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.

The role of inbreeding and outbreeding in herbivore resistance and tolerance in Vincetoxicum hirundinaria.

BACKGROUND AND AIMS: Inbreeding via self-fertilization may have negative effects on plant fitness (i.e. inbreeding depression). Outbreeding, or cross-fertilization between genetically dissimilar parental plants, may also disrupt local adaptation or allelic co-adaptation in the offspring and again lead to reduced plant fitness (i.e. outbreeding depression). Inbreeding and outbreeding may also increase plant vulnerability to natural enemies by altering plant quality or defence. The effects of inbreeding and outbreeding on plant size and response to herbivory in the perennial herb, Vincetoxicum hirundinaria, were investigated. METHODS: Greenhouse experiments were conducted using inbred and outbred (within- and between-population) offspring of 20 maternal plants from four different populations, quantifying plant germination, size, resistance against the specialist folivore, Abrostola asclepiadis, and tolerance of simulated defoliation. KEY RESULTS: Selfed plants were smaller and more susceptible to damage by A. asclepiadis than outcrossed plants. However, herbivore biomass on selfed and outcrossed plants did not differ. The effects of inbreeding on plant performance and resistance did not differ among plant populations or families, and no inbreeding depression at all was found in tolerance of defoliation. Between-population outcrossing had no effect on plant performance or resistance against A. asclepiadis, indicating a lack of outbreeding depression. CONCLUSIONS: Since inbreeding depression negatively affects plant size and herbivore resistance, inbreeding may modify the evolution of the interaction between V. hirundinaria and its specialist folivore. The results further suggest that herbivory may contribute to the maintenance of a mixed mating system of the host plants by selecting for outcrossing and reduced susceptibility to herbivore attack, and thus add to the growing body of evidence on the effects of inbreeding on the mating system evolution of the host plants and the dynamics of plant-herbivore interactions.

Associations of plant fitness, leaf chemistry, and damage suggest selection mosaic in plant-herbivore interactions.

The geographic mosaic theory of coevolution states that variation in species interactions forms the raw material for coevolutionary processes, which take place over large geographic scales. One key assumption underlying the process of coevolution in plant-herbivore interactions is that herbivores exert selection on their host plants and that this selection varies among plant populations. We examined spatial variation in the existence and strength of phenotypic selection on host plant resistance exerted by specialist herbivores in 17 archipelago populations of the perennial herb Vincetoxicum hirundinaria (Asclepiadaceae). In these highly fragmented populations, V. hirundinaria is consumed by the larvae of two specialist herbivores: the folivorous moth Abrostola asclepiadis and the seed predator Euphranta connexa. Selection imposed on host plants by these herbivores was examined by analyzing the associations between levels of herbivory, plant fitness, and contents of a number of leaf chemicals reflecting plant resistance to and quality for the herbivores. We found extensive spatial variation in the levels of herbivory and in plant fitness. More importantly, the impact of both leaf herbivory and seed predation on plant fitness varied among plant populations, indicating spatial variation in phenotypic selection. In addition, leaf chemistry varied widely among plant populations, reflecting spatial variation in plant quality as food for the herbivores. However, leaf compounds influenced folivory similarly in all the studied plant populations, and interestingly, some of the compounds were associated with the intensity of seed predation. Finally, some of the leaf compounds were associated with plant fitness, and the strength and direction of these associations varied among plant populations. The observed spatial variation in the strength of the interactions between V. hirundinaria and its specialist herbivores suggests a geographic selection mosaic. Because the occurrence and strength of spatial variation varied between the two specialist herbivores, our results highlight the importance of considering multiple enemies when trying to understand evolution of interactions between plants and their herbivores.

Genetic drift precluded adaptation of an insect seed predator to a novel host plant in a long-term selection experiment.

Host specialization is considered a primary driver of the enormous diversity of herbivorous insects. Trade-offs in host use are hypothesized to promote this specialization, but they have mostly been studied in generalist herbivores. We conducted a multi-generation selection experiment to examine the adaptation of the specialist seed-feeding bug, Lygaeus equestris, to three novel host plants (Helianthus annuus, Verbascum thapsus and Centaurea phrygia) and to test whether trade-offs promote specialization. During the selection experiment, body size of L. equestris increased more on the novel host plant H. annuus compared to the primary host plant, Vincetoxicum hirundinaria, but this effect was not observed in other fitness related traits. In addition to selection, genetic drift caused variation among the experimental herbivore populations in their ability to exploit the host plants. Microsatellite data indicated that the level of within-population genetic variation decreased and population differentiation increased more in the selection line feeding on H. annuus compared to V. hirundinaria. We found a negative correlation between genetic differentiation and heterozygosity at the end of the experiment, suggesting that differentiation was significantly affected by genetic drift. We did not find fitness trade-offs between L. equestris feeding on the four hosts. Thus, trade-offs do not seem to promote specialization in L. equestris. Our results suggest that this insect herbivore is not likely to adapt to a novel host species in a time-scale of 20 generations despite sufficient genetic variation and that genetic drift disrupted the response to selection.

Higher predation risk for insect prey at low latitudes and elevations.

Biotic interactions underlie ecosystem structure and function, but predicting interaction outcomes is difficult. We tested the hypothesis that biotic interaction strength increases toward the equator, using a global experiment with model caterpillars to measure predation risk. Across an 11,660-kilometer latitudinal gradient spanning six continents, we found increasing predation toward the equator, with a parallel pattern of increasing predation toward lower elevations. Patterns across both latitude and elevation were driven by arthropod predators, with no systematic trend in attack rates by birds or mammals. These matching gradients at global and regional scales suggest consistent drivers of biotic interaction strength, a finding that needs to be integrated into general theories of herbivory, community organization, and life-history evolution.

Plant-species diversity correlates with genetic variation of an oligophagous seed predator.

Several characteristics of habitats of herbivores and their food-plant communities, such as plant-species composition and plant quality, influence population genetics of both herbivores and their host plants. We investigated how different ecological and geographic factors affect genetic variation in and differentiation of 23 populations of the oligophagous seed predator Lygaeus equestris (Heteroptera) in southwestern Finland and in eastern Sweden. We tested whether genetic differentiation of the L. equestris populations was related to the similarity of vegetation, and whether there was more within-population genetic variation in habitats with a high number of plant species or in those with a large population of the primary food plant, Vincetoxicum hirundinaria. We also tested whether genetic differentiation of the populations was related to the geographic distance, and whether location of the populations on islands or on mainland, island size, or population size affected within-population genetic variation. Pairwise FST ranged from 0 to 0.1 indicating low to moderate genetic differentiation of populations. Differentiation increased with geographic distance between the populations, but was not related to the similarity of vegetation between the habitats. Genetic variation within the L. equestris populations did not increase with the population size of the primary food plant. However, the more diverse the plant community the higher was the level of genetic variation within the L. equestris population. Furthermore, the level of genetic variation did not vary significantly between island and mainland populations. The effect of the population size on within-population genetic variation was related to island size. Usually small populations are susceptible to loss of genetic variation, but small L. equestris populations on large islands seemed to maintain a relatively high level of within-population genetic variation. Our findings suggest that, in addition to geographic and species-specific ecological factors, the plant community affects population genetic structure of oligophagous herbivores.

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.