Plant-Herbivore Interaction in a Fragmented Landscape: Local Adaptation and Inbreeding

Reciprocal selection between interacting species is a major driver of biodiversity at both the genetic and the species level. This reciprocal selection, or coevolution, has led to the diversification of two highly diverse and abundant groups of organisms, flowering plants and their insect herbivores. In heterogeneous environments, the outcome of coevolved species interactions is influenced by the surrounding community and/or the abiotic environment. The process of adaptation allows species to adapt to their local conditions and to local populations of interacting species. However, adaptation can be disrupted or slowed down by an absence of genetic variation or by increased inbreeding, together with the following inbreeding depression, both of which are common in small and isolated populations that occur in fragmented environments. I studied the interaction between a long-lived plant Vincetoxicum hirundinaria and its specialist herbivore Abrostola asclepiadis in the southwestern archipelago of Finland. I focused on mutual local adaptation of plants and herbivores, which is a demonstration of reciprocal selection between species, a prerequisite for coevolution. I then proceeded to investigate the processes that could potentially hamper local adaptation, or species interaction in general, when the population size is small. I did this by examining how inbreeding of both plants and herbivores affects traits that are important for interaction, as well as among-population variation in the effects of inbreeding. In addition to bi-parental inbreeding, in plants inbreeding can arise from self-fertilization which has important implications for mating system evolution. I found that local adaptation of the plant to its herbivores varied among populations. Local adaptation of the herbivore varied among populations and years, being weaker in populations that were most connected. Inbreeding caused inbreeding depression in both plants and herbivores. In some populations inbreeding depression in herbivore biomass was stronger in herbivores feeding on inbred plants than in those feeding on outbred ones. For plants it was the other way around: inbreeding depression in anti-herbivore resistance decreased when the herbivores were inbred. Underlying some of the among-population variation in the effects of inbreeding is variation in plant phenolic compounds. However, variation in the modification of phenolic compounds in the digestive tract of the herbivore did not explain the inbreeding depression in herbivore biomass. Finally, adult herbivores had a preference for outbred host plants for egg deposition, and herbivore inbreeding had a positive effect on egg survival when the eggs were exposed to predators and parasitoids. These results suggest that plants and herbivores indeed exert reciprocal selection, as demonstrated by the significant local adaptation of V. hirundinaria and A. asclepiadis to one another. The most significant cause of disruption of the local adaptation of herbivore populations was population connectivity, and thus probably gene flow. In plants local adaptation tended to increase with increasing genetic variation. Whether or not inbreeding depression occurred varied according to the life-history stage of the herbivore and/or the plant trait in question. In addition, the effects of inbreeding strongly depended on the population. Taken together, inbreeding modified plant-herbivore interactions at several different levels, and can thus affect the strength of reciprocal selection between species. Thus inbreeding has the potential to affect the outcome of coevolution.Siirretty Doriast

Soil microbiota explain differences in herbivore resistance between native and invasive populations of a perennial herb

1. Soil microbiota can either slow down or facilitate plant invasions through their effects on plant performance. Associations with soil microbiota can also modify other plant traits such as herbivore resistance, which can indirectly affect the outcome of plant introductions.2. We studied the effects of soil microbiota on the perennial herbaceous legume Lupinus polyphyllus that hosts nitrogen-fixing mutualistic bacteria. We compared the plant performance, herbivore resistance and volatile organic compounds (VOCs) of plants from native (North American) and invasive (Finnish) populations of the species that were inoculated with intact or autoclaved soil from an invasive population.3. We found that plants of both origins greatly benefited from the intact soil inoculum with respect to all performance measures considered, suggesting that beneficial nitrogen-fixing rhizobia in the soil play a major role in shaping plant phenotypes. For three traits, effects of the intact soil inoculum were stronger in plants of native origin than in plants of invasive origin (number of leaves, herbivore resistance and total biomass). With the intact soil inoculum, plants of invasive origin were more resistant to snails than plants of native origin. Strikingly, differences in resistance to snails between plants of different origins disappeared entirely when soil microbes were reduced. Soil inoculum treatment altered the composition of the leaf VOC bouquet similarly regardless of plant origin.4. Synthesis. These results demonstrate the ability of Lupinus polyphyllus to associate with and benefit from putatively novel soil microbiota including rhizobia, which has likely contributed to its invasion success. Furthermore, it appears that the invasive populations have adapted to be less reliant on their symbionts, which further facilitates species spread. To our knowledge, this is the first study to demonstrate that differences in herbivore resistance between native and invasive plant populations of the same species can depend entirely on soil microbiota.</p

Glyphosate residues in soil can modify plant resistance to herbivores through changes in leaf quality.

Glyphosate is the most widely used non-selective herbicide in the world. Glyphosate residues in soil can affect plant quality by modifying plant physiology, hormonal pathways and traits, with potential consequences for plants' interactions with herbivores. We explored these indirect effects in the context of plant-herbivore interactions in a perennial, nitrogen-fixing herb. We quantified leaf herbivory for glyphosate-exposed and control plants grown in phosphorus-fertilized and non-fertilized soils, and assessed the impacts of glyphosate treatment on traits related to plant resistance against herbivores (leaf trichome density, leaf mass per area) and performance (aboveground biomass, root:shoot ratio, nodule number, nodule activity). Moreover, we conducted a laboratory feeding experiment to compare the palatability of leaves from glyphosate-exposed and control plants to a generalist mollusc herbivore. Herbivore damage and intensity in situ increased during the growing season regardless of glyphosate or phosphorus treatment. Glyphosate treatment reduced leaf trichome density but had no effect on the other plant traits considered. Herbivore damage was negatively associated with leaf trichome density. The feeding experiment revealed no difference in the feeding probability of mollusc herbivores between glyphosate-exposed and control plants. However, there was an interaction between glyphosate treatment and initial leaf area for leaf consumption by herbivores: leaf consumption increased with increasing leaf area in both groups, but at a lower rate for glyphosate-exposed plants than for control plants. Our results show that glyphosate residues in soil have the potential to indirectly affect aboveground herbivores through changes in leaf quality, which may have mixed consequences for folivore damage.</p

Introduced populations of the garden lupine are adapted to local generalist snails but have lost alkaloid diversity

Intraspecific variation in growth and defence among plant populations can be driven by differences in (a)biotic conditions, such as herbivory and resources. Introduction of species to novel environments affects simultaneously herbivory encountered by a plant and resource availability both directly and via altered competitive environment. Here, we address the question of how growth (leaf mass per area (LMA), plant size) and resistance traits (leaf alkaloids, leaf trichomes, resistance to a generalist snail) vary and covary between native and introduced populations of the garden lupine, Lupinus polyphyllus. We focused specifically on evolved differences among populations by measuring traits from plants grown from seed in a common environment. Plants from the introduced populations were more resistant against the generalist snail, Arianta arbustorum, and they had more leaf trichomes and higher LMA than plants from the native populations. The composition of alkaloids differed between native and introduced populations, with the native populations having more diversity in alkaloids among them. Resistance was positively associated with plant size and LMA across all populations. Other trait associations differed between native and introduced areas, implying that certain trade-offs may be fundamentally different between native and introduced populations. Our results suggest that, for the introduced populations, the loss of native herbivores and the alterations in resource availability have led to a lower diversity in leaf alkaloids among populations and may facilitate the evolution of novel trait optima without compensatory trade-offs. Such phytochemical similarity among introduced populations provides novel insights into mechanisms promoting successful plant invasions

Strong gene flow explains lack of mating system variation in the perennial herb, Vincetoxicum hirundinaria, in a fragmented landscape

Fragmented landscapes may have implications for the genetic structure of populations and for the microevolution of plant species. In particular, landscape fragmentation and/or population isolation might affect the evolution of plant mating systems. Here, we study the consequences of landscape fragmentation on the genetic structure of populations of a perennial herb, Vincetoxicum hirundinaria with a mixed mating system. Our study area, the south-western Finnish archipelago, was formed after the glacial ice sheet started to retreat 12 000 years ago. Due to the isostatic land uplift following the glacial retreat, suitable habitats have been formed gradually, and as a consequence, populations of V. hirundinaria differ in age, size and their degree of isolation in the area. We hypothesized that a mixed-mating system has been selected for in these populations due to the advantage of self-fertilization in newly colonized areas and the advantage of outcrossing in adaptation to heterogeneous environments. To test this hypothesis, we collected seeds of open-pollinated flowers from 13 V. hirundinaria populations differing in size, age and isolation, and used 15 microsatellite markers to perform progeny-array analysis to estimate population-level outcrossing rates, population genetic indices and population structure. We found that V. hirundinaria is almost completely outcrossing in the study area with no signs of past self-fertilization and/or mating among relatives. The overall low inbreeding coefficients indicate that even in small populations mating among relatives is rare. High allelic richness of both maternal and offspring genotypes as well as limited genetic differentiation among the studied populations indicate strong gene flow among them. Our findings suggest that V. hirundinaria has successful seed and pollen dispersal among populations that has allowed colonization of new habitats in this fragmented landscape and led to a genetically well-mixed group of populations at the scale of the study

Glyphosate residues alter the microbiota of a perennial weed with a minimal indirect impact on plant performance

Purpose In cold climates, glyphosate residues may linger in soils, with effects on plant-microbe interactions and, consequently, plant performance. Here, we explore the influence of glyphosate residues on the endophytic microbiota (bacteria and fungi) and performance of the perennial nitrogen-fixing weed Lupinus polyphyllus. Methods In a common garden, we grew plants from six populations of L. polyphyllus in glyphosate-treated or untreated control soils, with or without additional phosphorus. We sampled plant microbiota (leaves, roots, nodules) and assessed plant performance based on six traits: height, retrogression probability (i.e. shrinkage), biomass, root:shoot ratio, nodule number, and nodule viability. Results The richness of plant endophytic microbial communities was determined by soil phosphorus level rather than by glyphosate treatment. However, for bacteria, the composition of these communities differed between glyphosate-treated and control soils across plant tissue types; no difference was observed for fungi. The plant bacterial communities in both soil types were dominated by potential nitrogen-fixing bacteria belonging to family Bradyrhizobiaceae, and particularly so in glyphosate-treated soils. Overall, though, these changes in plant bacterial communities had a minor effect on plant performance: the only difference we detected was that the probability of retrogression was occasionally higher in glyphosate-treated soils than in control soils. Conclusion Our findings indicate that glyphosate-based herbicides, when applied at the recommended frequency and concentration, may not have critical effects on the growth of short-lived weeds after the safety period has passed; however, the endophytic microbiota of such weeds may experience longer-lasting shifts in community structure.</p

Supplementary material from Herbivory selects for tolerance and constitutive defense across stages of community succession

Supplementary methods for specialized metabolites analysis, figure of the arrangement of the study plots, supplementary results tables (effect of treatments, genetic correlations, heritabilities)

Endophytic Fungus Negatively Affects Salt Tolerance of Tall Fescue

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

Strong gene flow explains lack of mating system variation in the perennial herb, Vincetoxicum hirundinaria, in a fragmented landscape

Fragmented landscapes may have implications for the genetic structure of populations and for the microevolution of plant species. In particular, landscape fragmentation and/or population isolation might affect the evolution of plant mating systems. Here, we study the consequences of landscape fragmentation on the genetic structure of populations of a perennial herb, Vincetoxicum hirundinaria with a mixed mating system. Our study area, the south-western Finnish archipelago, was formed after the glacial ice sheet started to retreat 12 000 years ago. Due to the isostatic land uplift following the glacial retreat, suitable habitats have been formed gradually, and as a consequence, populations of V. hirundinaria differ in age, size and their degree of isolation in the area. We hypothesized that a mixed-mating system has been selected for in these populations due to the advantage of self-fertilization in newly colonized areas and the advantage of outcrossing in adaptation to heterogeneous environments. To test this hypothesis, we collected seeds of open-pollinated flowers from 13 V. hirundinaria populations differing in size, age and isolation, and used 15 microsatellite markers to perform progeny-array analysis to estimate population-level outcrossing rates, population genetic indices and population structure. We found that V. hirundinaria is almost completely outcrossing in the study area with no signs of past self-fertilization and/or mating among relatives. The overall low inbreeding coefficients indicate that even in small populations mating among relatives is rare. High allelic richness of both maternal and offspring genotypes as well as limited genetic differentiation among the studied populations indicate strong gene flow among them. Our findings suggest that V. hirundinaria has successful seed and pollen dispersal among populations that has allowed colonization of new habitats in this fragmented landscape and led to a genetically well-mixed group of populations at the scale of the study