Between-Population Outbreeding Affects Plant Defence

Between-population crosses may replenish genetic variation of populations, but may also result in outbreeding depression. Apart from direct effects on plant fitness, these outbreeding effects can also alter plant-herbivore interactions by influencing plant tolerance and resistance to herbivory. We investigated effects of experimental within- and between-population outbreeding on herbivore resistance, tolerance and plant fitness using plants from 13 to 19 Lychnis flos-cuculi populations. We found no evidence for outbreeding depression in resistance reflected by the amount of leaf area consumed. However, herbivore performance was greater when fed on plants from between-population compared to within-population crosses. This can reflect outbreeding depression in resistance and/or outbreeding effects on plant quality for the herbivores. The effects of type of cross on the relationship between herbivore damage and plant fitness varied among populations. This demonstrates how between-population outbreeding effects on tolerance range from outbreeding depression to outbreeding benefits among plant populations. Finally, herbivore damage strengthened the observed outbreeding effects on plant fitness in several populations. These results raise novel considerations on the impact of outbreeding on the joint evolution of resistance and tolerance, and on the evolution of multiple defence strategies.     

Simultaneous inbreeding modifies inbreeding depression in a plant–herbivore interaction

Because inbreeding is common in natural populations of plants and their herbivores, herbivore‐induced selection on plants, and vice versa, may be significantly modified by inbreeding and inbreeding depression. In a feeding assay with inbred and outbred lines of both the perennial herb, Vincetoxicum hirundinaria, and its specialist herbivore, Abrostola asclepiadis, we discovered that plant inbreeding increased inbreeding depression in herbivore performance in some populations. The effect of inbreeding on plant resistance varied among plant and herbivore populations. The among‐population variation is likely to be driven by variation in plant secondary compounds across populations. In addition, inbreeding depression in plant resistance was substantial when herbivores were outbred, but diminished when herbivores were inbred. These findings demonstrate that in plant–herbivore interactions expression of inbreeding depression can depend on the level of inbreeding of the interacting species. Furthermore, our results suggest that when herbivores are inbred, herbivore‐induced selection against self‐fertilisation in plants may diminish.     

Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage

Intraspecific plant diversity can modify the properties of associated arthropod communities and plant fitness. However, it is not well understood which plant traits determine these ecological effects. We explored the effect of intraspecific chemical diversity among neighbouring plants on the associated invertebrate community and plant traits. In a common garden experiment, intraspecific diversity among neighbouring plants was manipulated using three plant populations of wild cabbage that differ in foliar glucosinolates. Plants were larger, harboured more herbivores, but were less damaged when plant diversity was increased. Glucosinolate concentration differentially correlated with generalist and specialist herbivore abundance. Glucosinolate composition correlated with plant damage, while in polycultures, variation in glucosinolate concentrations among neighbouring plants correlated positively with herbivore diversity and negatively with plant damage levels. The results suggest that intraspecific variation in secondary chemistry among neighbouring plants is important in determining the structure of the associated insect community and positively affects plant performance.     

Transgenerational effects alter plant defence and resistance in nature

Trichomes, or leaf hairs, are epidermal extensions that take a variety of forms and perform many functions in plants, including herbivore defence. In this study, I document genetically determined variation, within‐generation plasticity, and a direct role of trichomes in herbivore defence for Mimulus guttatus. After establishing the relationship between trichomes and herbivory, I test for transgenerational effects of wounding on trichome density and herbivore resistance. Patterns of interannual variation in herbivore density and the high cost of plant defence makes plant–herbivore interactions a system in which transgenerational phenotypic plasticity (TPP) is apt to evolve. Here, I demonstrate that parental damage alters offspring trichome density and herbivore resistance in nature. Moreover, this response varies between populations. This is among the first studies to demonstrate that TPP contributes to variation in nature, and also suggests that selection can modify TPP in response to local conditions.     

Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata (Fabaceae)

The benefits of ant–plant–herbivore interactions for the plant depend on the abundance of ants and herbivores and the selective pressures these arthropods exert. In plants bearing extrafloral nectaries (EFN), different mean trait values may be selected for by different populations in response to local herbivore pressure, ultimately resulting in the evolution of differences in plant traits that attract ants as defensive agents against herbivory. To determine if variation in traits that mediate ant–plant interactions reflect herbivore selective pressures, we quantified intra- and inter-population variation in plant traits for eight populations of the EFN-bearing annual Chamaecrista fasciculata (Michx.) (Fabaceae). Censuses in rural and urban areas of Missouri and Illinois (USA) showed population differences in ant attendance and herbivore pressure. Seeds were collected from each population, and plants were grown in a common greenhouse environment to measure sugar production, nectar volume and composition, EFN size and time of emergence, leaf pubescence, and leaf quality throughout plant development. Populations varied mainly in terms of nectary size, sugar production, and nectar volume, but to a lesser degree in leaf pubescence. Populations of C. fasciculata within urban areas (low in insect abundance) had small nectaries and the lowest nectar production. There was a positive correlation across populations between herbivore density and leaf damage by those herbivores on the one hand and sugar production and nectar volume on the other. These results, in conjunction with lack of evidence for maternally based environmental effects, suggest that population differences in herbivore damage have promoted differential evolution of EFN-related traits among populations. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae)

Previous studies have demonstrated genetic variation for resistance to insect herbivores and host plant quality. The effect of plant mating system, an important determinant of the distribution of genetic variation, on host plant characteristics has received almost no attention. This study used a controlled greenhouse experiment to examine the effect of self- and cross-pollination in Mimulus guttatus (Scrophulariaceae) on resistance to and host plant quality for the xylem-feeding spittlebug Philaenus spumarius (Homoptera: Cercopidae). Spittlebugs were found to have a negative effect on two important fitness components in M. guttatus, flower production and above ground biomass. One of two M. guttatus populations examined showed a significant interaction between the pollination and herbivore treatments. In this case, the detrimental effects of herbivores on biomass and flower production were much more pronounced in inbred (self) plants. The presence of spittlebug nymphs increased inbreeding depression by as much as three times. Pollination treatments also had significant effects on important components of herbivore fitness, but these effects were in opposite directions in our two host plant populations. Spittlebug nymphs maturing on self plants emerged as significantly larger adults in one of our host plant populations, indicating that inbreeding increased host plant quality. In our second host plant population, spittlebug nymphs took significantly longer to develop to adulthood on self plants, indicating that inbreeding decreased host plant quality. Taken together these results suggest that the degree of inbreeding in host plant populations can have important and perhaps complex effects on the dynamics of plant-herbivore interactions and on mating-system evolution in the host.     

Relative importance of drought,soil quality,and plant species in determining the strength of plant–herbivore interactions

1. Although studies on plant–herbivore interactions comparing different plant species are common, little is known about the importance of environmental conditions in determining variation in herbivory within single plant species. 2. This study assessed the effects of experimentally manipulated nutrient and water availability on plant palatability, and compared these differences with differences among species. The extent to which these patterns can be explained by leaf toughness and specific leaf area was also investigated. Six plant species from the subfamily Carduoideae and four free‐living leaf chewing invertebrates were used in the study. 3. Herbivore preferences were significantly affected by soil nutrients and water regime and varied among plant as well as herbivore species. Generally, herbivores preferred watered plants and plants from nutrient‐poor soil. The effects of soil nutrients and water regime differed between the plant and herbivore species. The differences between the plant species were greater than those between the environmental treatments. Differences at both levels could be partly explained by leaf toughness and specific leaf area. Leaf toughness, in particular, turned to be an important predictor indicating that herbivores preferred species with softer leaves, and species from wetter conditions with reduced leaf toughness. 4. The environmental conditions in which plants are growing have significant effects on plant palatability. Between‐species comparisons thus need to pay attention to this variation. Future studies may consider how the effects of current conditions interact with conditions of plant origin to predict possible effects of changes in environmental conditions on the intensity of plant–herbivore interactions.     

Local variation in plant quality influences large‐scale population dynamics

Spatial variation in ecological systems can arise both as a consequence of variation in the quality and availability of resources and as an emergent property of spatially structured interactions. We used a spatially explicit model to simulate populations of herbivore hosts and their parasitoids in landscapes with different levels of variance in plant patch quality and different spatial arrangements of high‐ and low‐quality plant patches. We found that even small variation in patch quality at a fine spatial scale decreased overall herbivore populations, as parasitoid populations on low‐quality plant patches were subsidized by those from high‐quality neighbors. On landscapes with large, homogeneous regions of high‐ and low‐quality plant patches, herbivore populations increased with variation in patch quality. Overall, our results demonstrate that local variation in resource quality profoundly influences global population dynamics. In particular, fine‐scale variation in plant patch quality enhanced biological control of herbivores by parasitoids, suggesting that adding back plant genetic variation into perennial production systems may enhance the biological control of herbivores by their natural enemies.     

Contrasting patterns of herbivore and predator pressure on invasive and native plants

Invasive non-native plant species often harbor fewer herbivorous insects than related native plant species. However, little is known about how herbivorous insects on non-native plants are exposed to carnivorous insects, and even less is known on plants that have recently expanded their ranges within continents due to climate warming. In this study we examine the herbivore load (herbivore biomass per plant biomass), predator load (predator biomass per plant biomass) and predator pressure (predator biomass per herbivore biomass) on an inter-continental non-native and an intra-continental range-expanding plant species and two congeneric native species. All four plant species co-occur in riparian habitat in north-western Europe. Insects were collected in early, mid and late summer from three populations of all four species. Before counting and weighing the insects were classified to trophic guild as carnivores (predators), herbivores, and transients. Herbivores were further subdivided into leaf-miners, sap-feeders, chewers and gallers. Total herbivore loads were smaller on inter-continental non-native and intra-continental range-expanding plants than on the congeneric natives. However, the differences depended on time within growing season, as well as on the feeding guild of the herbivore. Although the predator load on non-native plants was not larger than on natives, both non-native plant species had greater predator pressure on the herbivores than the natives. We conclude that both these non-native plant species have better bottom-up as well as top-down control of herbivores, but that effects depend on time within growing season and (for the herbivore load) on herbivore feeding guild. Therefore, when evaluating insects on non-native plants, variation within season and differences among feeding guilds need to be taken into account.     

Variation in plant quality and the population dynamics of herbivores: there is nothing average about aphids

In the attempt to use results from small-scale studies to make large-scale predictions, it is critical that we take into account the greater spatial heterogeneity encountered at larger spatial scales. An important component of this heterogeneity is variation in plant quality, which can have a profound influence on herbivore population dynamics. This influence is particularly relevant when we consider that the strength of density dependence can vary among host plants and that the strength of density dependence determines the difference between exponential and density- dependent growth. Here, we present some simple models and analyses designed to examine the impact of variable plant quality on the dynamics of insect herbivore populations, and specifically the consequences of variation in the strength of density dependence among host plants. We show that average values of herbivore population growth parameters, calculated from plants that vary in quality, do not predict overall population growth. Furthermore, we illustrate that the quality of a few individual plants within a larger plant population can dominate herbivore population growth. Our results demonstrate that ignoring spatial heterogeneity that exists in herbivore population growth on plants that differ in quality can lead to a misunderstanding of the mechanisms that underlie population dynamics.     

Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea)

Natural populations of wild cabbage (Brassica oleracea) show significant qualitative diversity in heritable aliphatic glucosinolates, a class of secondary metabolites involved in defence against herbivore attack. One candidate mechanism for the maintenance of this diversity is that differential responses among herbivore species result in a net fitness balance across plant chemotypes. Such top-down differential selection would be promoted by consistent responses of herbivores to glucosinolates, temporal variation in herbivore abundance, and fitness impacts of herbivore attack on plants varying in glucosinolate profile. A 1-year survey across 12 wild cabbage populations demonstrated differential responses of herbivores to glucosinolates. We extended this survey to investigate the temporal consistency of these responses, and the extent of variation in abundance of key herbivores. Within plant populations, the aphid Brevicoryne brassicae consistently preferred plants producing the glucosinolate progoitrin. Among populations, increasing frequencies of sinigrin production correlated positively with herbivory by whitefly Aleyrodes proletella and negatively with herbivory by snails. Two Pieris butterfly species showed no consistent response to glucosinolates among years. Rates of herbivory varied significantly among years within populations, but the frequency of herbivory at the population scale varied only for B. brassicae. B. brassicae emerges as a strong candidate herbivore to impose differential selection on glucosinolates, as it satisfies the key assumptions of consistent preferences and heterogeneity in abundance. We show that variation in plant secondary metabolites structures the local herbivore community and that, for some key species, this structuring is consistent over time. We discuss the implications of these patterns for the maintenance of diversity in plant defence chemistry.     

Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities

Natural plant populations often show substantial heritable variation in chemical structure of secondary metabolites. Despite a great deal of evidence from laboratory studies that these chemicals influence herbivore behaviour and life history, there exists little evidence for the structuring of natural herbivore communities according to plant chemical profiles. Brassica oleracea (Brassicaceae) produces aliphatic glucosinolates, which break down into toxins when leaf tissue is damaged. Structural diversity in these glucosinolates is heritable, and varies considerably at two ecological scales in the UK: both within and between populations. We surveyed herbivore attack on plants producing different glucosinolates, using 12 natural B. oleracea populations. In contrast to the results of previous studies in this system, which suffered low statistical power, we found significant differential responses of herbivore species to heritable glucosinolates, both within and between plant populations. We found significant correlations between herbivore infestation rates and the presence or absence of two heritable glucosinolates: sinigrin and progoitrin. There was variation between herbivore species in the direction of response, the ecological scale at which responses were identified, and the correlations for some herbivore species changed at different times of the year. We conclude that variation in plant secondary metabolites can structure the community of herbivores that attack them, and propose that herbivore-mediated differential selection deserves further investigation as a mechanism maintaining the observed diversity of glucosinolates in wild Brassica.     

Effects of nitrogen deposition on the interaction between an aphid and its host plant

Abstract 1. Anthropogenic increases in nitrogen deposition are impacting terrestrial ecosystems worldwide. While some of the direct ecosystem‐level effects of nitrogen deposition are understood, the effects of nitrogen deposition on plant–insect interactions and on herbivore population dynamics have received less attention. 2. Nitrogen deposition will potentially influence both plant resource availability and herbivore population growth. If increases in herbivore population growth outstrip increases in resource availability, then increases in the strength of density dependence expressed within the herbivore population would be predicted. Alternatively, if plant resources respond more vigorously to nitrogen deposition than do herbivore populations, a decline in the strength of density dependence would be expected. No change in the strength of density dependence acting upon the herbivore population would suggest equivalent responses by herbivores and plants. 3. A density manipulation experiment was performed to examine the effect of nitrogen deposition on the interaction between a host plant, Asclepias tuberosa, and its herbivore, Aphis nerii. Aphid maximum per capita growth rate (R_max), carrying capacity (K), and the strength of density dependence were measured under three nitrogen deposition treatments. The effect of nitrogen deposition on the relationship among these three measures of insect population dynamics was explored. 4. Simulated nitrogen deposition increased aphid per capita population growth, plant foliar nitrogen concentrations, and plant biomass. Nitrogen deposition caused R_max and K to increase proportionally, leading to no overall change in the strength of density dependence. In this system, potential changes in the negative feedback processes operating on herbivore populations following nitrogen deposition appear to be buffered by concomitant changes in resource availability.     

Consequences of constitutive and induced variation in plant nutritional quality for immune defence of a herbivore against parasitism

The mechanisms through which trophic interactions between species are indirectly mediated by distant members in a food web have received increasing attention in the field of ecology of multitrophic interactions. Scarcely studied aspects include the effects of varying plant chemistry on herbivore immune defences against parasitoids. We investigated the effects of constitutive and herbivore-induced variation in the nutritional quality of wild and cultivated populations of cabbage (Brassica oleracea) on the ability of small cabbage white Pieris rapae (Lepidoptera, Pieridae) larvae to encapsulate eggs of the parasitoid Cotesia glomerata (Hymenoptera, Braconidae). Average encapsulation rates in caterpillars parasitised as first instars were low and did not differ among plant populations, with caterpillar weight positively correlating with the rates of encapsulation. When caterpillars were parasitised as second instar larvae, encapsulation of eggs increased. Caterpillars were larger on the cultivated Brussels sprouts plants and exhibited higher levels of encapsulation compared with caterpillars on plants of either of the wild cabbage populations. Observed differences in encapsulation rates between plant populations could not be explained exclusively by differences in host growth on the different Brassica populations. Previous herbivore damage resulted in a reduction in the larval weight of subsequent herbivores with a concomitant reduction in encapsulation responses on both Brussels sprouts and wild cabbage plants. To our knowledge this is the first study demonstrating that constitutive and herbivore-induced changes in plant chemistry act in concert, affecting the immune response of herbivores to parasitism. We argue that plant-mediated immune responses of herbivores may be important in the evaluation of fitness costs and benefits of herbivore diet on the third trophic level.     

Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland

The density-dependent effect of induced plant resistance on herbivore populations depends on the relationship between the amount of herbivore damage and the level of induced resistance produced by the plant. This relationship should influence the interaction of induced resistance and herbivore population dynamics, and if the relationship varies among plant genotypes, it could be subject to natural selection by herbivores. In this study the relationship between percent leaf area damaged and level of induced resistance was characterized for four genotypes of soybeans grown in a greenhouse. Damage ranging from 8 to 92% of leaf area was imposed using Mexican bean beetle larvae, and induced resistance was measured by bioassay using Mexican bean beetle adults. The level of induced resistance was significantly affected by the amount of damage, and the level of induced resistance varied significantly among the four genotypes. There was also a marginally significant interaction of damage and plant genotype, suggesting that the form of density dependence varies among these four genotypes of soybeans. These results suggest that these genotypes of plants might affect herbivore populations differently. If this variation is heritable, the form of density-dependent effects of induced resistance has the potential to evolve in this system.     

Plant chemistry and local adaptation of a specialized folivore

Local adaptation is central for creating and maintaining spatial variation in plant-herbivore interactions. Short-lived insect herbivores feeding on long-lived plants are likely to adapt to their local host plants, because of their short generation time, poor dispersal, and geographically varying selection due to variation in plant defences. In a reciprocal feeding trial, we investigated the impact of geographic variation in plant secondary chemistry of a long-lived plant, Vincetoxicum hirundinaria, on among-population variation in local adaptation of a specialist leaf-feeding herbivore, Abrostola asclepiadis. The occurrence and degree of local adaptation varied among populations. This variation correlated with qualitative and quantitative differences in plant chemistry among the plant populations. These findings provide insights into the mechanisms driving variation in local adaptation in this specialized plant-herbivore interaction.     

Geographic and genetic variation in the leaf surface resin components of Mimulus aurantiacus from southern California

Nearly 30% of the dry weight of leaves of the chaparral subshrub Mimulus aurantiacus comprise leaf surface resins. This resin provides some defense against the insect herbivore, Euphydryas chalcedona and may also protect plants from desiccation and UV light injury. The resin is composed of several components and the different components may contribute differentially to the resin's multiple protective roles. The quantities of each of seven resin components from field-grown plants, from six southern California populations of M. aurantiacus spanning a range of water availability and differing in attack by E. chalcedona, and clones from these plants grown in a common garden, were determined. Two predictions were tested: (1) E. chalcedona will attack plant populations with relatively low quantities of total resins and/or concentrations of the ortho dihydroxy resins, and (2) plant populations in drier environments will produce resin that is relatively richer in the methoxylated components than plant populations in more mesic environments. Although resin composition differed genetically among plant populations, the pattern of variation was not as predicted. Insect attack was not associated with lower levels of ortho dihydroxy compounds, and populations with higher proportions of methoxylated flavonoids were not found in the drier sites. The pattern of genetic variation among populations in resin composition therefore was not explained by the differences in chemical structure that were predicted to influence the role of the components as herbivore protectants or antidesiccants.     

Climate-driven diversity dynamics in plants and plant-feeding insects

The origin of species-rich insect-plant food webs has traditionally been explained by diversifying antagonistic coevolution between plant defences and herbivore counter-defences. However, recent studies combining paleoclimatic reconstructions with time-calibrated phylogenies suggest that variation in global climate determines the distribution, abundance and diversity of plant clades and, hence, indirectly influences the balance between speciation and extinction in associated herbivore groups. Extant insect communities tend to be richest on common plant species that have many close relatives. This could be explained either by climate-driven diffuse cospeciation between plants and insects, or by elevated speciation and reduced extinction in herbivore lineages associated with expanding host taxa (resources). Progress in paleovegetation reconstructions in combination with the rapidly increasing availability of fossil-calibrated phylogenies provide means to discern between these alternative hypotheses. In particular, the 'Diffuse cospeciation' scenario predicts closely matching main diversification periods in plants and in the insects that feed upon them, while the 'Resource abundance-dependent diversification' hypothesis predicts that both positive and negative responses of insect diversity are lagged in relation to host-plant availability. The dramatic Cenozoic changes in global climate provide multiple possibilities for studying the mechanisms by which climatic shifts may drive diversity dynamics in plants and insect herbivores.     

Plant reproductive allocation predicts herbivore dynamics across spatial and temporal scales

Life-history theory suggests that iteroparous plants should be flexible in their allocation of resources toward growth and reproduction. Such plasticity could have consequences for herbivores that prefer or specialize on vegetative versus reproductive structures. To test this prediction, we studied the response of the cactus bug (Narnia pallidicornis) to meristem allocation by tree cholla cactus (Opuntia imbricata). We evaluated the explanatory power of demographic models that incorporated variation in cactus relative reproductive effort (RRE; the proportion of meristems allocated toward reproduction). Field data provided strong support for a single model that defined herbivore fecundity as a time-varying, increasing function of host RRE. High-RRE plants were predicted to support larger insect populations, and this effect was strongest late in the season. Independent field data provided strong support for these qualitative predictions and suggested that plant allocation effects extend across temporal and spatial scales. Specifically, late-season insect abundance was positively associated with interannual changes in cactus RRE over 3 years. Spatial variation in insect abundance was correlated with variation in RRE among five cactus populations across New Mexico. We conclude that plant allocation can be a critical component of resource quality for insect herbivores and, thus, an important mechanism underlying variation in herbivore abundance across time and space.     

Light environment and the impacts of foliage quality on herbivorous insect attack and bird predation

Theory predicts that variation in plant traits will modify both the direct interactions between plants and herbivores and the indirect impacts of predators of those herbivores. Light has strong effects on leaf quality, so the impacts of herbivores and predators may differ between plants grown in sun and shade. However, past experiments have often been unable to separate the effects of light environment on plant traits and herbivory from direct effects on herbivores and predators. We first manipulated light availability in an open habitat using a shade cloth pre-treatment to produce oak saplings with different leaf qualities. Leaves on plants exposed to high light were thicker and tougher and had lower nitrogen and water contents, and higher carbon and phenolic contents than leaves on plants under a shade cloth. Then, in the main experiment, we moved all plants to a common shade environment where bird predators were excluded in a factorial design. We measured insect herbivore abundance and leaf damage. Herbivores were significantly more abundant and caused greater leaf damage on sun trees, although these leaf characteristics are usually associated with low-quality food. Bird exclusion did not change herbivore abundance but did increase leaf damage. Contrary to our predictions, the effects of birds did not differ between trees grown in sun and shade conditions. Thus, differences in effects of predators on herbivores and plants between light habitats, when observed, might be due to variation in predator abundance and not bottom-up effects of host plant quality.