully.

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Experimental macroevolution at microscales

Sometimes I find myself defending the value of microcosms and model organisms for ecological research. Research systems do not always have to involve a perfect mimicry of nature to provide useful information. A new paper in Evolution is a great example of how microcosms provide information that may not be accessible in any other system, making them a valuable tool in ecological research.

For example, macroevolutionary hypotheses are generally only testable using observational data. They suffer from the obvious problem that they generally relate to processes of speciation and extinction that occurred millions of years ago. The exception is the case of short generation, fast evolving microcosms, in which experimental macroevolution is actually possible. Which makes them really cool :-) In a new paper, Jiaqui Tan, Xian Yang and Lin Jiang showing that “Species ecological similarity modulates the importance of colonization history for adaptive radiation”. The question of how ecological factors such as competition and predation impact evolutionary processes such as the rapid diversification of a lineage (adaptive radiation) is an important one, but generally difficult to address (Nuismer & Harmon, 2015; Gillespie, 2004). Species that arrive to a new site will experience particular abiotic and biotic conditions that in turn may alter the likelihood that adaptive radiation will occur. Potentially, arriving early—before competitors are present—could maximize opportunities for usage of niche space and so allow adaptive radiation. Arriving later, once competitors are established, might suppress adaptive radiation.

More realistically, arrival order will interact with resident composition, and so the effects of arriving earlier or later are modified by the identities of the other species present in a site. After all, competitors may use similar resources, and compete less, or have greater resource usage and so compete more. Although hypotheses regarding adaptive radiation are often phrased in terms of a vague ‘niche space’, they might better be phrased in terms of niche differences and fitness differences. Under such a framework, simply having species present or not present at a site does not provide information about the amount of niche overlap. Using coexistence theory, Tan et al. produced a set of hypotheses predicting when adaptive radiation should be expected, given the biotic composition of the site (Figure below). In particular, they predicted that colonization history (order of arrival) would be less important in cases where species present interacted very little. Equally, when species had large fitness differences, they predicted that one species would suppress the other, and the order in which they arrived would be immaterial. ­

From Tan et al. 2017

The authors tested this using a bacterial microcosm with 6 bacterial competitors and a focal species – Pseudomonas fluorescens SBW25. SBW25 is known for its rapid evolution, which can produce genetically distinct phenotypes. Microcosm patches contained 2 species, SBW25 and one competitor species, and their order of arrival was varied. After 12 days, the phenotypic richness of SBW25 was measured in all replicates.

From Tan et al. 2017. Competitor order of arrival in general altered the final phenotypic richness of SBW25.

Both order of arrival and the identity of the competitor did indeed matter as predictors of final phenotypic richness (i.e. adaptive radiation) of SBW25. Further, these two variables interacted to significantly. Arrival order was most important when the 2 species were strong competitors (similar niche and fitness differences), in which case late arrival of SBW25 suppressed its radiation. On the other hand, when species interact weakly, arrival order had little affect on radiation. The effect of different interactions were not entirely simple, but particularly interesting to me was that fitness differences, rather than niche differences, often had important effects (see Figure below). The move away from considering the adaptive radiation hypothesis in terms of niche space, and restating it more precisely, here allowed important insights into the underlying mechanisms. Especially as researchers are developing more complex models of macroevolution, which incorporate factors such as evolution, having this kind of data available to inform them is really important.

Interaction between final phenotype richness and arrival order for B) niche differences and D) fitness differences. S-C refers to arrival of SWB25 first, C-S refers to its later arrival. 

Competition and invasions: evolving perspectives

Guest post by Brechann McGoey.

The field of invasion biology was sparked with the publication of Charles Elton’s book “The Ecology of Invasions by Animals and Plants” (1958). Beginning in the 1980s (Simberloff et al., 2013), there was a rapid growth in research effort, most of which focused on the ecology of invasive species, including their traits and impacts (Lee, 2002). However, the evolutionary causes and consequences of colonization are also critical to our understanding of species invasions (Bacigalupe, 2009; Crawford & Whitney, 2010).

Figure 1- Research on invasive species has increased rapidly (Google ngram viewer). 

The influential book "The Genetics of Colonizing Species" (1965) is an early and important example of efforts to integrate concepts from the fields of genetics, ecology and applied sciences to better understand invasions. The volume covers a vast breadth of topics and its authors include some of the best minds in evolution and ecology of the last century. Many of the ideas raised at the conference were on the cutting edge, and although there are a staggering number of valuable insights in the book, the authors were often contending with a lack of data. In the fifty years since its publication, there has been an explosion of studies on invasion biology, and though there we may sometimes be frustrated by a lack of progress both in theory and management, we are in a much better position to evaluate how the hypotheses and assertions of 1965 stand up in the face of empirical data. 

In his chapter on competition and migration, Dr. Kan-Ichi Sakai sought to outline how evolution and competitive ability would influence plant invasion dynamics. He points out that, in order to become established in a new environment, a colonizer must be able to compete with the native flora. Since the initial population size is small, there is likely selection for genotypes that can exploit the low-density conditions, by growing and reproducing rapidly. We now have data demonstrating responses to this kind of selection, for example, in the cane toad invasion of Australia where individuals near the invasion front have accelerated development and so can reproduce more quickly (Phillips, 2009).  Sakai also raises the concept of trade-offs between migratory and competitive abilities during colonization, an idea that has found support in much more recent models (Burton, Phillips, & Travis, 2010).

Figure 2-Cane toads have increased the rate of their spread. Those on the edge of the rangeare better dispersers and reproduce more quickly.

Sakai argues that the lack of a covariance between fitness and competitiveness will lead to the maintenance of variation in competitive ability, essentially concluding that being a good competitor is not correlated with fitness. Modern invasion biology has veered away from this assumption. The prominent hypothesis of the Evolution of Increased Competitive Ability (EICA) is based on the idea that invasive plants will experience relaxed selection for defensive traits, have more available resources, and evolve to become superior competitors (Blossey & Notzold, 1995). This presupposes a positive covariance between competitive ability and fitness in their new context.

Sakai also asserts that competitive ability is not a heritable trait. This conclusion was perhaps due to a lack of data on the heritability of traits important to competitive interactions, and a somewhat murky definition of "competitive ability", and has since been abandoned (Hühn, 1975). Empirical work since 1965 shows that competitive traits can be heritable, for example in size and allelopathy, and artificial selection of crops can successfully increase competitive ability (Worthington & Reberg-Horton, 2013), demonstrating its heritability. In light of this, invasive populations will often be able to respond to selection and increase their competitiveness in their new habitats, with sometimes devastating consequences for their native competitors.

We now have a plethora of data on competition, migration and invasions, and are able to reject and find support for ideas laid out by Sakai five decades ago. Competition is a crucial interaction in plant invasions, both in determining how resistant a community is to invasion (Keane & Crawley, 2002), and how successful a novel species will be. If we hope to understand invasion processes, we must incorporate evolutionary and ecological perspectives, and recognize how ecological and genetic factors act in concert during the spread of a novel species. Competitive dynamics offer an excellent opportunity to examine how ecology and evolution intersect during colonization.

References

Bacigalupe, L. D. (2009). Biological invasions and phenotypic evolution: a quantitative genetic perspective. Biological Invasions, 11(10), 2243–2250. doi:10.1007/s10530-008-9411-2

Baker, H. G., & Stebbins, G. L. (Eds.). (1965). The Genetics of Colonizing Species. New York: Academic Press.

Blossey, B., & Notzold, R. (1995). Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. Journal of Ecology, 83(5), 887–889.

Burton, O. J., Phillips, B. L., & Travis, J. M. J. (2010). Trade-offs and the evolution of life-histories during range expansion. Ecology Letters, 13(10), 1210–1220. doi:10.1111/j.1461-0248.2010.01505.x

Crawford, K. M., & Whitney, K. D. (2010). Population genetic diversity influences colonization success. Molecular Ecology, 19(6), 1253–1263. doi:10.1111/j.1365-294X.2010.04550.x

Elton, C. (1958). The Ecology of Invasions by Animals and Plants. London: Methuen.

Hühn, M. (1975). Estimation of broad sense heritability in plant populations: an improved method - Springer. Theoretical and Applied Genetics.

Keane, R. M., & Crawley, M. J. (2002). Exotic plant invasions and the enemy release hypothesis. Trends in Ecology & Evolution.

Lee, C. (2002). Evolutionary genetics of invasive species. Trends in Ecology & Evolution.

Phillips, B. L. (2009). The evolution of growth rates on an expanding range edge. Biology Letters, 5(6), 802–804. doi:10.1086/527494

Simberloff, D., Martin, J.-L., Genovesi, P., Maris, V., Wardle, D. A., Aronson, J., et al. (2013). Impacts of biological invasions: What's what and the way forward. Trends in Ecology & Evolution, 28(1), 58–66. doi:10.1016/j.tree.2012.07.013

Worthington, M., & Reberg-Horton, C. (2013). Breeding cereal crops for enhanced weed suppression: Optimizing allelopathy and competitive ability. Journal of Chemical Ecology, 39(2), 213–231. doi:10.1007/s10886-013-0247-6