Eavesdropping Micropredators as Dynamic Limiters of Sexual Signal Elaboration and Intrasexual Competition.

AbstractTo thoroughly understand the drivers of dynamic signal elaboration requires assessing the direct and indirect effects of naturally interacting factors. Here, we use structural equation modeling to test multivariate data from in situ observations of sexual signal production against a model of causal processes hypothesized to drive signal elaboration. We assess direct and indirect effects, and relative impacts, of male-male competition and attacks by eavesdropping frog-biting midges (Diptera: Corethrellidae) on call elaboration of male túngara frogs (Engystomops pustulosus). We find that the intensity of attacks by these micropredator flies drives the extent to which frogs elaborate their calls, likely due to a temporal trade-off between signaling and antimicropredator defense. Micropredator attacks appear to dynamically limit a male's call rate and complexity and consequently dampen the effects of intrasexual competition. In accounting for naturally interacting drivers of signal elaboration, this study presents a counterpoint to the mechanisms traditionally thought to drive sexual selection in this system. Moreover, the results shed light on the relatively unexamined and potentially influential role of eavesdropping micropredators in the evolution of sexual communication systems.

Large genetic divergence underpins cryptic local adaptation across ecological and evolutionary gradients.

Environmentally covarying local adaptation is a form of cryptic local adaptation in which the covariance of the genetic and environmental effects on a phenotype obscures the divergence between locally adapted genotypes. Here, we systematically document the magnitude and drivers of the genetic effect (VG) for two forms of environmentally covarying local adaptation: counter- and cogradient variation. Using a hierarchical Bayesian meta-analysis, we calculated the overall effect size of VG as 1.05 and 2.13 for populations exhibiting countergradient or cogradient variation, respectively. These results indicate that the genetic contribution to phenotypic variation represents a 1.05 to 2.13 s.d. change in trait value between the most disparate populations depending on if populations are expressing counter- or cogradient variation. We also found that while there was substantial variance among abiotic and biotic covariates, the covariates with the largest mean effects were temperature (2.41) and gamete size (2.81). Our results demonstrate the pervasiveness and large genetic effects underlying environmentally covarying local adaptation in wild populations and highlight the importance of accounting for these effects in future studies.

Life history variation is maintained by fitness trade-offs and negative frequency-dependent selection.

The maintenance of diverse life history strategies within and among species remains a fundamental question in ecology and evolutionary biology. By using a near-complete 16-year pedigree of 12,579 winter-run steelhead (Oncorhynchus mykiss) from the Hood River, Oregon, we examined the continued maintenance of two life history traits: the number of lifetime spawning events (semelparous vs. iteroparous) and age at first spawning (2-5 years). We found that repeat-spawning fish had more than 2.5 times the lifetime reproductive success of single-spawning fish. However, first-time repeat-spawning fish had significantly lower reproductive success than single-spawning fish of the same age, suggesting that repeat-spawning fish forego early reproduction to devote additional energy to continued survival. For single-spawning fish, we also found evidence for a fitness trade-off for age at spawning: older, larger males had higher reproductive success than younger, smaller males. For females, in contrast, we found that 3-year-old fish had the highest mean lifetime reproductive success despite the observation that 4- and 5-year-old fish were both longer and heavier. This phenomenon was explained by negative frequency-dependent selection: as 4- and 5-year-old fish decreased in frequency on the spawning grounds, their lifetime reproductive success became greater than that of the 3-year-old fish. Using a combination of mathematical and individual-based models parameterized with our empirical estimates, we demonstrate that both fitness trade-offs and negative frequency-dependent selection observed in the empirical data can theoretically maintain the diverse life history strategies found in this population.

How are nitrogen availability, fine-root mass, and nitrogen uptake related empirically? Implications for models and theory.

Understanding the effects of global change in terrestrial communities requires an understanding of how limiting resources interact with plant traits to affect productivity. Here, we focus on nitrogen and ask whether plant community nitrogen uptake rate is determined (a) by nitrogen availability alone or (b) by the product of nitrogen availability and fine-root mass. Surprisingly, this is not empirically resolved. We performed controlled microcosm experiments and reanalyzed published pot experiments and field data to determine the relationship between community-level nitrogen uptake rate, nitrogen availability, and fine-root mass for 46 unique combinations of species, nitrogen levels, and growing conditions. We found that plant community nitrogen uptake rate was unaffected by fine-root mass in 63% of cases and saturated with fine-root mass in 29% of cases (92% in total). In contrast, plant community nitrogen uptake rate was clearly affected by nitrogen availability. The results support the idea that although plants may over-proliferate fine roots for individual-level competition, it comes without an increase in community-level nitrogen uptake. The results have implications for the mechanisms included in coupled carbon-nitrogen terrestrial biosphere models (CN-TBMs) and are consistent with CN-TBMs that operate above the individual scale and omit fine-root mass in equations of nitrogen uptake rate but inconsistent with the majority of CN-TBMs, which operate above the individual scale and include fine-root mass in equations of nitrogen uptake rate. For the much smaller number of CN-TBMs that explicitly model individual-based belowground competition for nitrogen, the results suggest that the relative (not absolute) fine-root mass of competing individuals should be included in the equations that determine individual-level nitrogen uptake rates. By providing empirical data to support the assumptions used in CN-TBMs, we put their global climate change predictions on firmer ground.

Unlimited niche packing in a Lotka-Volterra competition game.

A central question in the study of ecology and evolution is: "Why are there so many species?" It has been shown that certain forms of the Lotka-Volterra (L-V) competition equations lead to an unlimited number of species. Furthermore, these authors note how any change in the nature of competition (the competition kernel) leads to a finite or small number of coexisting species. Here we build upon these works by further investigating the L-V model of unlimited niche packing as a reference model and evolutionary game for understanding the environmental factors restricting biodiversity. We also examine the combined eco-evolutionary dynamics leading up to the species diversity and traits of the ESS community in both unlimited and finite niche-packing versions of the model. As an L-V game with symmetric competition, we let the strategies of individuals determine the strength of the competitive interaction (like competes most with like) and also the carrying capacity of the population. We use a mixture of analytic proofs (for one and two species systems) and numerical simulations. For the model of unlimited niche packing, we show that a finite number of species will evolve to specific convergent stable minima of the adaptive landscape (also known as species archetypes). Starting with a single species, faunal buildup can proceed either through species doubling as each diversity-specific set of minima are reached, or through the addition of species one-by-one by randomly assigning a speciation event to one of the species. Either way it is possible for an unlimited number or species to evolve and coexist. We examine two simple and biologically likely ways for breaking the unlimited niche-packing: (1) some minimum level of competition among species, and (2) constrain the fundamental niche of the trait space to a finite interval. When examined under both ecological and evolutionary dynamics, both modifications result in convergent stable ESSs with a finite number of species. When the number of species is held below the number of species in an ESS coalition, we see a diverse array of convergent stable niche archetypes that consist of some species at maxima and some at minima of the adaptive landscape. Our results support those of others and suggest that instead of focusing on why there are so many species we might just as usefully ask, why are there so few species?

The world's biomes and primary production as a triple tragedy of the commons foraging game played among plants.

Plants appear to produce an excess of leaves, stems and roots beyond what would provide the most efficient harvest of available resources. One way to understand this overproduction of tissues is that excess tissue production provides a competitive advantage. Game theoretic models predict overproduction of all tissues compared with non-game theoretic models because they explicitly account for this indirect competitive benefit. Here, we present a simple game theoretic model of plants simultaneously competing to harvest carbon and nitrogen. In the model, a plant's fitness is influenced by its own leaf, stem and root production, and the tissue production of others, which produces a triple tragedy of the commons. Our model predicts (i) absolute net primary production when compared with two independent global datasets; (ii) the allocation relationships to leaf, stem and root tissues in one dataset; (iii) the global distribution of biome types and the plant functional types found within each biome; and (iv) ecosystem responses to nitrogen or carbon fertilization. Our game theoretic approach removes the need to define allocation or vegetation type a priori but instead lets these emerge from the model as evolutionarily stable strategies. We believe this to be the simplest possible model that can describe plant production.

Synthesis and modeling perspectives of rhizosphere priming.

The rhizosphere priming effect (RPE) is a mechanism by which plants interact with soil functions. The large impact of the RPE on soil organic matter decomposition rates (from 50% reduction to 380% increase) warrants similar attention to that being paid to climatic controls on ecosystem functions. Furthermore, global increases in atmospheric CO2 concentration and surface temperature can significantly alter the RPE. Our analysis using a game theoretic model suggests that the RPE may have resulted from an evolutionarily stable mutualistic association between plants and rhizosphere microbes. Through model simulations based on microbial physiology, we demonstrate that a shift in microbial metabolic response to different substrate inputs from plants is a plausible mechanism leading to positive or negative RPEs. In a case study of the Duke Free-Air CO2 Enrichment experiment, performance of the PhotoCent model was significantly improved by including an RPE-induced 40% increase in soil organic matter decomposition rate for the elevated CO2 treatment--demonstrating the value of incorporating the RPE into future ecosystem models. Overall, the RPE is emerging as a crucial mechanism in terrestrial ecosystems, which awaits substantial research and model development.

Game theory and plant ecology.

The fixed and plastic traits possessed by a plant, which may be collectively thought of as its strategy, are commonly modelled as density-independent adaptations to its environment. However, plant strategies may also represent density- or frequency-dependent adaptations to the strategies used by neighbours. Game theory provides the tools to characterise such density- and frequency-dependent interactions. Here, we review the contributions of game theory to plant ecology. After briefly reviewing game theory from the perspective of plant ecology, we divide our review into three sections. First, game theoretical models of allocation to shoots and roots often predict investment in those organs beyond what would be optimal in the absence of competition. Second, game theoretical models of enemy defence suggest that an individual's investment in defence is not only a means of reducing its own tissue damage but also a means of deflecting enemies onto competitors. Finally, game theoretical models of trade with mutualistic partners suggest that the optimal trade may reflect competition for access to mutualistic partners among plants. In short, our review provides an accessible entrance to game theory that will help plant ecologists enrich their research with its worldview and existing predictions.

Ecological implications of single and mixed nitrogen nutrition in Arabidopsis thaliana.

BACKGROUND: Ecologists recognize that plants capture nitrogen in many chemical forms that include amino acids. Access to multiple nitrogen types in plant communities has been argued to enhance plant performance, access to nitrogen and alter ecological interactions in ways that may promote species coexistence. However, data supporting these arguments have been limited. While it is known that plants uptake amino acids from soil, long term studies that link amino acid uptake to measures of plant performance and potential reproductive effort are not typically performed. Here, a series of experiments that link uptake of nitrate, glutamine or asparagine with lifetime reproductive effort in Arabidopsis thaliana are reported. Nitrogen was offered either singly or in mixture and at a variety of combinations. Traits related to reproductive output were measured, as was the preference for each type of nitrogen. RESULTS: When plants were supplied with a single nitrogen type at concentrations from 0.1-0.9 mM, the ranking of nitrogen types was nitrate > glutamine > asparagine in terms of the relative performance of plants. When plants were supplied with two types of nitrogen in mixture at ratios between 0.1:0.9-0.9:0.1 mM, again plants performed best when nitrate was present, and poorly when amino acids were mixed. Additionally, stable isotopes revealed that plants preferentially captured nitrogen types matching the hierarchy of nitrate > glutamine > asparagine. Comparing between the two experiments revealed that mixed nitrogen nutrition was a net cost to the plants. CONCLUSIONS: Plant performance on mixed nitrogen was less than half the performance on equal amounts of any single nitrogen type. We asked: why did A. thaliana capture amino acids when doing so resulted in a net cost? We argue that available data cannot yet answer this question, but hypothesize that access to lower quality forms of nitrogen may become important when plants compete.

Negative frequency dependent selection unites ecology and evolution.

From genes to communities, understanding how diversity is maintained remains a fundamental question in biology. One challenging to identify, yet potentially ubiquitous, mechanism for the maintenance of diversity is negative frequency dependent selection (NFDS), which occurs when entities (e.g., genotypes, life history strategies, species) experience a per capita reduction in fitness with increases in relative abundance. Because NFDS allows rare entities to increase in frequency while preventing abundant entities from excluding others, we posit that negative frequency dependent selection plays a central role in the maintenance of diversity. In this review, we relate NFDS to coexistence, identify mechanisms of NFDS (e.g., mutualism, predation, parasitism), review strategies for identifying NFDS, and distinguish NFDS from other mechanisms of coexistence (e.g., storage effects, fluctuating selection). We also emphasize that NFDS is a key place where ecology and evolution intersect. Specifically, there are many examples of frequency dependent processes in ecology, but fewer cases that link this process to selection. Similarly, there are many examples of selection in evolution, but fewer cases that link changes in trait values to negative frequency dependence. Bridging these two well-developed fields of ecology and evolution will allow for mechanistic insights into the maintenance of diversity at multiple levels.

Plant root growth and the marginal value theorem.

All organisms must find and consume resources to live, and the strategies an organism uses when foraging can have significant impacts on their fitness. Models assuming optimality in foraging behavior, and which quantitatively account for the costs, benefits, and biological constraints of foraging, are common in the animal literature. Plant ecologists on the other hand have rarely adopted an explicit framework of optimality with respect to plant root foraging. Here, we show with a simple experiment that the marginal value theorem (MVT), one of the most classic models of animal foraging behavior, can provide novel insights into the root foraging behavior of plants. We also discuss existing data in the literature, which has not usually been linked to MVT to provide further support for the benefits of an optimal foraging framework for plants. As predicted by MVT, plants invest more time and effort into highly enriched patches than they do to low-enriched patches. On the basis of this congruency, and the recent calls for new directions in the plant foraging literature, we suggest plant ecologists should work toward a more explicit treatment of the idea of optimality in studies of plant root foraging. Such an approach is advantageous because it forces a quantitative treatment of the assumptions being made and the constraints on the system. While we believe significant insight can be gained from the use of preexisting models of animal foraging, ultimately plant ecologists will have to develop taxa-specific models that account for the unique biology of plants.

When does mutualism offer a competitive advantage? A game-theoretic analysis of host-host competition in mutualism.

Due to their non-motile nature, plants rely heavily on mutualistic interactions to obtain resources and carry out services. One key mutualism is the plant-microbial mutualism in which a plant trades away carbon to a microbial partner for nutrients like nitrogen and phosphorous. Plants show much variation in the use of this partnership from the individual level to entire lineages depending upon ecological, evolutionary and environmental context. We sought to determine how this context dependency could result in the promotion, exclusion or coexistence of the microbial mutualism by asking if and when the partnership provided a competitive advantage to the plant. To that end, we created a 2 × 2 evolutionary game in which plants could either be a mutualist and pair with a microbe or be a non-mutualist and forgo the partnership. Our model includes both frequency dependence and density dependence, which gives us the eco-evolutionary dynamics of mutualism evolution. As in all models, mutualism only evolved if it could offer a competitive advantage and its net benefit was positive. However, surprisingly the model reveals the possibility of coexistence between mutualist and non-mutualist genotypes due to competition between mutualists over the microbially obtained nutrient. Specifically, frequency dependence of host strategies can make the microbial symbiont less beneficial if the microbially derived resources are shared, a phenomenon that increasingly reduces the frequency of mutualism as the density of competitors increases. In essence, ecological competition can act as a hindrance to mutualism evolution. We go on to discuss basic experiments that can be done to test and falsify our hypotheses.

Allelopathy as an evolutionary game.

In plants, most competition is resource competition, where one plant simply preempts the resources away from its neighbors. Interference competition, as the name implies, is a form of direct interference to prevent resource access. Interference competition is common among animals that can physically fight, but in plants, one of the main mechanisms of interference competition is allelopathy. Allelopathic plants release cytotoxic chemicals into the environment which can increase their ability to compete with surrounding organisms for limited resources. The circumstances and conditions favoring the development and maintenance of allelochemicals, however, are not well understood. Particularly, despite the obvious benefits of allelopathy, current data suggest it seems to have only rarely evolved. To gain insight into the cost and benefit of allelopathy, we have developed a 2 × 2 matrix game to model the interaction between plants that produce allelochemicals and plants that do not. Production of an allelochemical introduces novel cost associated with both synthesis and detoxifying a toxic chemical but may also convey a competitive advantage. A plant that does not produce an allelochemical will suffer the cost of encountering one. Our model predicts three cases in which the evolutionarily stable strategies are different. In the first, the nonallelopathic plant is a stronger competitor, and not producing allelochemicals is the evolutionarily stable strategy. In the second, the allelopathic plant is the better competitor, and production of allelochemicals is the more beneficial strategy. In the last case, neither is the evolutionarily stable strategy. Instead, there are alternating stable states, depending on whether the allelopathic or nonallelopathic plant arrived first. The generated model reveals circumstances leading to the evolution of allelochemicals and sheds light on utilizing allelochemicals as part of weed management strategies. In particular, the wide region of alternative stable states in most parameterizations, combined with the fact that the absence of allelopathy is likely the ancestral state, provides an elegant answer to the question of why allelopathy seems to rarely evolve despite its obvious benefits. Allelopathic plants can indeed outcompete nonallelopathic plants, but this benefit is simply not great enough to allow them to go to fixation and spread through the population. Thus, most populations would remain purely nonallelopathic.

Pisum sativum has no competitive responses to neighbors: A case study in (non)reproducible plant biology.

Plant-plant competition is ubiquitous in nature. However, studying below ground behavior of roots has always posed certain difficulties. Pea (Pisum sativum L.) has become a common study species for questions about how plant roots respond to neighboring plant roots and barriers in soil. However, published results point in several different directions. This has sometimes been interpreted as pea having sophisticated context dependent responses that can change in complex ways depending on its surroundings, but it could also just point to small statistical power resulting in type I or II statistical errors. To explore this further, here, we combine the result of five new experiments with published results to examine 18 unique experiments from 10 different studies and 6 cultivars of pea for a total of 254 replicate plants. We used a Bayesian hierarchical meta-analysis approach to estimating the likely effect size from the available data, as well as quantify heterogeneity among different experiments, studies and cultivars. The posterior distributions show that, at the coarsest possible scale of total root production, it is unlikely that P. sativum root growth is influenced by either neighbors or pot volume that varies primarily by depth. We find no evidence of publication bias and conclude that this is simply due to statistical sampling error and the scientific method combined with frequentist statistics operating as intended. We suggest that further work on pea should consider repeating experiments that reported finer scale root plasticity at the rhizosphere scale or consider exploring different pot geometries such as volume that varies by depth or width. We also suggest that more diversity in study species are needed to better understand the neighbor-volume response.

Toleration games: compensatory growth by plants in response to enemy attack is an evolutionarily stable strategy.

Damage to plants from natural enemies is a ubiquitous feature of the natural world. Accordingly, plants have evolved a variety of strategies to deal with attack from enemies including the ability to simply tolerate attack. Tolerance often involves some form of compensatory response, such as the regrowth of tissues following damage. While ecological models of defence are common, there has been less effort to make predictions about the evolutionary stability of tolerance. Here, we present and experimentally test a game theoretic model of tolerance to herbivory. Plants in the model have a vector strategy which includes both root and shoot production, and herbivores in the model have a scalar strategy which is time spent foraging. The evolutionarily stable strategy (ESS) is the set of root growth, shoot growth and herbivore foraging which simultaneously maximizes all player's fitness. Compensatory growth is not guaranteed, but it may emerge as an ESS if it maximizes plant fitness. We also experimentally tested the model predictions using wheat and simulated herbivory by clipping 0, 15, 30, 45 or 60 % of shoot production, and measured root, shoot and fruit production at senescence. The model predicted that compensatory growth was often an ESS when herbivores were either above- or below-ground. Plants in the experiment followed model predictions. Specifically, plants produced more tissues than expected based on damage, and for 15 % damage this allowed them to maintain equal fitness compared to undamaged plants. The model allows for above- and below-ground herbivory to be modelled, and predicts their impact on whole plant growth and reproduction. For example, we can predict the effects of shoot damage on root growth. When combined with other advances in predicting plant ecology with evolutionary game theory, we anticipate that this will be a valuable tool for generating further testable hypotheses.

Assessing local adaptation vs. plasticity under different resource conditions in seedlings of a dominant boreal tree species.

Under changing climate conditions, understanding local adaptation of plants is crucial to predicting the resilience of ecosystems. We selected black spruce (Picea mariana), the most dominant tree species in the North American boreal forest, in order to evaluate local adaptation vs. plasticity across regions experiencing some of the most extreme climate warming globally. Seeds from three provenances across the latitudinal extent of this species in northwestern Canada were planted in a common garden study in growth chambers. Two levels of two resource conditions were applied (low/high nutrient and ambient/elevated CO2) in a fully factorial design and we measured physiological traits, allocational traits, growth and survival. We found significant differences in height, root length and biomass among populations, with southern populations producing the largest seedlings. However, we did not detect meaningful significant differences among nutrient or CO2 treatments in any traits measured, and there were no consistent population-level differences in physiological traits or allocation patterns. We found that there was greater mortality after simulated winter in the high nutrient treatment, which may reflect an important shift in seedling growth strategies under increased resource availability. Our study provides important insight into how this dominant boreal tree species might respond to the changing climate conditions predicted in this region.

When Michaelis and Menten met Holling: towards a mechanistic theory of plant nutrient foraging behaviour.

Plants are adept at assessing and responding to nutrients in soil, and generally proliferate roots into nutrient-rich patches. An analogy between this growth response and animal foraging movement is often drawn, but because of differences between plants and animals it has not always been clear how to directly apply existing foraging theory to plants. Here we suggest one way to unite pre-existing ideas in plant nutrient uptake with foraging theory. First, we show that the Michaelis-Menten equation used by botanists and the Holling disc equation used by zoologists are actually just rearrangements of the same functional response. This mathematical unity permits the translation of existing knowledge about the nutrient uptake physiology of plants into the language of foraging behaviour, and as a result gives botanists direct access to foraging theory. Second, we developed a model of root foraging precision based on the Holling disc equation and the marginal value theorem, and parameterize it from the literature. The model predicts (i) generally plants should invest in higher quality patches compared to lower quality patches, and as patch background-contrast increases; (ii) low encounter rates between roots and nutrients result in high root foraging precision; and (iii) low handling times for nutrients should result in high root foraging precision. The available data qualitatively support these predictions. Third, to parameterize the model above we undertook a review of the literature. From that review we obtained parameter estimates for nitrate and/or ammonium uptake for 45 plant species from 38 studies. We observe that the parameters ranged over six orders of magnitude, there was no trade-off in foraging ability for nitrate versus ammonium: plants that were efficient foragers for one form of nitrogen were efficient foragers for the other, and there was also no phylogenetic signal in the parameter estimates.

Molecular identification of roots from a grassland community using size differences in fluorescently labelled PCR amplicons of three cpDNA regions.

Elucidating patterns of root growth is essential for a better understanding of the functioning of plant-dominated ecosystems. To this end, reliable and inexpensive methods are required to determine species compositions of root samples containing multiple species. Previous studies use a range of PCR-based approaches, but none have examined a species pool greater than 10 or 30 when evaluating mixed and single species samples, respectively. We present a method that evaluates size differences in fluorescently labelled PCR amplicons (fluorescent fragment length polymorphism) of the trnL intron and the trnT-trnL and trnL-trnF intergenic spacers. Amplification success of the trnT-trnL spacer was limited, but variation in the trnL intron and the trnL-trnF spacer was sufficient to distinguish over 80% of the 95 species (97% of the 77 genera) evaluated from a diverse fescue grassland community. Moreover, we identified species known to be present in mixed samples of 4, 8, 12, and 16 species on average 82% of the time. However, this approach is sensitive to detecting species known to be absent (false positives) when using our key of 95 species. Comparing unknowns to a limited species pool ameliorates this problem, comparable to a researcher using prior knowledge of what species could be found in a sample to constrain the identification of species. Comparisons to other methods and future improvements are discussed. This method is efficient, cost- effective and broadly applicable to many ecosystems.

Plants integrate information about nutrients and neighbors.

Animals regularly integrate information about the location of resources and the presence of competitors, altering their foraging behavior accordingly. We studied the annual plant Abutilon theophrasti to determine whether a plant can demonstrate a similarly complex response to two conditions: presence of a competitor and heterogeneous resource distributions. Individually grown plants fully explored the pot by using a broad and uniform rooting distribution regardless of soil resource distributions. Plants with competitors and uniform soil nutrient distributions exhibited pronounced reductions in rooting breadth and spatial soil segregation among the competing individuals. In contrast, plants with competitors and heterogeneous soil nutrient distributions reduced their root growth only modestly, indicating that plants integrate information about both neighbor and resource distributions in determining their root behavior.