How is coevolution significant in community ecology

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Thompson JN. This approach has documented both conflicting [61] , [62] and nonconflicting coevolution [63] — [65]. There is a rich theory describing the evolution of mutualisms [66] , [67].

Theoretical predictions often suggest that mutualistic interactions have the potential to break down into parasitic interactions [47] , [68] , [69] ; this is an extreme form of conflicting interests between species. If mutualism breakdown into parasitism is common, then conflicting coevolution is likely, and this will likely diminish the effects of climate change.

Nonetheless, if mutualistic partners can enforce good behavior of their partners [68] , then nonconflicting coevolution is expected.

For example, the plant Medicago truncatula discriminately rewards the most beneficial mycorrhizal partners with more carbohydrates, and mycorrhizal partners form partnerships only with the roots that provide the most carbohydrates [7]. Thus, each partner constrains the selection pressure of the other to allow only nonconflicting coevolution. If nonconflicting coevolution is frequently imposed by mutualists, our results suggest that coevolution between mutualistic species will exaggerate, rather than diminish, the effects of climate change on species densities.

Conflicting coevolution is expected for most types of predator-prey or consumer-resource interactions, because increases in prey defenses will decrease benefits to predators, and increases in predator effectiveness will be detrimental to prey. Nonetheless, evolution of parasite virulence could be different [70] , [71].

The conventional wisdom is that parasites should evolve to be less virulent, because this will increase their transmission among hosts; parasites are not transmitted by dead hosts, at least not for long [72]. Nonetheless, this ignores, among other things, the relationship between the production of large numbers of propagules that generally harms the host and transmission rates, and more-detailed analyses generally predict evolution of parasite virulence to represent a balance between higher virulence caused by selection for production of propagules and lower virulence caused by selection for lengthening the transmission period [73].

Therefore, evolution of the parasite may be nonconflicting with the host, even at the same time evolution of the host to limit infection is conflicting with the parasite. In models describing this interaction results not shown , we found that when climatic changes directly affect the parasite, coevolution in the host fuels a negative feedback loop that mitigates the effects of climate change.

In contrast, in some cases when climatic changes directly affect the host, coevolution can lead to a positive feedback loop that exaggerates the effects of climate change on the host density. Thus, when there are both conflicting and nonconflicting coevolution, the ultimate outcome will be determined by whether the host or parasite experiences greater evolutionary change.

Given the widespread occurrences of both conflicting and nonconflicting coevolution in competition and mutualism, and to a lesser extent in predator-prey interactions, systems will have to be studied on a case-by-case basis to predict and test the role of coevolution in modifying the effects of climate change. This could be done either using experimental studies or taking advantage of naturally occurring environmental gradients.

An example of an experimental study is given by Lopez-Pascua and Buckling [74] , who performed an environmental manipulation of bacterial productivity by altering nutrient concentrations in the growth media. They showed that increasing bacterial productivity increases the rate of coevolution between bacteria and phages.

They proposed that this is due, in part, to increased selection pressure on the bacterial population in environments with high productivity high intrinsic rates of bacterial increase. This increased selection stems from increased encounters with phages, as phages numerically respond to increased bacterial density.

The phages then evolve greater infectivity in response to bacterial evolution. This explanation is consistent with our theoretical expectations for conflicting evolution of prey and predators; increasing the prey intrinsic rate of increase leads to evolution of stronger prey defenses against the predator Figure 4C.

In addition to experimental manipulations of environmental factors, it is possible to take advantage of natural environmental gradients similar to classical studies of character displacement.

For example, in a field experiment, Toju et al. Female beetles use their snout to pierce the camellia fruit pericarp and oviposit eggs into seeds, with oviposition success determined by the length of the beetle's snout and ovipositor relative to the pericarp thickness. Thus, plant defense is determined by pericarp thickness, and beetle snout and ovipositor lengths determine beetle ability to overcome this defense.

The authors measured beetle and plant traits along a latitudinal gradient, and previous work had showed that plants exhibit faster potential for growth at lower latitudes [76]. Thus, in the camellia-beetle arms race we expect that coevolution will favor plants more at lower latitudes. The authors indeed found this to be the case; plants in high latitude populations that experienced endemic predation by beetles had pericarp thicknesses similar to populations that did not experience beetles.

In contrast, at lower latitudes plant populations that experienced beetle predation had thicker pericarps than populations that did not. There was thus an increase in plant defense along the environmental gradient. Furthermore, this plant defense increased with decreasing latitude at a greater rate than weevil ovipositor length, suggesting that plants exhibited a larger coevolutionary advantage in environmental conditions with increased prey growth [75].

These results support our theoretical predictions that higher prey intrinsic rates of increase should lead to a coevolutionary advantage to prey, thereby buffering the changes in predator densities driven by climate change. The majority of coevolutionary studies involving environmental manipulations or environmental gradients have been conducted on predator-prey or herbivore-plant systems where conflicting coevolution is likely. Similar experiments that document changes in traits and density might help build a better understanding of coevolution in competitive and mutualistic relationships.

Laboratory studies have suggested that coevolution can lead to a reversal of competitive hierarchy in just 24 generations [15] , and can occur fast enough to drive population dynamics [16]. Therefore, experimental competition studies in which environmental factors are manipulated are possible for some types of organisms. Environmental gradient, rather than experimental, studies will be more practical for larger organisms with longer lifespans that operate at larger spatial scales.

Using character displacement to infer conflicting versus nonconflicting coevolution is necessarily correlative, although it opens up the study of coevolution in the context of climate change to a much wider range of species under natural spatial and temporal scales.

Studies that evaluate coevolution over environmental gradients fit within the broader conceptual paradigm of geographic mosaic theory [77] in which differences in coevolutionary selection among spatially separated populations are analyzed as genotype by genotype by environment interactions. A key feature of geographic mosaic theory is that some local populations experience environmental conditions under which coevolutionary pressures are strong. This pair of equations has the same general structure as that we have used for Equations 1 — 4.

Thus, our results address the possible character of evolution within coevolutionary hotspots, and how coevolutionary outcomes might differ under different environmental regimes.

We have only considered local populations, explicitly ignoring gene flow among populations. Thus, we have ignored the large body of theoretical and empirical studies evaluating gene flow among populations under different selective forces [77] — [79].

For example, Nuismer et al. When interaction types vary spatially, however, both dynamic and equilibrium clines occur, and the presence of each depends on the levels of selection and gene flow across the landscape [80]. In an experimental bacteria-bacteriophage community, bacteriophages became locally maladapted in the absence of gene flow, but became locally adapted when gene flow occurred between bacteriophage populations [81].

The importance of gene flow in both theoretical and empirical studies gives a caution to our recommendation that natural environmental gradients be used to assess the character of coevolution—conflicting versus nonconflicting—and whether coevolution sets up positive or negative feedback loops to environmental changes.

Gene flow and a geographic mosaic of selective pressure may dampen or otherwise modify the effects of local selection on coevolutionary traits.

While it is recognized that evolution will play a role in determining how climatic changes directly affect species [18] , the interactions among species force us to also consider coevolution between species. Our models suggest that the effects of coevolution on population densities depend on the presence of conflicting versus nonconflicting coevolutionary interests.

While we encourage future studies that experimentally manipulate both coevolution and environmental change, we acknowledge that experiments are likely to be difficult logistically for most study systems. It may be possible, however, to use character displacement across environmental gradients to distinguish whether conflicting versus nonconflicting coevolution is more likely, even when directly measuring coevolution is impossible.

Experimental [15] and environmental gradient [60] approaches to infer the nature of coevolution are both five decades old, and we hope that our theoretical results provide new impetus for these types of studies. They give needed information to anticipate whether coevolution will increase or decrease the effects of climate change on the densities of interacting species.

Generalist predator equilibrium densities and traits. Equilibrium values of prey and generalist predator population densities A, B and traits C, D for different climatic conditions. A, C The prey intrinsic rate of increase rose linearly with climate E , while the predation rate was unaffected. B, D The predation rate increased linearly with climate E , while prey growth was unaffected.

Analytical approximation for changes in species abundances with coevolution. Rosenheim, B. Barton, H. Fan, C. Herren, B. Krimmel, M. Meisner, E. Murell, A. Sadeh, J. Usinowicz, K.

Webert, and K. Zemenick provided helpful discussion. Abstract Background Recent studies suggest that environmental changes may tip the balance between interacting species, leading to the extinction of one or more species. Author Summary Recent studies suggest that environmental changes may tip the balance between species that interact with each other, leading to the extinction of one or more species.

Introduction Climatic changes, or indeed any change in the environment, have the potential to cause the local extinction of species, and to alter community composition and ecosystem functioning [1]. Modeling Coevolution To evaluate the effects of climate change, we present three coevolutionary models describing competitive, mutualistic, and predator-prey relationships between two species. Box 1. Analysis of Coevolution during Climate Change To analyze the effects on densities and species traits that climate-driven changes in intrinsic rates of increase can have, we used an analytical approach akin to loop analysis [82].

Competition We modeled coevolution of two competitors using a discrete-time, modified Lotka-Volterra competition model. Mutualism The model for two mutualists has the same structure as the competition model 1. Predation For predator-prey interactions we used a discrete-time version of a model in which the predator attack rate is determined by traits of both prey, 1, t , and predator, 2, t [51].

Results To illustrate the importance of coevolution—especially the contrast between conflicting and nonconflicting coevolution—for the response of populations to environmental changes, we conducted two types of simulations.

Competition To illustrate the competition model, we began by simulating the consequences of raising the environmental quality for species 1 increasing E through time while varying the rate of coevolution. Download: PPT. Mutualism As with competition, the effects of coevolution on mutualists depended on the type of coevolution. Predation For competition and mutualism, interacting species might have either conflicting or nonconflicting coevolutionary feedbacks.

Discussion We have shown, using simple models, that coevolution may increase or decrease the effect of environmental change, depending on the form that coevolution takes between species. Competitive Coevolution It has long been recognized that coevolution can lead to increased asymmetries in competitive abilities [15] , which is the hallmark of conflicting coevolution. Mutualistic Coevolution There is a rich theory describing the evolution of mutualisms [66] , [67].

Predator-Prey Coevolution Conflicting coevolution is expected for most types of predator-prey or consumer-resource interactions, because increases in prey defenses will decrease benefits to predators, and increases in predator effectiveness will be detrimental to prey. Predicting the Effects of Climate Change Given the widespread occurrences of both conflicting and nonconflicting coevolution in competition and mutualism, and to a lesser extent in predator-prey interactions, systems will have to be studied on a case-by-case basis to predict and test the role of coevolution in modifying the effects of climate change.

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