The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa

Although the evolution of plant response to herbivory can involve either resistance (a decrease in susceptibility to herbivore damage) or tolerance (a decrease in the per unit effect of herbivory on plant fitness), until recently few studies have explicitly incorporated both of these characters. Moreover, theory suggests these characters do not evolve independently, and also that the pattern of natural selection acting on resistance and tolerance depends on their costs and benefits. In a genotypic selection analysis on an experimental population of Brassica rapa (Brassicaceae) I found a complex set of correlational selection gradients acting on resistance and tolerance of damage by flea beetles (Phyllotreta cruciferae: Chrysomelidae) and weevils (Ceutorhynchus assimilis: Curculionidae), as well as directional and stabilizing selection on resistance to attack by weevils. Evolution of response to flea beetle attack is constrained by a strong allocation cost of tolerance, and this allocation cost may be caused by a complex correlation among weevil resistance, weevil tolerance, flea beetle resistance, and flea beetle tolerance. Thus, one important conclusion of this study is that ecological costs may involve complex correlations among multiple characters, and for this reason these costs may not be detectable by simple pairwise correlations between characters. The evolution of response to weevil attack is probably constrained by a series of correlations between weevil resistance, weevil tolerance, and fitness in the absence of weevil damage, and possibly by a cost of tolerance of weevil damage. However, the nature of these constraints is complicated by apparent overcompensation for weevil damage. Because damage by both flea beetles and weevils had non-linear effects on plant fitness, standard measures of tolerance were not appropriate. Thus, a second important contribution of this study is the use of the area under the curve defined by the regression of fitness on damage and damage-squared as a measure of tolerance. This revised version was published online in July 2006 with corrections to the Cover Date.     

EVOLUTIONARY ECOLOGY OF DATURA STRAMONIUM L. IN CENTRAL MEXICO: NATURAL SELECTION FOR RESISTANCE TO HERBIVOROUS INSECTS

It has been assumed that herbivores constitute a selective agent for the evolution of plant resistance. However, few studies have tested this hypothesis. In this study, we look at the annual weed Datura stramonium for evidence of current natural selection for resistance to herbivorous insects. Paternal half-sib families obtained through controlled crosses were exposed to herbivores under natural conditions. The plants were damaged by two folivorous insects: the tobacco flea beetle Epitrix parvula and the grasshopper Sphenarium purpurascens. Selection was estimated using a multiple-regression analysis of plant size and of damage by the two herbivores on plant fitness measured as fruit production for both individual phenotypes and family breeding values (genetic analysis). Directional phenotypic selection was detected for both larger plant size and lower resistance to the flea beetles, whereas stabilizing phenotypic selection was revealed for resistance to S. purpurascens. However, performing the same analyses on the breeding values of the characters revealed directional and stabilizing selection only for plant size. Thus, no agreement existed between the results of the two types of analyses, nor was there any detectable potential for genetic change in the studied population because of selection on herbivore resistance. The narrow-sense heritability of every trait studied was small (all <0.1) and not different from zero. The potential for evolutionary response to natural selection for higher resistance to herbivores in the studied population of D. stramonium is probably limited by lack of genetic variation. Natural selection acts on phenotypes, and the detection of phenotypic selection on resistance to herbivores confirms their ecological importance in determining plant fitness. However, evolutionary inferences based solely on phenotypic selection analyses must be interpreted with caution.     

PAIRWISE VERSUS DIFFUSE NATURAL SELECTION AND THE MULTIPLE HERBIVORES OF SCARLET GILIA,IPOMOPSIS AGGREGATA

Recent theoretical studies have argued that plant-herbivore coevolution proceeds in a diffuse rather than a pairwise manner in multispecies interactions when at least one of two conditions are met: (1) genetic correlations exist between plant resistances to different herbivore species; and (2) ecological interactions between herbivores sharing a host plant cause nonadditive impacts of herbivory on plant fitness. We present results from manipulative field experiments investigating the single and interactive fitness effects of three types of herbivory on scarlet gilia (Ipomopsis aggregata) over two years of study. We utilize these data to test whether selection imposed by herbivore attack on date of first flowering is pairwise (independent) or diffuse (dependent) in nature. Our results reveal complex patterns of the fitness effect of herbivores. Simulated early season browsing had a strong negative fitness effect on plants and also reduced subsequent insect attack. Surprisingly, this ecological interaction did not translate into significant interactions between clipping and insect manipulations on plant fitness. However, we detected a significant interaction between seed fly and caterpillar herbivory on plant fitness, with the negative effect of either insect being greatest when occurring alone. These results suggest that herbivore-imposed selection may have pairwise and diffuse components. In our selection analysis of flowering phenology, we discovered significant pairwise linear selection imposed by clipping, diffuse linear selection imposed by insects, and diffuse nonlinear selection imposed by clipping and insect attack acting simultaneously. Our results reveal that the evolution of flowering phenology in scarlet gilia may be in response to diffuse and pairwise natural selection imposed by multiple herbivores. We discuss the evolution of resistance characters in light of diffuse versus pairwise forms of linear and nonlinear selection and stress the complexity of selection imposed by suites of interacting species.     

Consequences of sequential attack for resistance to herbivores when plants have specific induced responses

Plants in nature are attacked sequentially by herbivores, and theory predicts that herbivore-specific responses allow plants to tailor their defenses. We present a novel field test of this hypothesis, and find that specific responses of Solanum dulcamara lead to season-long consequences for two naturally colonizing herbivores, irrespective of the second herbivore to attack plants. This result indicates that responses induced by the initial herbivore made plants less responsive to subsequent attack. We show that initial herbivory by flea beetles and tortoise beetles induce distinct plant chemical responses. Initial herbivory by flea beetles lowered the occurrence of conspecifics and tortoise beetles relative to controls. Conversely, initial herbivory by tortoise beetles did not influence future herbivory. Remarkably, the experimentally imposed second herbivore to feed on plants did not modify consequences (induced resistance or lack thereof) of the first attacker. Induction of plant chemical responses was consistent with these ecological effects; i.e. the second herbivore did not modify the plant's initial induced response. Thus, canalization of the plant resistance phenotype may constrain defensive responses in a rapidly changing environment.     

Effects of two types of herbivores on the population dynamics of a perennial herb

The joint effects of multiple herbivores on their shared host plant have received increasing interest recently. The influence of herbivores on population dynamics of their host plants, especially the relative roles of different types of damage, is, however, still poorly understood. Here, we present a modelling approach, including both deterministic and stochastic matrix modelling, to be used in estimating fitness effects of multiple herbivores on perennial plants. We examined the effects and relative roles of two specialist herbivores, a pre-dispersal seed predator, Euphranta connexa, and a leaf-feeding moth, Abrostola asclepiadis, on the population dynamics and long-term fitness of their shared host plant, a long-lived perennial herb Vincetoxicum hirundinaria (Asclepiadaceae). We collected demographic data during 3 years and combined these data with the effects of natural levels of herbivory measured from the same individuals. We found that both seed predation and leaf herbivory reduced population growth of V. hirundinaria, but only very high damage levels changed the growth trend of the vigorously growing study populations from positive to negative. Demographic modelling indicated that seed predation had a greater impact on plant population growth than leaf herbivory. The effect of leaf herbivory was weaker and diminished with increasing level of seed predation. Evaluation of individual fitness components, however, suggested that leaf herbivory contributed more strongly to host plant fitness than seed predation. Our results emphasize that understanding the effects of a particular herbivore on plant population dynamics requires also knowledge on other herbivores present in the system, because the effect of a particular type of herbivory on plant population dynamics is likely to vary according to the intensity of other types of herbivory. Furthermore, evaluating herbivore impact from using individual fitness components does not necessarily reflect the long-term effects on total plant fitness.     

Herbivory and natural selection on flowering phenology in wild sunflower, Helianthus annuus

Plant fitness is strongly affected by flowering phenology, and there are several ecological factors that are thought to shape the distribution of flowering times. One relatively underexamined factor is the timing and intensity of attack by herbivores that feed on flowers or developing seeds. This study tests the hypothesis that herbivores that feed on developing seeds of wild sunflower, Helianthus annuus (Asteraceae), impose selection on flowering phenology. First, the study population was found to contain genetic variation for mean date of flowering, so this trait could evolve if natural selection were operating. Next, the phenological pattern of abundance of five seed-feeding herbivores was documented. Damage by three herbivores, Haplorhynchites aeneus (Cucurlionidae), the head-clipping weevil, Homoeosoma electellum (Lepidoptera: Pyralidae), the sunflower moth, and Suleima helianthana (Lepidoptera: Tortricidae), the sunflower bud moth, was highest early in the flowering season, and declined as the season progressed. Damage by one herbivore, the seed fly Gymnocarena diffusa (Diptera: Tephrididae), was lowest early in the flowering season and increased as the season progressed. Finally, damage by two seed weevils, Smicronyx fulvus and S. sordidus (Curculionidae), whose damage was not distinguished, was constant through the flowering period. Third, damage by Haplorhynchites, Homoeosoma, and Suleima was found to be detrimental to plant fitness, suggesting that plants that flower when these herbivores are not abundant should have higher fitness. Finally, two phenotypic selection analyses were performed. The first included damage by Homoeosoma and Suleima, as well as flowering date, leaf area, and inflorescence diameter, as characters predicting plant fitness. In this analysis directional selection was found to act to decrease damage by the two herbivores, but did not act on flowering date. The second selection analysis was identical except that damage by the two herbivores was not included. In this analysis significant directional selection was found to favor later-flowering plants. Comparison of these two analyses suggests that all selection on flowering phenology is attributable to damage by Homoeosoma and Suleima: plants that flower later avoid damage by these two herbivores. While other influences on flowering phenology, such as pollination, mate availability, and seasonality, have been well documented, this study is one of few to demonstrate natural selection on flowering phenology that is a direct consequence of insect attack. Received: 17 November 1998 / Accepted: 18 July 1999     

Heterogeneity of plant phenotypes caused by herbivore-specific induced responses influences the spatial distribution of herbivores

Abstract.  1. Herbivory can induce resistance in a plant and the induced phenotype may be disfavoured by subsequent herbivores. Yet, as the distance between plants in a population increases, limited mobility may make a herbivore more likely to feed and oviposit on host plants in its immediate surroundings.
2. The present study tested whether a herbivore's preference and distribution across plants with different induced phenotypes was influenced by the spatial distribution of plants. A fragmented population of Solanum dulcamara plants was created. This consisted of discrete, spatially separated patches with different histories of damage, either herbivory from adult flea beetles ( Psylliodes affinis ), tortoise beetles ( Plagiometriona clavata ), or mechanical damage. Each patch was separated by 7 m and consisted of 12 plants that were spaced 30 cm apart. Then a fixed number of adult tortoise beetles were introduced to each patch, and movement and oviposition within and between spatially separate homogeneous patches (receiving one type of damage) were compared with movement and oviposition within heterogeneous patches (containing all three types of damage) over the growing season.
3. Flea beetle and tortoise beetle herbivory consistently induced different phytochemical responses in S. dulcamara (polyphenol oxidase and peroxidase), and adult tortoise beetles avoided oviposition on the flea beetle induced plants within heterogeneous patches. However, between homogeneous patches, plant phenotype did not influence oviposition. Colonisation by naturally occurring flea beetle adults followed a similar pattern.
4. These results suggest that the heterogeneity of plant phenotypes can influence herbivore choice and distribution at small but not large spatial scales.     

Cost of trichome production and resistance to a specialist insect herbivore in <Emphasis Type="Italic">Arabidopsis lyrata</Emphasis>

Theory predicts that trade-offs between resistance to herbivory and other traits positively affecting fitness can maintain genetic variation in resistance within plant populations. In the perennial herb Arabidopsis lyrata, trichome production is a resistance trait that exhibits both qualitative and quantitative variation. Using a paternal half-sib design, we conducted two greenhouse experiments to ask whether trichomes confer resistance to oviposition and leaf herbivory by the specialist moth Plutella xylostella, and to examine potential genetic constraints on evolution of increased resistance and trichome density. In addition, we examined whether trichome production is induced by insect herbivory. We found strong positive genetic and phenotypic correlations between leaf trichome density and resistance to leaf herbivory, demonstrating that the production of leaf trichomes increases resistance to leaf damage by P. xylostella. Also resistance to oviposition tended to increase with increasing leaf trichome density, but genetic and phenotypic correlations were not statistically significant. Trichome density and resistance to leaf herbivory were negatively correlated genetically with plant size in the absence of herbivores, but not in the presence of herbivores. There was no evidence of increased trichome production after leaf damage by P. xylostella. The results suggest that trichome production and resistance to leaf herbivory are associated with a cost and that the direction of selection on resistance and trichome density depends on the intensity of herbivory.     

Latitudinal variation in resistance and tolerance to herbivory in the perennial herb Lythrum salicaria is related to intensity of herbivory and plant phenology

Both the length of the growing season and the intensity of herbivory often vary along climatic gradients, which may result in divergent selection on plant phenology, and on resistance and tolerance to herbivory. In Sweden, the length of the growing season and the number of insect herbivore species feeding on the perennial herb Lythrum salicaria decrease from south to north. Previous common‐garden experiments have shown that northern L. salicaria populations develop aboveground shoots earlier in the summer and finish growth before southern populations do. We tested the hypotheses that resistance and tolerance to damage vary with latitude in L. salicaria and are positively related to the intensity of herbivory in natural populations. We quantified resistance and tolerance of populations sampled along a latitudinal gradient by scoring damage from natural herbivores and fitness in a common‐garden experiment in the field and by documenting oviposition and feeding preference by specialist leaf beetles in a glasshouse experiment. Plant resistance decreased with latitude of origin, whereas plant tolerance increased. Oviposition and feeding preference in the glasshouse and leaf damage in the common‐garden experiment were negatively related to damage in the source populations. The latitudinal variation in resistance was thus consistent with reduced selection from herbivores towards the northern range margin of L. salicaria. Variation in tolerance may be related to differences in the timing of damage in relation to the seasonal pattern of plant growth, as northern genotypes have developed further than southern have when herbivores emerge in early summer.     

Contrary effects of jasmonate treatment of two closely related plant species on attraction of and oviposition by a specialist herbivore

Elevated jasmonic acid (JA) concentrations in response to herbivory can induce wounded plants to produce defences against herbivores. In laboratory and field experiments we compared the effects of exogenous JA treatment to two closely related cabbage species on the host‐searching and oviposition preference of the diamondback moth (DBM), Plutella xylostella. JA‐treated Chinese cabbage (Brassica campestris) was less attractive than untreated Chinese cabbage to ovipositing DBM, while JA‐treatment of common cabbage (B. oleracea) made plants more attractive than untreated controls for oviposition by this insect. Similar effects were observed when plants of the two species were damaged by DBM larvae. In the absence of insect‐feeding, or JA application, Chinese cabbage is much more attractive to DBM than common cabbage. Inducible resistance therefore appears to occur in a more susceptible plant and induced susceptibility appears to occur in a more resistant plant, suggesting a possible balance mechanism between constitutive and inducible defences to a specialist herbivore.     

ECOLOGICAL COSTS OF PLANT RESISTANCE TO HERBIVORES IN THE CURRENCY OF POLLINATION

In this paper, we examine how ecological costs of resistance might be manifested through plant relationships with pollinators. If defensive compounds are incorporated into floral structures or if they are sufficiently costly that fewer rewards are offered to pollinators, pollinators may discriminate against more defended plants. Here we consider whether directional selection for increased resistance to herbivores could be constrained by opposing selection through pollinator discrimination against more defended plants. We used artificial selection to create two populations of Brassica rapa plants that had high and low myrosinase concentrations and, consequently, high and low resistance to flea beetle herbivores. We measured changes in floral characters of plants in both damaged and undamaged states from these populations with different resistances to flea beetle attack. We also measured pollinator visitation to plants, including numbers of pollinators and measures of visit quality (numbers of flowers visited and time spent per flower). Damage from herbivores resulted in reduced petal size, as did selection for high resistance to herbivores later in the plant lifetime. In addition, floral display (number of open flowers) was also altered by an interaction between these two effects. Changes in floral traits translated into overall greater use of low-resistance, undamaged plants based on total amount of time pollinators spent foraging on plants. Total numbers of pollinators attracted to plants did not differ among treatments; however, pollinators spent significantly more time per flower on plants from the low-resistance population and tended to visit more flowers on these plants as well. Previous work by other investigators on the same pollinator taxa has shown that longer visit times are associated with greater male and female plant fitness. Because initial numbers of pollinators did not differ between selection regimes, palatability and/or amount of rewards offered by high- and low-resistance populations are likely to be responsible for these patterns. During periods of pollinator limitation, less defended plants may have a selective advantage and pollinator preferences may mediate directional selection imposed by herbivores. In addition, if pollinator preferences limit seed set in highly defended plants, then lower seed set previously attributed to allocation costs of defense may also reflect greater pollinator limitation in these plants relative to less defended plants.     

Jasmonate-mediated induced plant resistance affects a community of herbivores

1. The negative effect of induced plant resistance on the preference and performance of herbivores is a well‐documented ecological phenomenon that is thought to be important for both plants and herbivores. This study links the well‐developed mechanistic understanding of the biochemistry of induced plant resistance in the tomato system with an examination of how these mechanisms affect the community of herbivores in the field. 2. Several proteins that are induced in tomato foliage following herbivore damage have been linked causally to reductions in herbivore performance under laboratory conditions. Application of jasmonic acid, a natural elicitor of these defensive proteins, to tomato foliage stimulates induced responses to herbivory. 3. Jasmonic acid was sprayed on plants in three doses to generate plants with varying levels of induced responses, which were measured as increases in the activities of proteinase inhibitors and polyphenol oxidase. 4. Field experiments conducted over 3 years indicated that induction of these defensive proteins is associated with decreases in the abundance of all four naturally abundant herbivores, including insects in three feeding guilds, caterpillars, flea beetles, aphids, and thrips. Induced resistance killed early instars of noctuid caterpillars. Adult flea beetles strongly preferred control plants over induced plants, and this effect on host plant preference probably contributed to differences in the natural abundance of flea beetles. 5. The general nature of the effects observed in this study suggests that induced resistance will suppress many members of the herbivore community. By linking plant biochemistry, insect preference, performance, and abundance, tools can be developed to manipulate plant resistance sensibly and to predict its outcome under field conditions.     

The effect of rhizosphere microbes outweighs host plant genetics in reducing insect herbivory

Rhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, a direct comparison of the relative influence of rhizosphere microbes versus plant genetics on herbivory levels and on metabolites related to defence is lacking. In the crucifer Boechera stricta, we tested the effects of rhizosphere microbes and plant population on herbivore resistance, the primary metabolome, and select secondary metabolites. Plant populations differed significantly in the concentrations of six glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae. The population with lower GLS levels experienced ~60% higher levels of aphid (Myzus persicae) attack; no association was observed between GLS and damage by a second herbivore, flea beetles (Phyllotreta cruciferae). Rhizosphere microbiome (disrupted vs. intact native microbiome) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively about three‐ and seven‐fold higher among plants grown in the disrupted versus intact native microbiome treatment. These differences may be attributable to shifts in primary metabolic pathways previously implicated in host defence against herbivores, including increases in pentose and glucoronate interconversion among plants grown with an intact microbiome. Furthermore, native microbiomes with distinct community composition (as estimated from 16s rRNA amplicon sequencing) differed two‐fold in their effect on host plant susceptibility to aphids. The findings suggest that rhizosphere microbes, including distinct native microbiomes, can play a greater role than population in defence against insect herbivores, and act through metabolic mechanisms independent of population.     

Diffuse interactions between two herbivores and constraints on the evolution of resistance in horsenettle (<Emphasis Type="Italic">Solanum carolinense</Emphasis>)

Interactions between plants and herbivores are considered “diffuse” if the ecological interactions between two species, or their evolutionary responses, differ depending on the presence of a third species. I looked for evidence of diffuse interactions among horsenettle (Solanum carolinense) and two common herbivores. Plants experimentally protected from lace bugs (Gargaphia solani) were twice as susceptible to attack from flea beetles (Epitrix fuscula) once transplanted into the field. Thus, the selective benefit to horsenettle of resistance against lace bugs in nature would likely be diminished by increased attack from flea beetles. Moreover, the relative rank among horsenettle genotypes for resistance against flea beetles was changed by prior exposure to lace bugs. Thus, the genetic expression of resistance to flea beetles would depend on the “lace bug environment.” By affecting selective pressures or response to selection, these sorts of diffuse interactions in a plant-herbivore community can slow the host plant’s evolution of resistance to its herbivores.     

Genetic and sexual separation between insect resistant and susceptible Barbarea vulgaris plants in Denmark

Co‐evolution between herbivores and plants is believed to be one of the processes creating Earth’s biodiversity. However, it is difficult to disentangle to what extent diversification is really driven by herbivores or by other historical‐geographical processes like allopatric isolation. In the cruciferous plant Barbarea vulgaris, some Danish individuals are resistant to herbivory by flea beetles (Phyllotreta nemorum), whereas others are not. The flea beetles are, in parallel, either resistant or susceptible to the plants defenses. To understand the historical‐evolutionary framework of these interactions, we tested how genetically divergent resistant and susceptible plants are, using microsatellite markers. To test whether they are reproductively fully compatible, resistant and susceptible plants were grown intermixed in an outdoor experiment, and the paternity of open‐pollinated offspring was determined by analysis of molecular markers. Resistant and susceptible Danish plants were genetically strongly differentiated and produced significantly fewer hybrids than expected from random mating or nearest neighbour mating. Our results suggest that the two types belong to different evolutionary lineages that have been (partly) isolated at some time, during which genetic and reproductive divergence evolved. A parsimonious scenario could be that the two plant types were isolated in different refugia during the previous ice age, from which they migrated into and met in Denmark and possibly neighbouring regions. If so, resistance and susceptibility has for unknown reasons become associated with the different evolutionary lineages.     

Tests of associational defence provided by hairy plants for glabrous plants of Arabidopsis halleri subsp. gemmifera against insect herbivores

1. Trichome‐producing (hairy) and trichomeless (glabrous) plants of Arabidopsis halleri subsp. gemmifera were investigated to test whether plant resistance to herbivory depends on the plants' phenotypes and/or the phenotypes of neighbouring plants (associational effects). 2. A common garden experiment was conducted in which the relative frequency of hairy and glabrous plants was manipulated. Two species of leaf‐chewing insects (larvae of a white butterfly and a cabbage sawfly) were found less often on hairy plants than on glabrous plants. By contrast, the numbers of aphids and flea beetles did not differ significantly between hairy and glabrous plants. For none of these insects did abundance depend on the frequency of the two plant morphs. 3. A field survey was conducted in two natural populations of A. halleri. In the first population, a species of white butterfly was the dominant herbivore, and hairy plants incurred less leaf damage than glabrous plants across 2 years. By contrast, in the other population, where flea beetles were dominant, there were no consistent differences in leaf damage between the two types of plants. In neither of the two populations was any evidence found of associational effects. 4. This study did not provide any conclusive evidence of associational effects of anti‐herbivore resistance, but it was discovered that trichomes can confer resistance to certain herbivores. Given the results of previous work by the authors on associational effects against a flightless leaf beetle, such associational effects of the trichome dimorphism of A. halleri were herbivore‐specific.     

COST OF GLANDULAR TRICHOMES,A “RESISTANCE” CHARACTER IN DATURA WRIGHTII REGEL (SOLANACEAE)

Models regarding the evolution of plant resistance to herbivory often assume that the primary mechanism maintaining resistance polymorphisms is the balance between benefits of increased resistance to herbivores and costs associated with the production of a resistance character. However, rarely has it been demonstrated that genetically based resistance traits are costly. Here, we document costs associated with the production of glandular trichomes, a resistance character in Datura wrightii that is predominantly under the control of a single gene of large effect. In the absence of herbivores, plants with glandular trichomes (sticky) produced 45% fewer viable seeds than plants with nonglandular trichomes (velvety). Although both plant types flowered with similar frequency, sticky plants matured fewer capsules and fewer of their seeds germinated. The fitness difference between the types in herbivore-free conditions was not mitigated by the addition of water, a potentially limiting resource for sticky plants. Under herbivore pressure, there was no significant fitness difference between the types, although the fitness of velvety plants was still higher than that of sticky plants. This occurred even though velvety plants sustained more herbivore damage than sticky plants and were more likely to be attacked by most herbivore species present. The fitness difference between the plant types was especially reduced when herbivore-attacked plants were watered, which indicates that sticky plants may have higher tolerance for damage than velvety plants when supplied with a potentially limiting resource. Yet, the maintenance of a fitness deficit (albeit small and nonsignificant) for sticky plants when attacked by herbivores indicates no net benefit associated with the production of glandular trichomes in this first year of our study. These results add to our current understanding that herbivore resistance characters can be costly and raise the question of how this genetic polymorphism is maintained in wild populations.     

Overcompensating plants: their expression of resistance traits and effects on herbivore preference and performance

Overcompensation is a plant tolerance response in which plants have higher fitness after herbivory than without damage. Although it has been demonstrated that plants are able to simultaneously express resistance and tolerance traits, it remains unclear whether overcompensating plants are also inducing resistance‐mediating secondary metabolite production and how herbivores perform on plants that overcompensate. Our previous work has shown that a potato variety [Solanum tuberosum L. cv. Pastusa Suprema (Solanaceae)] from Colombia can express overcompensatory responses to damage by larvae of the Guatemalan potato moth, Tecia solanivora Povolny (Lepidoptera: Gelechiidae). Here we investigated (1) whether potatoes that express overcompensatory responses also induce resistance traits and (2) how the previous damage affects Guatemalan potato moth preference and performance. Our results show that larval feeding not only systemically induces higher tuber biomass but also an increased production of resistance‐related compounds, such as phenolics and proteinase inhibitors. Pupal mass increased with increasing tuber size, whereas changes in tuber secondary metabolism did not correlate with any metric of larval performance. Oviposition preference did not change between induced and undamaged plants. Our data show that potato plants expressing overcompensatory responses also induce secondary compounds known to increase resistance against herbivores. However, the induced response was relatively small, reducing the opportunities for a negative effect on the herbivore. Hypotheses for why larvae perform better in larger tubers and are not affected by the secondary metabolism are discussed. From an ecological and agricultural point of view, our results suggest that the expression of overcompensatory traits could have positive effects on herbivore performance.     

Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants

Plants are often attacked by pathogens and insects. Their combined impact on plant performance and fitness depends on complicated three-way interactions and the plant’s ability to compensate for resource losses. Here, we evaluate the response of Barbarea vulgaris, a wild crucifer, to combined attack by an oomycete Albugo sp., a plant pathogen causing white rust, and a flea beetle, Phyllotreta nemorum. Plants from two B. vulgaris types that differ in resistance to P. nemorum were exposed to Albugo and P. nemorum alone and in combination and then monitored for pathogen infection, herbivore damage, defence compounds, nutritional quality, biomass and seed production. Albugo developed infections in the insect-resistant plants, whereas insect-susceptible plants were scarcely infected. Concentrations of Albugo DNA were higher in plants also exposed to herbivory; similarly, flea beetle larvae caused more damage on Albugo-infected plants. Concentrations of saponins and glucosinolates strongly increased when the plants were exposed to P. nemorum and when the insect-susceptible plants were exposed to Albugo, and some of these compounds increased even more in the combined treatment. The biomass of young insect-susceptible plants was lower following exposure to flea beetles, and the number of leaves of both plant types was negatively affected by combined exposure. After flowering, however, adult plants produced similar numbers of viable seeds, irrespective of treatment. Our findings support the concept that pathogens and herbivores can affect each other’s performance on a host plant and that the plant reacts by inducing specific and general defences. However, plants may be able to compensate for biomass loss from single and combined attacks over time.