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.
Information of the patterns of genetic variation in plant resistance and tolerance against herbivores and genetic trade‐offs between these two defence strategies is central for our understanding of the evolution of plant defence. We found genetic variation in resistance to two specialist herbivores and in tolerance to artificial damage but not to a specialist leaf herbivore in a long‐lived perennial herb. Seedlings tended to have genetic variation in tolerance to artificial damage. Genetic variation in tolerance of adult plants to artificial damage was not consistent in time. Our results suggest that the level of genetic variation in tolerance and resistance depends on plant life‐history stage, type of damage and timing of estimating the tolerance relative to the occurrence of the damage, which might reflect the pattern of selection imposed by herbivory. Furthermore, we found no trade‐offs between resistance and tolerance, which suggests that the two defence strategies can evolve independently.
Summary1. Due to geographically variable species interactions, plants may become locally adapted to their sympatric herbivores and pollinators. However, adaptation to the abiotic environment may significantly affect plant interactions with herbivores and pollinators. Local adaptation to the abiotic environment may constrain local adaptation to herbivores and pollinators under contrasting selection pressures, resulting in trade-offs in local adaptation. 2. We studied local adaptation of a perennial herb, Vincetoxicum hirundinaria, in a reciprocal transplant experiment among four populations and measured plant fitness, pollination success and resistance to two specialist herbivores. We also estimated local adaptation of these two herbivores and generalist pollinators to their sympatric plant populations. Local adaptation was compared with within-population genetic variation, genetic and geographical divergence, and with divergence in terms of population size, environmental conditions and plant secondary chemistry. We further compared local adaptation to the environment, to local adaptation to herbivores and pollinators to detect possible trade-offs in local adaptation. 3. The existence and degree of local adaptation varied among the plant populations. Plants from two populations were locally adapted to their sympatric leaf herbivores and plants from two populations were locally adapted to their abiotic environment. Herbivores from one population were locally adapted to their sympatric plant population. Local adaptation of V. hirundinaria to the seed predator increased with increasing among-population divergence in precipitation and temperature. Local adaptation to the seed predator and the environment increased with increasing population genetic variation. Local adaptation of V. hirundinaria in fitness and in herbivore resistance also correlated positively, suggesting lack of trade-offs in local adaptation. 4. Synthesis. These results demonstrate that species interactions can lead to a mosaic of locally adapted plant, herbivore and pollinator populations. In addition to natural enemies, genetic variation, the abiotic environment and mutualistic interactions contribute to the evolution of local adaptation in long-lived plants. These results provide new insights into the patterns and causes of variation in local adaptation and are among the first to demonstrate that conflicting selection pressures within a population do not constrain local adaptation in multiple traits.
The global decline in pollinators has partly been blamed on pesticides, leading some to propose pesticide-free farming as an option to improve pollination. However, herbivores are likely to be more prevalent in pesticide-free environments, requiring knowledge of their effects on pollinators, and alternative crop protection strategies to mitigate any potential pollination reduction. Strawberry leaf beetles (SLB) Galerucella spp. are important strawberry pests in Northern Europe and Russia. Given that SLB attack both leaf and flower tissue, we hypothesized pollinators would discriminate against SLB-damaged strawberry plants (Fragaria vesca, cultivar ‘Rügen’), leading to lower pollination success and yield. In addition we screened the most common commercial cultivar ‘Rügen’ and wild Swedish F. vesca genotypes for SLB resistance to assess the potential for inverse breeding to restore high SLB resistance in cultivated strawberry. Behavioral observations in a controlled experiment revealed that the local pollinator fauna avoided strawberry flowers with SLB-damaged petals. Low pollination, in turn, resulted in smaller more deformed fruits. Furthermore, SLB-damaged flowers produced smaller fruits even when they were hand pollinated, showing herbivore damage also had direct effects on yield, independent of indirect effects on pollination. We found variable resistance in wild woodland strawberry to SLB and more resistant plant genotypes than the cultivar ‘Rügen’ were identified. Efficient integrated pest management strategies should be employed to mitigate both direct and indirect effects of herbivory for cultivated strawberry, including high intrinsic plant resistance.
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.
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.
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