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Volatile organic compounds (VOCs) in general and herbivory-induced plant volatiles (HIPVs) in particular are increasingly understood as major mediators of information transfer between plant tissues. Recent findings have moved the field of plant communication closer to a detailed understanding of how plants emit and perceive VOCs and seem to converge on a model that juxtaposes perception and emission mechanisms. These new mechanistic insights help to explain how plants can integrate different types of information and how environmental noise can affect the transmission of information. At the same time, ever-new functions of VOC-mediated plant-plant interactions are being revealed. Chemical information transfer between plants is now known to fundamentally affect plant organismal interactions and, additionally, population, community, and ecosystem dynamics. One of the most exciting new developments places plant-plant interactions along a behavioral continuum with an eavesdropping strategy at one end and mutually beneficial information-sharing among plants within a population at the other. Most importantly and based on recent findings as well as theoretical models, plant populations can be predicted to evolve different communication strategies depending on their interaction environment. We use recent studies from ecological model systems to illustrate this context dependency of plant communication. Moreover, we review recent key findings about the mechanisms and functions of HIPV-mediated information transfer and suggest conceptual links, such as to information theory and behavioral game theory, as valuable tools for a deeper understanding of how plant-plant communication affects ecological and evolutionary dynamics.

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Plants defend themselves from herbivory by either reducing damage (resistance) or minimizing its negative fitness effects with compensatory growth (tolerance). Herbivore pressure can fluctuate from year to year in an early secondary successional community, which can create temporal variation in selection for defence traits. We manipulated insect herbivory and successional age of the community as agents of natural selection in replicated common gardens with the perennial herb Solidago altissima. In these genotypic selection experiments, herbivory consistently selected for better defended plants in both successional communities. Herbivore suppression increased plant survival and the probability of flowering only in mid-succession. Despite these substantial differences in the effects of herbivory between early and mid-succession, the selection on defence traits did not change. Succession affected selection only on aboveground biomass, with positive selection in early but not mid-succession, suggesting an important role of competition in the selective environment. These results demonstrate that changes in the community that affect key life-history traits in an individual species can occur over very short timescales in a dynamic secondary successional environment. The resulting community context-driven variation in natural selection may be an important, yet overlooked, contributor to adaptive mosaics across populations.

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Vertically transmitted endophytic fungi can mitigate the negative effects of salinity encountered by their host grass and alter the competitive interactions between plant individuals. To experimentally study the interactive effects of the fungal endophyte Epichloë coenophiala on salt tolerance and intraspecific competition of its host plant, tall fescue Festuca arundinacea, we subjected 15 maternal lines of each Epichloë associated (E+) and Epichloë free (E-) tall fescue to salt treatment and competition in the greenhouse and common garden. Then, to explore variation in endophyte incidence in natural populations of tall fescue, we surveyed 23 natural populations occurring on or near the Baltic Sea coast in Aland islands in southwestern Finland for endophyte incidence, distance to shore, and competitive environment. Under salinity in the greenhouse, E- plants grew larger than E+ plants, but there was no size difference in the control treatment. E- plants grew taller and were more likely to flower than E+ plants when grown in benign conditions in the common garden but not with salinity or competition. The frequency of Epichloë incidence was high (90%) in natural populations, and it decreased towards the shore and risk of salt exposure. These results demonstrate a negative effect of Epichloë endophyte on the salt tolerance of its host. The high incidence of Epichloë in natural populations of tall fescue in the northern part of the species distribution range is likely due to factors other than salinity.

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Introduced species, which establish in novel environments, provide an opportunity to explore trait evolution and how it may contribute to the distribution and spread of species. Here, we explore trait changes of the perennial herb Lupinus polyphyllus based on 11 native populations in the western USA and 17 introduced populations in Finland. More specifically, we investigated whether introduced populations outperformed native populations in traits measured in situ (seed mass) and under common garden conditions during their first year (plant size, flowering probability, and number of flowering shoots). We also explored whether climate of origin (temperature) influenced plant traits and quantified the degree to which trait variability was explained collectively by country and temperature as compared to other population-level differences. Three out of four plant traits differed between the native and introduced populations; only seed mass was similar between countries, with most of its variation attributed to other sources of intraspecific variation not accounted for by country and temperature. Under common garden conditions, plants originating from introduced populations were larger than those originating from native populations. However, plants from the introduced range flowered less frequently and had fewer flowering shoots than their native-range counterparts. Temperature of a population's origin influenced plant size in the common garden, with plant size increasing with increasing mean annual temperature in both native and introduced populations. Our results of the first year reveal genetic basis for phenotypic differences in some fitness-related traits between the native and introduced populations of L. polyphyllus. However, not all of these trait differences necessarily contribute to the invasion success of the species and thus may not be adaptive, which raises a question how persistent the trait differences observed in the first year are later in individuals' life for perennial herbs.

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Plant volatile organic compounds (VOCs) are major vehicles of information transfer between organisms and mediate many ecological interactions [1-3]. Altering VOC emission in response to herbivore damage has been hypothesized to be adaptive, as it can deter subsequent herbivores [4], attract natural enemies of herbivores [5], or transmit information about attacks between distant parts of the same plant [6-9]. Neighboring plants may also respond to these VOC cues by priming their own defenses against oncoming herbivory, thereby reducing future damage [10-12]. However, under which conditions such information sharing provides fitness benefits to emitter plants, and, therefore, whether selection by herbivores affects the evolution of such VOC signaling, is still unclear [13]. Here, we test the predictions of two alternative hypotheses, the kin selection and mutual benefits hypotheses [14], to uncover the selective environment that may favor information sharing in plants. Measuring the response to natural selection in Solidago altissima, we found strong effects of herbivory on the way plants communicated with neighbors. Plants from populations that experienced selection by insect herbivory induced resistance in all neighboring conspecifics by airborne cues, whereas those from populations experiencing herbivore exclusion induced resistance only in neighbors of the same genotype. Furthermore, the information-sharing plants converged on a common, airborne VOC signal upon damage. We demonstrate that herbivory can drive the evolution of plant-plant communication via induction of airborne cues and suggest plants as a model system for understanding information sharing and communication among organisms in general.

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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.

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The quality and outcome of organismal interactions are not only a function of genotypic composition of the interacting species, but also the surrounding environment. Both the strength and direction of natural selection on interacting populations vary with the community context, which itself is changed by these interactions. Here, we test for the role of interacting evolutionary and ecological processes in plant-herbivore interactions during early community succession in the tall goldenrod, Solidago altissima. We use surveys in a large-scale field experiment with repeated plots representing 6 years of early oldfield succession and reciprocal transplant common garden experiments to test for the relative importance of rapid evolution (genetic) and environmental changes (soil quality) in affecting mean plant resistance and growth phenotypes during community succession. While plant growth varied strongly with soil quality over the first 5 years of agricultural abandonment, plant secondary metabolism, and herbivore resistance varied minimally with the soil environment. Instead, mean composition and abundance of plant secondary compound bouquets differed between S. altissima plants from populations collected in communities in the first ("early") and sixth ("intermediate") years of oldfield succession, which was reflected in the feeding preference of the specialist herbivore, Trirhabda virgata, for early succession lines. Moreover, this preference was most pronounced on poorer quality, early succession soils. Overall, our data demonstrate that plant quality varies for insect herbivores during the course of early succession and this change is a combination of altered genotypic composition of the population and phenotypic plasticity in different soil environments.

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Local adaptation of interacting species to one another indicates geographically variable reciprocal selection. This process of adaptation is central in the organization and maintenance of genetic variation across populations. Given that the strength of selection and responses to it often vary in time and space, the strength of local adaptation should in theory vary between generations and among populations. However, such spatiotemporal variation has rarely been explicitly demonstrated in nature and local adaptation is commonly considered to be relatively static. We report persistent local adaptation of the short-lived herbivore Abrostola asclepiadis to its long-lived host plant Vincetoxicum hirundinaria over three successive generations in two studied populations and considerable temporal variation in local adaptation in six populations supporting the geographic mosaic theory. The observed variation in local adaptation among populations was best explained by geographic distance and population isolation, suggesting that gene flow reduces local adaptation. Changes in herbivore population size did not conclusively explain temporal variation in local adaptation. Our results also imply that short-term studies are likely to capture only a part of the existing variation in local adaptation.

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Inbreeding can profoundly affect the interactions of plants with herbivores as well as with the natural enemies of the herbivores. We studied how plant inbreeding affects herbivore oviposition preference, and whether inbreeding of both plants and herbivores alters the probability of predation or parasitism of herbivore eggs. In a laboratory preference test with the specialist herbivore moth Abrostola asclepiadis and inbred and outbred Vincetoxicum hirundinaria plants, we discovered that herbivores preferred to oviposit on outbred plants. A field experiment with inbred and outbred plants that bore inbred or outbred herbivore eggs revealed that the eggs of the outbred herbivores were more likely to be lost by predation, parasitism or plant hypersensitive responses than inbred eggs. This difference did not lead to differences in the realized fecundity as the number of hatched larvae did not differ between inbred and outbred herbivores. Thus, the strength of inbreeding depression in herbivores decreases when their natural enemies are involved. Plant inbreeding did not alter the attraction of natural enemies of the eggs. We conclude that inbreeding can significantly alter the interactions of plants and herbivores at different life-history stages, and that some of these alterations are mediated by the natural enemies of the herbivores.

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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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