Jennifer A. Lau

Direct and ecological costs of resistance to herbivory

Herbivores can consume significant amounts of plant biomass in many environments. Yet plants are not defenseless against such attack. Although defenses might benefit plants in the presence of herbivores, herbivore attack varies both spatially and temporally, and the expression of plant resistance to herbivores can be costly in the absence of plant enemies. Costs can be described as allocation costs, resource-based tradeoffs between resistance and fitness, or as ecological costs, decreases in fitness resulting from interactions with other species. Here, we update the seminal 1996 Bergelson and Purrington review of resistance costs and find that many more studies have documented costs of resistance (sensu lato) than found during the 1996 survey. Eighty-two percent of studies in which genetic background is controlled, demonstrate significant fitness reductions associated with herbivore resistance. We categorize studies by type of resistance, induced or constitutive, by type of cost, and also by the degree to which investigators controlled for genetic background. Recent work has commonly detected both direct resistance costs, such as resource-based tradeoffs, and ecological costs, which depend on interactions with other species.

Community heterogeneity and the evolution of interactions between plants and insect herbivores

Plant communities vary tremendously in terms of productivity, species diversity, and genetic diversity within species. This vegetation heterogeneity can impact both the likelihood and strength of interactions between plants and insect herbivores. Because altering plant‐herbivore interactions will likely impact the fitness of both partners, these ecological effects also have evolutionary consequences. We review several hypothesized and well‐documented mechanisms whereby variation in the plant community alters the plant‐herbivore interaction, discuss potential evolutionary outcomes of each of these ecological effects, and conclude by highlighting several avenues for future research. The underlying theme of this review is that the neighborhood of plants is an important determinant of insect attack, and this results in feedback effects on the plant community. Because plants exert selection on herbivore traits and, reciprocally, herbivores exert selection on plant‐defense traits, variation in the plant community likely contributes to spatial and temporal variation in both plant and insect traits, which could influence macroevolutionary patterns.

Rapid responses of soil microorganisms improve plant fitness in novel environments

Global change is challenging plant and animal populations with novel environmental conditions, including increased atmospheric CO2 concentrations, warmer temperatures, and altered precipitation regimes. In some cases, contemporary or “rapid” evolution can ameliorate the effects of global change. However, the direction and magnitude of evolutionary responses may be contingent upon interactions with other community members that also are experiencing novel environmental conditions. Here, we examine plant adaptation to drought stress in a multigeneration experiment that manipulated aboveground–belowground feedbacks between plants and soil microbial communities. Although drought stress reduced plant growth and accelerated plant phenologies, surprisingly, plant evolutionary responses to drought were relatively weak. In contrast, plant fitness in both drought and nondrought environments was linked strongly to the rapid responses of soil microbial community structure to moisture manipulations. Specifically, plants were most fit when their contemporary environmental conditions (wet vs. dry soil) matched the historical environmental conditions (wet vs. dry soil) of their associated microbial community. Together, our findings suggest that, when faced with environmental change, plants may not be limited to “adapt or migrate” strategies; instead, they also may benefit from association with interacting species, especially diverse soil microbial communities, that respond rapidly to environmental change.

Evolutionary ecology of plant–microbe interactions: soil microbial structure alters selection on plant traits

• Below-ground microbial communities influence plant diversity, plant productivity, and plant community composition. Given these strong ecological effects, are interactions with below-ground microbes also important for understanding natural selection on plant traits? • Here, we manipulated below-ground microbial communities and the soil moisture environment on replicated populations of Brassica rapa to examine how microbial community structure influences selection on plant traits and mediates plant responses to abiotic environmental stress. • In soils with experimentally simplified microbial communities, plants were smaller, had reduced chlorophyll content, produced fewer flowers, and were less fecund when compared with plant populations grown in association with more complex soil microbial communities. Selection on plant growth and phenological traits also was stronger when plants were grown in simplified, less diverse soil microbial communities, and these effects typically were consistent across soil moisture treatments. • Our results suggest that microbial community structure affects patterns of natural selection on plant traits. Thus, the below-ground microbial community can influence evolutionary processes, just as recent studies have demonstrated that microbial diversity can influence plant community and ecosystem processes.

Inference of allelopathy is complicated by effects of activated carbon on plant growth

Allelopathy can play an important role in structuring plant communities, but allelopathic effects are often difficult to detect because many methods used to test for allelopathy can be confounded by experimental artifacts. The use of activated carbon, a technique for neutralizing allelopathic compounds, is now employed in tests for allelopathy; however, this technique also could produce large experimental artifacts. In three independent experiments, it was shown that adding activated carbon to potting media affected nutrient availability and plant growth. For most species tested, activated carbon increased plant biomass, even in the absence of the potentially allelopathic agent. The increased growth corresponded to increased plant nitrogen content, likely resulting from greater nitrogen availability. Activated carbon also affected nitrogen and other nutrient concentrations in soil media in the absence of plants. The observed effects of activated carbon on plant growth can confound its use to test for allelopathy. The detection of allelopathy relies on the difference between plant growth in medium with carbon and that in medium without carbon in the presence of the potentially allelopathic competitor; however, this difference may be biased if activated carbon alters soil nutrient availability and plant growth even in the absence of the focal allelopathic agent.

Mechanisms contributing to stability in ecosystem function depend on the environmental context.

Stability in ecosystem function is an important but poorly understood phenomenon. Anthropogenic perturbations alter communities, but how they change stability and the strength of stabilizing mechanisms is not clear. We examined temporal stability (invariability) in aboveground productivity in replicated 18-year time series of experimentally perturbed grassland plant communities. We found that disturbed annual-dominated communities were more stable than undisturbed perennial communities, coincident with increases in the stabilizing effect of mean-variance scaling. We also found that nitrogen-fertilized communities maintained stability despite losses in species richness, probably because of increased compensatory dynamics and increased dominance by particularly stable dominant species. Among our communities, slight variation in diversity was not the strongest mechanism driving differences in stability. Instead, our study suggests that decreases in individual species variabilities and increases in the relative abundance of stable dominant species may help maintain stability in the functioning of ecosystems confronted with eutrophication, disturbance, and other global changes.

Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation

Biological invasions are ‘natural’ experiments that can improve our understanding of contemporary evolution. We evaluate evidence for population differentiation, natural selection and adaptive evolution of invading plants and animals at two nested spatial scales: (i) among introduced populations (ii) between native and introduced genotypes. Evolution during invasion is frequently inferred, but rarely confirmed as adaptive. In common garden studies, quantitative trait differentiation is only marginally lower (~3.5%) among introduced relative to native populations, despite genetic bottlenecks and shorter timescales (i.e. millennia vs. decades). However, differentiation between genotypes from the native vs. introduced range is less clear and confounded by nonrandom geographic sampling; simulations suggest this causes a high false‐positive discovery rate (>50%) in geographically structured populations. Selection differentials (¦s¦) are stronger in introduced than in native species, although selection gradients (¦β¦) are not, consistent with introduced species experiencing weaker genetic constraints. This could facilitate rapid adaptation, but evidence is limited. For example, rapid phenotypic evolution often manifests as geographical clines, but simulations demonstrate that nonadaptive trait clines can evolve frequently during colonization (~two‐thirds of simulations). Additionally, QST‐FST studies may often misrepresent the strength and form of natural selection acting during invasion. Instead, classic approaches in evolutionary ecology (e.g. selection analysis, reciprocal transplant, artificial selection) are necessary to determine the frequency of adaptive evolution during invasion and its influence on establishment, spread and impact of invasive species. These studies are rare but crucial for managing biological invasions in the context of global change.

Effects of low-efficiency pollinators on plant fitness and floral trait evolution in Campanula americana (Campanulaceae)

Floral visitors vary in their pollination efficiency and their preferences for floral traits. If low-efficiency pollinators decrease the amount of pollen available to higher efficiency visitors, then low-efficiency visitors may actually have negative fitness consequences for the plants that they visit. We used experimental arrays in two populations to determine the floral preferences and the fitness effects of low-efficiency (or “ugly”) pollinators on Campanula americana. These ugly pollinators (halictid bees) preferentially visited flowers with pollen over flowers that had had their pollen removed. C. americana pollen color varies quantitatively from light tan to dark purple, and we found that natural variation in pollen color influenced the magnitude of halictid preferences for flowers with pollen. In general, preferences for flowers with pollen were stronger when the ugly pollinators foraged in arrays of flowers with tan-colored pollen than in arrays with purple-colored pollen. When plants received few visits by efficient Bombus pollinators, visits by ugly pollinators significantly decreased siring success relative to plants where visits by ugly pollinators were prevented. In contrast, ugly pollinators did not influence siring success when higher efficiency pollinators were more abundant. Thus, the relationship between low-efficiency pollinators and the plants that they visit varies from commensalistic to antagonistic depending on the presence of other pollinators in the community. Our findings suggest that the negative fitness effects and floral preferences of low-efficiency or “ugly” pollinators may contribute to the maintenance of a pollen color polymorphism in C. americana.

EVOLUTIONARY RESPONSES OF NATIVE PLANTS TO NOVEL COMMUNITY MEMBERS

Abstract Both ecological and evolutionary processes can influence community assembly and stability, and native community members may respond both ecologically and evolutionarily as additional species enter established communities. Biological invasions provide a unique opportunity to examine these responses of native community members to novel species additions. Here, I use reciprocal transplant experiments among naturally invaded and uninvaded environments, along with experimental removals of exotic species, to determine whether exotic plant competitors and exotic insect herbivores evoke evolutionary changes in native plants. Specifically, I address whether the common native plant species Lotus wrangelianus has responded evolutionarily to a series of biological invasions by adapting to the presence of the exotic plant Medicago polymorpha and the exotic insect herbivore Hypera brunneipennis. Despite differences in selection regimes between invaded and uninvaded environments and the presence of genetic variation for traits relevant to the novel competitive and plant-herbivore interactions, these experiments failed to reveal evidence that Lotus has responded evolutionarily to the double invasion of Medicago followed by H. brunneipennis. However, when herbivory from H. brunneipennis was experimentally reduced, Lotus plants from source populations invaded by Medicago outperformed plants from uninvaded source populations when transplanted into heavily invaded destination environments. Therefore, Lotus showed evidence of adaptation to Medicago invasion but not to the newer invasion of an exotic shared herbivore. The presence of this exotic insect herbivore alters the outcome of evolutionary responses in this system and counteracts adaptation by the native Lotus to invasion by the exotic plant Medicago. This result has broad implications for the conservation of native communities. While native species may be able to adapt to the presence of one or a few exotics, a multitude of invasions may limit the ability of natives to respond evolutionarily to the novel and frequently changing selection pressures that arise with subsequent invasions.

EXPERIMENTAL VERIFICATION OF ECOLOGICAL NICHE MODELING IN A HETEROGENEOUS ENVIRONMENT

The current range of ecological habitats occupied by a species reflects a combination of the ecological tolerance of the species, dispersal limitation, and competition. Whether the current distribution of a species accurately reflects its niche has important consequences for the role of ecological niche modeling in predicting changes in species ranges as the result of biological invasions and climate change. We employed a detailed data set of species occurrence and spatial variation in biotic and abiotic attributes to model the niche of a native California annual plant, Collinsia sparsiflora. We tested the robustness of our model for both the realized and fundamental niche by planting seeds collected from four populations, representing two ecotypes, into plots that fully represented the five-dimensional niche space described by our model. The model successfully predicted which habitats allowed for C. sparsiflora persistence, but only for one of the two source ecotypes. Our results show that substantial niche divergence has occurred in our sample of four study populations, illustrating the importance of adequately sampling and describing within-species variation in niche modeling.