Towards a general theory of biodiversity for the Anthropocene

One of Darwin’s most influential ideas was that species originate by the process of natural selection (Darwin, 1859). Though deceivingly simple, it took biologists more than a century to confirm (Coyne and Orr, 2004). One form of natural selection that has now been well documented is ecological speciation (Schluter, 2001). Ecological speciation begins when individuals in a population exhibit variation in their phenotype along an ecological niche axis that corresponds to their use of limiting resources (e.g., space, food, mates) in space or time (Fig. 1A inset, solid red and blue distributions represent individuals that vary in phenotype along a hypothetical niche axis). Examples include Darwin’s finches that vary in beak morphologies that influence the size of seeds they can eat (Grant and Grant, 2006), or body shapes of Stickleback fishes that influence feeding success in the benthic verses pelagic habitat of lakes (Schluter and McPhail, 1992).

When phenotypic variation among individuals occurs along a niche axis with two or more adaptive peaks (Fig. 1A inset, red and blue lines show a ‘fitness landscape’ with adaptive peaks on y-axis), a population can undergo divergent selection, splitting into two populations composed of individuals that each achieve maximal fitness at different values along the niche axis (Schluter, 2001). When divergent selection among individuals becomes sufficiently strong, reproductive isolation can occur, and the population can split into two ecologically distinct species that each use limiting resources (space, food, mates, etc.) differently in space or time.

Models of ecological speciation assume that ecological opportunities lead to niche differences among individuals in a population, and that fitness differences on an adaptive landscape create a selection pressure for individuals to diverge into distinct species. Niche and fitness differences are the same terms now being used by ecologists to explain how species coexist after they evolve. The ecological theory described next suggests that if fitness differences among individuals evolve faster than niche differences, then long-term coexistence of two populations undergoing ecological speciation is not possible (Fig. 1, trajectory to sister taxa A, B). If, however, niche differences evolve faster than fitness differences, coexistence can occur after ecological speciation (Fig. 1, trajectory leading to sister taxa C, D). Thus, the evolutionary trajectory of divergence of niche and fitness differences among individuals determines whether species coexist after reproductive isolation occurs.

Historically, ecologists have assumed that after species evolve, the only thing that can maintain diversity and allow species to coexist is niche differences (Chase and Leibold, 2003). Indeed, common wisdom has long been that evolutionary divergence must cause species to use limiting resources differently in space or time or, if not, competitive exclusion and extinction of the inferior species is inevitable (Gause, 1934). This niche theory of biodiversity was challenged in 2001 when Hubbell (2001) published his Unified Neutral Theory of Biodiversity, arguing that biodiversity is not maintained by niche differences, but rather, by species being so similar to each other that their competitive interactions are ‘neutral’. When interactions are neutral, meaning that competing with an individual of one’s own species has the same consequence as competing with an individual of another species, then species diversity is maintained by a simple balance between speciation rates and random walks to extinction (called ecological ‘drift’ as an analogy to genetic drift).

It has been argued that Neutral Theory is the limiting case of Chesson’s (2000) more general theory of biodiversity (Adler et al., 2007). Chesson showed that most models of species coexistence can be partitioned into two forces that jointly determine whether two species stably coexist. The first force, which Chesson called ‘stabilizing’, represent various forms of traditional niche differences, all of which cause species to limit their own growth rates more strongly than they limit the growth of other species (Fig. 1, x-axis). All niche differences lead to frequency dependent growth such that species have a per capita growth advantage when they are rare in a community. The second force, which Chesson called ‘equalizing’, minimize fitness differences among species (Fig. 1, y-axis). Fitness differences stem from variation in biological traits that would influence the outcome of competition even if species had no niche differences among them (Adler et al., 2007). These traits are the same as those that influence individual reproductive success, such as the per capita population growth rate (Carroll et al., 2011; HilleRisLambers et al., 2012; Narwani et al., 2013).

Chesson showed that for species to stably coexist, niche differences must be larger than fitness differences (Fig. 1, area below 45° line dissecting graph). Thus, if the diverging populations that lead to sister taxa evolve niche differences more rapidly than fitness differences, the ecological species that result should also exhibit long-term, stable coexistence (Fig. 1, trajectories for species C, D and E, F). If, however, diverging populations that lead to sister taxa evolve fitness differences more rapidly than niche differences, the individuals or species that are inferior competitors will go extinct, and diversity will not be maintained over ecological time-frames (Fig. 1, trajectory for species A, B).

Chesson’s theory opens the door for a common set of equations that link concepts in ecological speciation to the ecological maintenance of diversity in competitive communities. Chesson’s theory has also recently been used to show how species coexistence can predict the efficiency of resource use, and production of biomass in communities that control the functioning of ecosystems.

Over the past several decades, there has been a concerted effort to merge concepts in community and ecosystem ecology into common conceptual and theoretical frameworks (Loreau, 2010; Chapin et al., 1997). While community ecology has historically focused on explaining patterns of biodiversity, distributions of populations, and species interactions, ecosystem ecology has focused on explaining the fluxes of energy and the cycles of elements that limit the productivity of life. An increasing number of topics like ‘ecological stoichiometry’ (Sterner and Elser, 2002), ‘ecosystem engineering’ (Jones et al., 1994), ‘trophic cascades’ (Estes et al., 2011) and ‘biodiversity and ecosystem functioning’ (Naeem, 2002), have formed at the intersection of these two fields, emphasizing that the composition and diversity of species in communities not only respond to, but also directly control, fluxes of energy and matter.

A recent sequence of publications have taken theories of species coexistence from community ecology and used these to explain how biodiversity should impact ecosystem-level processes. Tilman et al. (1997) and Loreau (2004) were among first to use traditional models of niche differentiation to show how this force that contributes to coexistence translates mathematically to the sequestration of carbon or nutrients and production of biomass in ecosystems. More recently, Carroll et al. (2011) took a classic model of competition — the MacArthur niche model — and showed how coexistence in this model could be translated into Chesson’s niche differences (ND), and fitness differences (FD). While ND allow diverse communities to capture resources more efficiently and produce more overall biomass, the magnitude of ND required for species to coexist depends on the magnitude of FD that hasten competitive exclusion. As such, the balance of ND and FD that influence competitive coexistence also control the efficiency and productivity of entire communities, with the greatest ecosystem functioning occurring when ND are large relative to FD (Fig. 1, colors from yellow to red indicate increasingly efficient and productive communities).

Use of Chesson’s theory of coexistence to examine how both niche and fitness differences influence ecosystem functioning (Carroll et al., 2011) opens the door for a common set of equations that not only predict the maintenance of biodiversity in ecological time, but also the functional role of biodiversity in controlling the efficiency and productivity of ecosystems.

I have argued that for select modes of evolution (ecological speciation) and certain types of communities (competitive), we are well-within reach of a set of models that simultaneously explain the origin, maintenance, and function of biodiversity. There are, however, still many challenges we face in formalizing these models and extending them to biodiversity more broadly. Therefore, I end with four proposed research foci for the near future:

1. We need to do more to formalize the intersection among disciplines mathematically. While all of the concepts in Fig. 1A, B, and C overlap conceptually, many of the processes that occur at the intersection of the disciplines have yet to be formalized. Models of species coexistence and ecosystem functioning consider niche and fitness differences as static properties of species interactions, but need to model them as dynamic properties that are under selective pressures to evolve along adaptive landscapes. Models of ecological speciation have long considered the evolution of niche differences, but have yet to formalize how fitness differences influence the success of diverging populations when competing for resources. We need to take these overlapping concepts and formalize them in models that explicitly span the interface between evolution, community, and ecosystems ecology.

2. We also need to empirically measure the rates of evolution of both niche and fitness differences, and discern the selective forces that contribute to each. It is common for evolutionary biologists to measure divergence of individuals along niche axes, and for ecologists to measure how niche differences influence competition and coexistence. But we rarely consider how divergence and stable coexistence simultaneously depend on fitness differences that place selective pressures on individuals, and that influence the competitive inequalities among species. Because the origin, maintenance, and function of diversity all depend on the relative balance of ND vs. FD, we need to measure and compare rates of evolution of both forces and determine whether they respond to the same or different selective pressures.

3. We need to move beyond a simple consideration of just competitive communities. Models in Fig. 1 presently focus on competing individuals and species. They ignore other forms of interaction, such as mutualisms that some believe are more common than once thought (Bruno et al., 2003), and trophic interactions like predator-prey relationships that influence both niche and fitness differences of species interacting in food-webs. The steps needed to extend our thinking to other forms of interaction have already begun (Gross, 2008; Chesson and Kuang, 2008), but are only in preliminary phases of development.

4. Lastly, we need to extend these models to predict ecosystem services. The utility of any general theory of biodiversity will ultimately be judged by its ability to predict outputs that have direct human value. Ecologists have, thus far, been too content to measure stocks and fluxes of nutrients and biomass that, at best, have only indirect relevance for society. Few people beyond ecologists care about an ecological function like net primary production — that is, until that particular measurement is placed in a context where it can be translated into value (e.g., economic value of wood production in a forest, recreational value of a coral reef that has been overgrown by algae). Any general theory of biodiversity that can help us navigate and curb biodiversity loss in the Anthropocene will need to translate the function of biodiversity more directly into goods and services that can be quantified with economic valuation. I am hopeful that, five years from now, we can add panel D to Figure 1 representing theory that translates ecological functions to human value.

These four steps are essential short-term goals if we are to predict the causes and consequences of biological change in an era of human domination of the planet. Should we achieve these goals and move closer to a general model of biodiversity, we may yet navigate the Anthropocene in a way that curbs the current tide of extinction, and protects our biological prosperity into the future.

© 2013 Cardinale. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

I thank C. Miller and A. Narwani for comments that improved this article, and the U.S. National Science Foundation’s DIMENSIONS of Biodiversity program for funding (DEB-1046121).