The complex circuitry of interactions determining coexistence among plants and mycorrhizal fungi.

We present a mechanistic model of coexistence among a mycorrhizal fungus and one or two plant species that compete for a single nutrient. Plant-fungal coexistence is more likely if the fungus is better at extracting the environmental nutrient than the plant and the fungus acquires carbon from the plant above a minimum rate. When they coexist, their interaction can shift from mutualistic to parasitic at high nutrient availability. The fungus is a second nutrient source for plants and can promote the coexistence of two plant competitors if one is better at environmental nutrient extraction and the other is better at acquiring the nutrient from the fungus. Because it extracts carbon from both plants, the fungus also serves as a conduit of apparent competition between the plants. Consequently, the plant with the lower environmental nutrient extraction rate can drive the plant with the higher environmental nutrient extraction rate extinct at high carbon supply rates. This model illustrates mechanisms to explain several observed patterns, including shifts in plant-mycorrhizal growth responses and coexistence along nutrient gradients, equivocal results among experiments testing the effect of mycorrhizal fungi on plant diversity, and differences in plant diversity among ecosystems dominated by different mycorrhizal groups.

Eco-evolutionary feedbacks among pollinators, herbivores, and their plant resources.

Eco-evolutionary feedbacks among multiple species occur when one species affects another species' evolution via its effects on the abundance and traits of a shared partner species. What happens if those two species enact opposing effects on their shared partner's population growth? Furthermore, what if those two kinds of interactions involve separate traits? For example, many plants produce distinct suites of traits that attract pollinators (mutualists) and deter herbivores (antagonists). Here, we develop a model to explore how pollinators and herbivores may influence each other's interactions with a shared plant species via evolutionary effects on the plant's nectar and toxin traits. The model results predict that herbivores indirectly select for the evolution of increased nectar production by suppressing plant population growth. The model also predicts that pollinators indirectly select for the evolution of increased toxin production by plants and increased counterdefenses by herbivores via their positive effects on plant population growth. Unless toxins directly affect pollinator foraging, plants always evolve increases in attraction and defense traits when they interact with both kinds of foragers. This work highlights the value of incorporating ecological dynamics to understand the entangled evolution of mutualisms and antagonisms in natural communities.

Environmental Conditions during Development Affect Sexual Selection through Trait-Fitness Relationships.

AbstractSexual selection can be shaped by spatial variation in environmental features among populations. Differences in sexual selection among populations generated through the effects of the environment could be shaped via four paths: differences in mean absolute fitness, differences in the means or variances of phenotypes, or differences in the absolute fitness-trait function relationship. Because sexual selection occurs only during the adult life stage, most studies have focused on identifying environmental features that influence these metrics of fitness and trait distributions among adults. However, these adult features could also be affected by environmental factors experienced in early life stages that then shape the trajectory for sexual selection during the adult life stage. Here we investigated how among-population variation in environmental conditions during the juvenile (larval) stage of two species of Enallagma damselflies shapes sexual selection on male body size. We found that environmental factors related to predation pressures, lake primary productivity, and habitat availability play a role in shaping spatial variation in sexual selection. This acts mainly through how the environment affects absolute fitness-body size associations, not spatial variation in mean fitness or body size means and variances. These results demonstrate that the underpinnings of sexual selection in the wild can arise from environmental conditions during prereproductive life stages.

MicroRNAs as Indicators into the Causes and Consequences of Whole-Genome Duplication Events.

Whole-genome duplications (WGDs) have long been considered the causal mechanism underlying dramatic increases to morphological complexity due to the neo-functionalization of paralogs generated during these events. Nonetheless, an alternative hypothesis suggests that behind the retention of most paralogs is not neo-functionalization, but instead the degree of the inter-connectivity of the intended gene product, as well as the mode of the WGD itself. Here, we explore both the causes and consequences of WGD by examining the distribution, expression, and molecular evolution of microRNAs (miRNAs) in both gnathostome vertebrates as well as chelicerate arthropods. We find that although the number of miRNA paralogs tracks the number of WGDs experienced within the lineage, few of these paralogs experienced changes to the seed sequence, and thus are functionally equivalent relative to their mRNA targets. Nonetheless, in gnathostomes, although the retention of paralogs following the 1R autotetraploidization event is similar across the two subgenomes, the paralogs generated by the gnathostome 2R allotetraploidization event are retained in higher numbers on one subgenome relative to the second, with the miRNAs found on the preferred subgenome showing both higher expression of mature miRNA transcripts and slower molecular evolution of the precursor miRNA sequences. Importantly, WGDs do not result in the creation of miRNA novelty, nor do WGDs correlate to increases in complexity. Instead, it is the number of miRNA seed sequences in the genome itself that not only better correlate to instances in complexification, but also mechanistically explain why complexity increases when new miRNA families are established.

The Evolution of Resource Provisioning in Pollination Mutualisms.

AbstractResource dynamics influence the contemporary ecology of consumer-resource mutualisms. Suites of resource traits, such as floral nectar components, also evolve in response to different selective pressures, changing the ecological dynamics of the interacting species at the evolutionary equilibrium. Here we explore the evolution of resource-provisioning traits in a biotically pollinated plant that produces nectar as a resource for beneficial consumers. We develop a mathematical model describing natural selection on two quantitative nectar traits: maximum nectar production rate and maximum nectar reservoir volume. We use this model to examine how nectar production dynamics evolve under different ecological conditions that impose varying cost-benefit regimes on resource provisioning. The model results predict that natural selection favors higher nectar production when ecological factors limit the plant or pollinator's abundance (e.g., a lower productivity environment or a higher pollinator conversion efficiency). We also find that nectar traits evolve as a suite in which higher costs of producing one trait select for a compensatory increase in investment in the other trait. This empirically explicit approach to studying the evolution of consumer-resource mutualisms illustrates how natural selection acting via direct and indirect pathways of species interactions generates patterns of resource provisioning seen in natural systems.

When Ecology Fails: How Reproductive Interactions Promote Species Coexistence.

That species must differ ecologically is often viewed as a fundamental condition for their stable coexistence in biological communities. Yet, recent work has shown that ecologically equivalent species can coexist when reproductive interactions and sexual selection regulate population growth. Here, we review theoretical models and highlight empirical studies supporting a role for reproductive interactions in maintaining species diversity. We place reproductive interactions research within a burgeoning conceptual framework of coexistence theory, identify four key mechanisms in intra- and interspecific interactions within and between sexes, speculate on novel mechanisms, and suggest future research. Given the preponderance of sexual reproduction in nature, our review suggests that this is a neglected path towards explaining species diversity when traditional ecological explanations have failed.

Disentangling ecologically equivalent from neutral species: The mechanisms of population regulation matter.

The neutral theory of biodiversity explored the structure of a community of ecologically equivalent species. Such species are expected to display community drift dynamics analogous to neutral alleles undergoing genetic drift. While entire communities of species are not ecologically equivalent, recent field experiments have documented the existence of guilds of such neutral species embedded in real food webs. What demographic outcomes of the interactions within and between species in these guilds are expected to produce ecological drift versus coexistence remains unclear. To address this issue, and guide empirical testing, we consider models of a guild of ecologically equivalent competitors feeding on a single resource to explore when community drift should manifest. We show that community drift dynamics only emerge when the density-dependent effects of each species on itself are identical to its density-dependent effects on every other guild member. In contrast, if each guild member directly limits itself more than it limits the abundance of other guild members, all species in the guild are coexisting, even though they all are ecologically equivalent with respect to their interactions with species outside the guild (i.e. resources, predators, mutualists). Hence, considering only interspecific ecological differences generating density dependence, and not fully accounting for the preponderance of mechanisms causing intraspecific density dependence, will provide an incomplete picture for segregating between neutrality and coexistence. We also identify critical experiments necessary to disentangle guilds of ecologically equivalent species from those experiencing ecological drift, as well as provide an overview of ways of incorporating a mechanistic basis into studies of species coexistence and neutrality. Identifying these characteristics, and the mechanistic basis underlying community structure, is not merely an exercise in clarifying the semantics of coexistence and neutral theories, but rather reflects key differences that must exist among community members in order to determine how and why communities are structured.

Increased levels of superoxide dismutase suppress meiotic segregation errors in aging oocytes.

The risk of meiotic segregation errors increases dramatically during a woman's thirties, a phenomenon known as the maternal age effect. In addition, several lines of evidence indicate that meiotic cohesion deteriorates as oocytes age. One mechanism that may contribute to age-induced loss of cohesion is oxidative damage. In support of this model, we recently reported (Perkins et al. in Proc Natl Acad Sci U S A 113(44):E6823-E6830, 2016) that the knockdown of the reactive oxygen species (ROS)-scavenging enzyme, superoxide dismutase (SOD), during meiotic prophase causes premature loss of arm cohesion and segregation errors in Drosophila oocytes. If age-dependent oxidative damage causes meiotic segregation errors, then the expression of extra SOD1 (cytosolic/nuclear) or SOD2 (mitochondrial) in oocytes may attenuate this effect. To test this hypothesis, we generated flies that contain a UAS-controlled EMPTY, SOD1, or SOD2 cassette and induced expression using a Gal4 driver that turns on during meiotic prophase. We then compared the fidelity of chromosome segregation in aged and non-aged Drosophila oocytes for all three genotypes. As expected, p{EMPTY} oocytes subjected to aging exhibited a significant increase in nondisjunction (NDJ) compared with non-aged oocytes. In contrast, the magnitude of age-dependent NDJ was significantly reduced when expression of extra SOD1 or SOD2 was induced during prophase. Our findings support the hypothesis that a major factor underlying the maternal age effect in humans is age-induced oxidative damage that results in premature loss of meiotic cohesion. Moreover, our work raises the exciting possibility that antioxidant supplementation may provide a preventative strategy to reduce the risk of meiotic segregation errors in older women.

Limiting Similarity? The Ecological Dynamics of Natural Selection among Resources and Consumers Caused by Both Apparent and Resource Competition.

Much of ecological theory presumes that natural selection should foster species coexistence by phenotypically differentiating competitors so that the stability of the community is increased, but whether this will actually occur is a question of the ecological dynamics of natural selection. I develop an evolutionary model of consumer-resource interactions based on MacArthur's and Tilman's classic works, including both resource and apparent competition, to explore what fosters or retards the differentiation of resources and their consumers. Analyses of this model predict that consumers will differentiate only on specific ranges of environmental gradients (e.g., greater productivity, weaker stressors, lower structural complexity), and where it occurs, the magnitude of differentiation also depends on gradient position. In contrast to "limiting similarity" expectations, greater intraspecific phenotypic variance results in less differentiation among the consumers because of how phenotypic variation alters the fitness landscapes driving natural selection. In addition, the final structure of the community that results from the coevolution of these interacting species may be highly contingent on the initial properties of the species as the community is being assembled. These results highlight the fact that evolutionary conclusions about community structure cannot be based on ecological arguments of community stability or coexistence but rather must be explicitly based on the ecological dynamics of natural selection.

Female mate preferences on high-dimensional shape variation for male species recognition traits.

Females in many animal species must discriminate between conspecific and heterospecific males when choosing mates. Such mating preferences that discriminate against heterospecifics may inadvertently also affect the mating success of conspecific males, particularly those with more extreme phenotypes. From this expectation, we hypothesized that female mate choice should cause Enallagma females (Odonata: Coenagrionidae) to discriminate against conspecific males with more extreme phenotypes of the claspers males use to grasp females while mating - the main feature of species mate recognition in these species. To test this, we compared cerci sizes and shapes between males that were captured while mating with females to males that were captured at the same time but not mating in three Enallagma species. In contrast to our hypothesis, we found only one of forty comparisons of shape variation that was consistent with females discriminating against males with more extreme cerci shapes. Instead, differences in cerci shape between mating and single males suggested that females displayed directional preferences on 1-4 aspects of cerci shape in two of the species in our samples. These results suggest that whereas some directional biases in mating based on cerci shape occur, the intraspecific phenotypic variation in male cerci size and shape is likely not large enough for females to express any significant incidental discrimination among conspecifics with more extreme shapes.

Mechanical and tactile incompatibilities cause reproductive isolation between two young damselfly species.

External male reproductive structures have received considerable attention as a cause of reproductive isolation (RI), because the morphology of these structures often evolves rapidly between populations. This rapid evolution presents the potential for mechanical incompatibilities with heterospecific female structures during mating and could thus prevent interbreeding between nascent species. Although such mechanical incompatibilities have received little empirical support as a common cause of RI, the potential for mismatch of reproductive structures to cause RI due to incompatible species-specific tactile cues has not been tested. We tested the importance of mechanical and tactile incompatibilities in RI between Enallagma anna and E. carunculatum, two damselfly species that diverged within the past ∼250,000 years and currently hybridize in a sympatric region. We quantified 19 prezygotic and postzygotic RI barriers using both naturally occurring and laboratory-reared damselflies. We found incomplete mechanical isolation between the two pure species and between hybrid males and pure species females. Interestingly, in mating pairs for which mechanical isolation was incomplete, females showed greater resistance and refusal to mate with hybrid or heterospecific males compared to conspecific males. This observation suggests that tactile incompatibilities involving male reproductive structures can influence female mating decisions and form a strong barrier to gene flow in early stages of speciation.

The Ecological Dynamics of Natural Selection: Traits and the Coevolution of Community Structure.

Natural selection has both genetic and ecological dynamics. The fitnesses of individuals change with their ecological context, and so the form and strength of selective agents change with abiotic factors and the phenotypes and abundances of interacting species. I use standard models of consumer-resource interactions to explore the ecological dynamics of natural selection and how various trait types influence these dynamics and the resulting structure of a community of coevolving species. Evolutionary optima favored by natural selection depend critically on the abundances of interacting species, and the traits of species can undergo dynamic cycling in limited areas of parameter space. The ecological dynamics of natural selection can also drive shifts from one adaptive peak to another, and these ecologically driven adaptive peak shifts are fundamental to the dynamics of niche differentiation. Moreover, this ecological differentiation is fostered in more productive and more benign environments where species interactions are stronger and where the selection gradients generated by species interactions are stronger. Finally, community structure resulting from coevolution depends fundamentally on the types of traits that underlie species interactions. The ecological dynamics of the process cannot be simplified, neglected, or ignored if we are to build a predictive theory of natural selection.

Multi-locus phylogeny and divergence time estimates of Enallagma damselflies (Odonata: Coenagrionidae).

Reconstructing evolutionary patterns of species and populations provides a framework for asking questions about the impacts of climate change. Here we use a multilocus dataset to estimate gene trees under maximum likelihood and Bayesian models to obtain a robust estimate of relationships for a genus of North American damselflies, Enallagma. Using a relaxed molecular clock, we estimate the divergence times for this group. Furthermore, to account for the fact that gene tree analyses can overestimate ages of population divergences, we use a multi-population coalescent model to gain a more accurate estimate of divergence times. We also infer diversification rates using a method that allows for variation in diversification rate through time and among lineages. Our results reveal a complex evolutionary history of Enallagma, in which divergence events both predate and occur during Pleistocene climate fluctuations. There is also evidence of diversification rate heterogeneity across the tree. These divergence time estimates provide a foundation for addressing the relative significance of historical climatic events in the diversification of this genus.

Predation risk shapes thermal physiology of a predaceous damselfly.

Predation risk has strong effects on organismal physiology that can cascade to impact ecosystem structure and function. Physiological processes in general are sensitive to temperature. Thus, the temperature at which predators and prey interact may shape physiological response to predation risk. We measured and evaluated how temperature and predation risk affected growth rates of predaceous damselfly nymphs (Enallagma vesperum, Odonata: Coenagrionidae). First, we conducted growth trials at five temperatures crossed with two levels of predation risk (fish predator present versus absent) and measured growth rates, consumption rates, assimilation efficiencies, and production efficiencies of 107 individual damselflies. Second, we used a model to evaluate if and how component physiological responses to predation risk affected growth rates across temperatures. In the absence of mortality threat, growth rates of damselflies increased with warming until about 23.5 °C and then began to decline, a typical unimodal response to changes in temperature. Under predation risk, growth rates were lower and the shape of the thermal response was less apparent. Higher metabolic and survival costs induced by predation risk were only partially offset by changes in consumption rates and assimilation efficiencies and the magnitude of non-consumptive effects varied as a function of temperature. Furthermore, we documented that thermal physiology was mediated by predation risk, a known driver of organismal physiology that occurs in the context of species interactions. A general understanding of climatic impacts on ectothermic populations requires consideration of the community context of thermal physiology, including non-consumptive effects of predators.

Is dispersal neutral?

Dispersal is difficult to quantify and often treated as purely stochastic and extrinsically controlled. Consequently, there remains uncertainty about how individual traits mediate dispersal and its ecological effects. Addressing this uncertainty is crucial for distinguishing neutral versus non-neutral drivers of community assembly. Neutral theory assumes that dispersal is stochastic and equivalent among species. This assumption can be rejected on principle, but common research approaches tacitly support the 'neutral dispersal' assumption. Theory and empirical evidence that dispersal traits are under selection should be broadly integrated in community-level research, stimulating greater scrutiny of this assumption. A tighter empirical connection between the ecological and evolutionary forces that shape dispersal will enable richer understanding of this fundamental process and its role in community assembly.

Keystone and intraguild predation, intraspecific density dependence, and a guild of coexisting consumers.

Previous models of diamond-shaped and intraguild predation community modules have represented the essence of the trade-off necessary for a top predator to prevent competitive exclusion among a set of resource-limited consumers. However, at most two consumers can coexist in these models. In this article, I show how intraspecific density dependence in the consumers can permit many more than two consumers to coexist in these community modules. Moreover, responses of the community to removal of the top predator depend on the patterns of the strengths of species interactions relative to the strengths of intraspecific density dependence. If the consumers experience similar strengths of intraspecific density dependence, removing the top predator will in most cases have little effect on consumer species richness. A substantial reduction in consumer species richness with predator removal (i.e., the keystone predation effect) will typically occur only when the consumer that can support a population at the lowest resource abundance also (1) experiences substantially weaker intraspecific density dependence than other consumers and (2) experiences significantly higher levels of mortality from the predator. These results identify how intraspecific density dependence fosters the coexistence of multiple consumers in two important community modules and shapes the responses of these community modules to perturbations such as predator removal.

Maternal age and spine development in a rotifer: ecological implications and evolution.

Brachionus calyciflorus typically develops long, defensive spines only in response to a kairomone from the predatory rotifer, Asplanchna. However, in the absence of any environmental induction, females of some clones produce daughters with increasingly long spines as they age; late-born individuals can have posterolateral spines as long as those induced by Asplanchna: up to 50% or more of body length. Here, we construct a model using data from life-table and predator-prey experiments to assess how this maternal-age effect can influence the distribution of spine lengths in reproducing populations and provide defense against Asplanchna predation. When Asplanchna is absent, the frequency of individuals with late birth orders rapidly becomes extremely low; thus, any cost associated with the production of long-spined individuals is minimal. When Asplanchna is present at densities too low for spine induction, and preys selectively on individuals with no or short posterolateral spines, the frequency of long-spined individuals rapidly increases until a stable birth-order structure is reached. As a result, mortality from Asplanchna predation is greatly reduced. The pronounced and novel birth-order effect in this rotifer appears to be an effective bet-hedging strategy to limit predation by Asplanchna when its kairomone induces no or less than maximal spine development.