Colin M. Orians

Herbivores, Vascular Pathways, and Systemic Induction: Facts and Artifacts

Over the past 10 years there has been tremendous growth in our understanding of molecular, chemical, and morphological induction of traits involved in the resistance of plants to herbivores. Although it is well established that the patterns of induction can be constrained by a plants vascular architecture, studies often fail to account for these constraints. Failure to do so has the potential to severely underestimate both the patterns and extent of induction. Here I review (1) the evidence for vascular control of induced responses, (2) how interspecific variation in phyllotaxy influences spatial patterning of induction, (3) the factors, phloem transport and volatile production, that may break down vascular constraints and lead to more widespread induction, and (4) the experimental approaches that could be compromised when vascular architecture is not considered. I show that vascular constraints in systemic induction are commonplace, but vary among species. I suggest that when induction is more widespread than expected from patterns of phyllotaxy, differences in vascular connectivity and volatile production may be responsible. I argue that advances in the mechanisms of systemic induction, cross-talk between different signal transduction pathways, specificity of induction, costs and benefits of systemic induction, and the effects of induced changes on herbivores and their natural enemies require that experiments be designed to examine and/or control for vascular constraints in systemic induction.

Morphological and molecular evidence for hybridization and introgression in a willow ( Salix ) hybrid zone

Hybrid zones provide biologists with the opportunity to examine genetic and ecological interactions between differentiated populations. Accurate identification of hybrid genealogies is considered a necessary prerequisite to understanding observed patterns of hybridization–related phenomena. We analysed molecular and morphological data from individuals in a hybrid zone between two species of willows (Salix sericea Marshall and S. eriocephala Michaux) and report the use of randomly amplified polymorphic DNA (RAPD), chloroplast DNA (cpDNA), and ribosomal DNA (rDNA) markers, as well as vegetative morphology and foliar chemistry data to identify individuals in terms of hybrid genealogy and to infer the direction and extent of backcrossing and introgression within the hybrid zone. A novel version of a maximum likelihood estimate approach (developed for this study) was used to calculate hybrid index scores from RAPD marker data; this method produced results similar to those obtained using traditional arithmetic methods. Distribution of rDNA, cpDNA, and chemistry data were examined within the graphical context of RAPD–based hybrid index score histograms and principal component analyses (PCA) on RAPD and morphology data. Seven of the 21 plants classified as S. eriocephala in the field were possible introgressants. Another plant presented an unequivocal example of backcrossed S. sericea chemistry and RAPD markers. Inter– and intraspecific chloroplast diversity found within the hybrid zone suggests both historic introgression (perhaps in a glacial refugium), and contemporary hybridization. Patterns of inheritance and expression within the hybrid zone suggest that morphological characters are often not expressed in a simple additive fashion, and problems associated with both morphological and molecular data are considered.

The effects of hybridization in plants on secondary chemistry: implications for the ecology and evolution of plant–herbivore interactions

Natural hybridization is a frequent phenomenon in plants. It can lead to the formation of new species, facilitate introgression of plant traits, and affect the interactions between plants and their biotic and abiotic environments. An important consequence of hybridization is the generation of qualitative and quantitative variation in secondary chemistry. Using the literature and my own results, I review the effects of hybridization on plant secondary chemistry, the mechanisms that generate patterns of chemical variation, and the possible consequences of this variation for plants and herbivores. Hybrids are immensely variable. Qualitatively, hybrids may express all of the secondary chemicals of the parental taxa, may fail to express certain parental chemicals, or may express novel chemicals that are absent in each parent. Quantitatively, concentrations of parental chemicals may vary markedly among hybrids. There are five primary factors that contribute to variation: parental taxa, hybrid class (F(1), F(2), etc.), ploidy level, chemical class, and the genetics of expression (dominance, recessive vs. additive inheritance). This variation is likely to affect the process of chemical diversification, the potential for introgression, the likelihood that hybrids will facilitate host shifts by herbivores, and the conditions that might lead to enhanced hybrid susceptibility and lower fitness.

Vascular Architecture Generates Fine Scale Variation in Systemic Induction of Proteinase Inhibitors in Tomato

Systemic induction following damage has been found in many plant species. Despite this widespread appreciation for the importance of induction, few studies have characterized the spatial variability of induction. We used tomato, Lycopersicon esculentum, to examine how damage to a single leaf affected the spatial distribution of systemic induction of proteinase inhibition in leaves above the damaged leaf. We crushed each leaflet of the second true leaf with forceps and measured the spatial distribution of proteinase inhibition in leaves 3, 4, and 5 at 8, 16, 24, 48, 72, and 120 hr. Constitutive levels of proteinase inhibitor activity were quantified in undamaged plants. We hypothesized that, due to vascular control of signal movement, systemic induction would show both among and within leaf variability. Following damage to leaf 2, induction was most pronounced in leaf 5 and minimal in leaf 3. In general, proteinase inhibitor activity was greatest at 24 hr and then declined. As predicted by vascular architecture, the near side of leaves in adjacent orthostichies showed higher induction than the far side of leaves. There was no increase in proteinase inhibitor activity in the undamaged neighboring plants. Overall our results demonstrate that systemic induction of proteinase inhibitors is partially controlled by vascular architecture and that future studies on systemic induction should examine the vascular architecture of the plants being studied. We argue that this spatial variation may influence the performance of herbivores sensitive to induced chemical changes.

Methyl jasmonate elicits rapid changes in carbon and nitrogen dynamics in tomato

• Evidence is emerging to support the notion that in response to herbivory, plants undergo changes in their primary metabolism and are able to fine-tune the allocation of new and existing resources and temporarily direct them to storage organs. • We hypothesized that simulated herbivory increases the export of resources out of the affected tissues and increases allocation to roots. We used short-lived radioisotopes to study in vivo the dynamics of newly incorporated (11)CO(2) and (13)NH(3). Methyl jasmonate (MeJA), a known defense elicitor, was applied to the foliage of tomato plants and 4 h later we monitored leaf uptake, export and whole-plant allocation of [(11)C]photosynthate and [(13)N]amino acids. • There was a marginally significant decrease in the fixation of (11)CO(2), and an increase in the export of newly acquired carbon and nitrogen out of MeJA-treated leaves. The proportion of nitrogen allocated to roots increased, whereas the proportion of carbon did not change. • These results are in agreement with our hypotheses, showing a change in the allocation of resources after treatment with MeJA; this may reduce the chance of resources being lost to herbivores and act as a buffer to biotic stress by increasing the potential for plant regrowth and survival after the attack.

Herbivore-induced resource sequestration in plants: why bother?

Herbivores can cause numerous changes in primary plant metabolism. Recent studies using radioisotopes, for example, have found that insect herbivores and related cues can induce faster export from leaves and roots and greater partitioning into tissues inaccessible to foraging herbivores. This process, termed induced resource sequestration, is being proposed as an important response of plants to cope with herbivory. Here, we review the evidence for resource sequestration and suggest that associated allocation and ecological costs may limit the benefit of this response because resources allocated to storage are not immediately available to other plant functions or may be consumed by other enemies. We then present a conceptual model that describes the conditions under which benefits might outweigh costs of induced resource sequestration. Benefits and costs are discussed in the context of differences in plant life-history traits and biotic and abiotic conditions, and new testable hypotheses are presented to guide future research. We predict that intrinsic factors related to life history, ontogeny and phenology will alter patterns of induced sequestration. We also predict that induced sequestration will depend on certain external factors: abiotic conditions, types of herbivores, and trophic interactions. We hope the concepts presented here will stimulate more focused research on the ecological and evolutionary costs and benefits of herbivore-induced resource sequestration.

Evolution of plant defenses in nonindigenous environments.

Exotic plants provide a unique opportunity to explore the evolution of defense allocation in plants. Many studies have focused on whether enemy release leads to a change in defense allocation. Little research has focused on induced defenses and on how resource availability in the nonindigenous range might cause evolutionary shifts in defense trait allocation. We examine (a) the major evolutionary hypotheses predicting defense expression in plants, (b) the hypotheses explaining defense evolution of exotic species, and (c) the importance of geographic variation in ecological interactions to defense evolution (geographic mosaics). In addition, we review the strengths and weaknesses of experimental approaches, present case studies, and suggest areas that deserve further attention.

Willow hybridization differentially affects preference and performance of herbivorous beetles

We examined the preferences and performances of five beetle species (four chrysomelids and one scarab) on two species of willows (Salix sericea and S. eriocephala) and their interspecific hybrids. Beetle species differed markedly in their responses. In preference assays, two chrysomelid beetle species (Calligrapha multipunctata bigsbyana and Plagiodera versicolora) preferred hybrids, two chrysomelids (Chrysomela scripta and Ch. Knabi) preferred hybrids and S. sericea, and the scarab beetle (Popillia japonica) preferred S. eriocephala. Experiments with purified salicortin indicated that salicortin concentration may contribute to these preferences.

Secondary chemistry of hybrid and parental willows: Phenolic glycosides and condensed tannins inSalix sericea, S. eriocephala, and their hybrids

Salix sericea andS. eriocephala differ markedly in secondary chemistry.S. sericea produces phenolic glycosides, salicortin and 2′-cinnamoylsalicortin, and low concentrations of condensed tannin. In contrast,S. eriocephala produces no phenolic glycosides, but high concentrations of condensed tannins. Hybrid chemistry is intermediate for both types of chemicals, suggesting predominantly additive inheritance of these two defensive chemical systems from the parental species. However, there is extensive variation among hybrids. This variation may be due to genetic variation among parental genotypes, which genes were passed on, or to subsequent back-crossing. The differences in chemistry are likely to exert a strong effect on the relative susceptibility of hybrid and parental willows to herbivores.

Genetic and soil-nutrient effects on the abundance of herbivores on willow

The effects of soil-nutrient environment, plant genotype, and the interaction between the two on the resistance of the willow, Salix sericea, to insect species in a diverse herbivore community was measured. We found that soil-nutrient environment influenced plant growth and the abundance of most herbivores of S. sericea. However, environmental effects on herbivore abundance were often modified by plant genetics; the abundance of four of seven herbivores exhibited significant genotypeby-environment interaction effects. Pure genotype effects were mostly small and non-significant. The effects of fertilization differed among herbivores. Several herbivores were more abundant on fertilized plants, one was less abundant, and the abundance of others did not change. We found that feeding guild was a poor predictor of herbivore response. Finally we found significant phenotypic and genetic correlations among growth rate, internode length, and the abundances of several herbivores.