Gene flow from foreign provenances into local plant populations: Fitness consequences and implications for biodiversity restoration

Long-distance transplantation of seed material as done in restoration programs has raised concerns about the risks associated with the introduction of maladapted genotypes that may hybridize with neighboring native conspecifics and decrease local population fitness (outbreeding depression). We studied the consequences of gene flow from foreign provenances into local populations in the common grassland species Plantago lanceolata (Plantaginaceae). Three generations of intraspecific hybrids (F(1), F(2), and backcross to the local plants) were produced by controlled crossings between local plants and plants from geographically or environmentally distant populations. Their performance was compared to that of within-population crosses in a field experiment. Early growth in some interpopulation hybrids was significantly reduced, and this decrease in performance was higher in progeny of crosses with the local population from a different habitat than with geographically distant populations. At the end of the growing season, most fitness-related traits of the interpopulation hybrids were close to the average of their parents. Crosses with low-performing foreign parents therefore resulted in reduced fitness of the hybrids compared to the local plants and dilution of local adaptation. We conclude that the introduction of maladapted populations from distant or ecologically distinct environments might, at least temporarily, decrease the fitness of neighboring local plants.     

Differentiation and adaptation in <Emphasis Type="Italic">Brassica nigra</Emphasis> populations: interactions with related herbivores

Local adaptation and population differentiation of plants are well documented, but studies on interactions with natural enemies are rare. In particular, evidence for plant adaptation to the local biotic environment, such as herbivores remains poor. We used the black mustard Brassica nigra, an annual species of river valley and coastal habitats to (1) analyse population differentiation in plant traits and herbivory in a common garden experiment, (2) examine home versus away differences in a reciprocal transplant experiment and (3) test whether plants are adapted to local herbivores or vice versa under standard greenhouse conditions. In the common garden experiment, we found significant differentiation in plant traits, leaf damage and herbivore number among seven populations of B. nigra from France and Germany (distance 15–1,000 km). Differences were particularly strong among coastal and river valley populations and did not necessarily increase with geographical distance. A herbivore removal treatment did not change population differentiation when compared with the control allowing natural colonisation. The reciprocal transplant experiment at a scale of 15–30 km did not reveal local plant adaptation, whilst one dominant herbivore species (Meligethes aeneus) occurred in significantly higher numbers on local plants. A greenhouse experiment combining three aphid (Brevicoryne brassicae) and plant populations of the same provenance indicated herbivore adaptation to their local plants rather than plant adaptation, but overall contrasts between local and non-local combinations were not significant. The results suggest that herbivores may counteract local plant adaptation to other environmental factors. Our study has important implications for plant translocations in ecological restoration projects.     

Local biotic adaptation of trees and shrubs to plant neighbors

Natural selection as a result of plant–plant interactions can lead to local biotic adaptation. This may occur where species frequently interact and compete intensely for resources limiting growth, survival, and reproduction. Selection is demonstrated by comparing a genotype interacting with con‐ or hetero‐specific sympatric neighbor genotypes with a shared site‐level history (derived from the same source location), to the same genotype interacting with foreign neighbor genotypes (from different sources). Better genotype performance in sympatric than allopatric neighborhoods provides evidence of local biotic adaptation. This pattern might be explained by selection to avoid competition by shifting resource niches (differentiation) or by interactions benefitting one or more members (facilitation). We tested for local biotic adaptation among two riparian trees, Populus fremontii and Salix gooddingii, and the shrub Salix exigua by transplanting replicated genotypes from multiple source locations to a 17 000 tree common garden with sympatric and allopatric treatments along the Colorado River in California. Three major patterns were observed: 1) across species, 62 of 88 genotypes grew faster with sympatric neighbors than allopatric neighbors; 2) these growth rates, on an individual tree basis, were 44, 15 and 33% higher in sympatric than allopatric treatments for P. fremontii, S. exigua and S. gooddingii, respectively, and; 3) survivorship was higher in sympatric treatments for P. fremontii and S. exigua. These results support the view that fitness of foundation species supporting diverse communities and dominating ecosystem processes is determined by adaptive interactions among multiple plant species with the outcome that performance depends on the genetic identity of plant neighbors. The occurrence of evolution in a plant‐community context for trees and shrubs builds on ecological evolutionary research that has demonstrated co‐evolution among herbaceous taxa, and evolution of native species during exotic plants invasion, and taken together, refutes the concept that plant communities are always random associations.     

Palatability of weeds from different European origins to the slugs Deroceras reticulatum Müller and Arion lusitanicus Mabille

As part of a study on the significance of seed provenances in schemes to enhance biodiversity in agricultural habitats, juvenile plants of Cichorium intybus, Daucus carota, Leucanthemum vulgare and Silene alba of different European origins were exposed to grazing by two slug species, Deroceras reticulatum and Arion lusitanicus. Living plants were offered in trays, either in a glasshouse (Deroceras) or outdoors (Arion). The amount of herbivory was origin-dependent, with higher losses for all four species from German and Hungarian provenances compared with English and Swiss plants. The main trend was similar for both slug species except in the case of Daucus, and there was a significant ‘origin × plant species’ interaction. We found strong correlations between provenance-specific herbivory and certain climatic characteristics of the corresponding regions, i.e. winter minimum temperatures, and dryness in spring and late summer, which are crucial for the development of slugs. The results can be interpreted in terms of a SW-NE European climatic gradient and may be a consequence of differences in the need for plant defences against herbivory by slugs. Additionally, the data on palatability were compared with susceptibility towards two parasites which occurred in a field experiment, a leaf miner on Leucanthemum vulgare and a rust fungus on Silene alba. While specific leaf mining frequencies on Leucanthemum contrasted with the palatability of the different provenances to slugs, the rust infection on Silene was low on local and German plants, and higher on the more distant provenances from England and Hungary.     

Do Induced Responses Mediate the Ecological Interactions Between the Specialist Herbivores and Phytopathogens of an Alpine Plant?

Plants are not passive victims of the myriad attackers that rely on them for nutrition. They have a suite of physical and chemical defences, and are even able to take advantage of the enemies of their enemies. These strategies are often only deployed upon attack, so may lead to indirect interactions between herbivores and phytopathogens. In this study we test for induced responses in wild populations of an alpine plant (Adenostyles alliariae) that possesses constitutive chemical defence (pyrrolizidine alkaloids) and specialist natural enemies (two species of leaf beetle, Oreina elongata and Oreina cacaliae, and the phytopathogenic rust Uromyces cacaliae). Plants were induced in the field using chemical elicitors of the jasmonic acid (JA) and salicylic acid (SA) pathways and monitored for one month under natural conditions. There was evidence for induced resistance, with lower probability and later incidence of attack by beetles in JA-induced plants and of rust infection in SA-induced plants. We also demonstrate ecological cross-effects, with reduced fungal attack following JA-induction, and a cost of SA-induction arising from increased beetle attack. As a result, there is the potential for negative indirect effects of the beetles on the rust, while in the field the positive indirect effect of the rust on the beetles appears to be over-ridden by direct effects on plant nutritional quality. Such interactions resulting from induced susceptibility and resistance must be considered if we are to exploit plant defences for crop protection using hormone elicitors or constitutive expression. More generally, the fact that induced defences are even found in species that possess constitutively-expressed chemical defence suggests that they may be ubiquitous in higher plants.     

Coping with an antagonist: the impact of a phytopathogenic fungus on the development and behaviour of two species of alpine leaf beetle

Herbivorous insects and phytopathogenic fungi often share their host plants. This creates a network of direct and indirect interactions, with far‐reaching consequences for the ecology and evolution of all three parties. In the Alps, the leaf beetles Oreina elongata and Oreina cacaliae (Coleoptera: Chrysomelidae), and the rust fungus Uromyces cacaliae (Uredinales: Pucciniaceae) are found on the same host plant, Adenostyles alliariae (Asterales: Asteraceae). We compare the impact of rust infection on these two closely‐related beetle species, one of which, O. cacaliae, is a specialist on A. alliariae, while the other, O. elongata, moves repeatedly between Adenostyles and an alternative host, Cirsium spinosissimum. Larval performance, feeding preference, oviposition choice and dispersal behaviour were studied in field and laboratory experiments. When reared on rust‐infected leaves, larvae of both beetle species had lower growth rates, lower maximum weights and longer development times. Larvae and adults discriminated among diets in feeding trials, showing a preference for discs cut from healthy leaves over those bearing a patch of sporulating rust, those from elsewhere on an infected leaf, and those from an upper leaf on an infected plant. Females of the two species differed in behaviour: in O. cacaliae they favoured healthy leaves for larviposition, while in O. elongata they showed no significant preference during oviposition. In the field, larvae and adults of both species dispersed more rapidly when placed on infected host plants. The results demonstrate that rust infection reduces the quality of the plant as a host for both Oreina species, and they combine the ability to detect systemic infection with the evolution of evasive behaviours. For these beetles, competition with a rust clearly increases the difficulty of survival in the harsh conditions of alpine environments, and may have a profound impact on the evolution of their life history traits and host plant use.     

Spatial scale of local adaptation in a plant-pathogen metapopulation

The rate and scale of gene flow can strongly affect patterns of local adaptation in host-parasite interactions. I used data on regional pathogen occurrence to infer the scale of pathogen dispersal and to identify pathogen metapopulations in the interaction between Plantago lanceolata and its specialist phytopathogen, Podosphaera plantaginis. Frequent extinctions and colonizations were recorded in the metapopulations, suggesting substantial gene flow at this spatial scale. The level of pathogen local adaptation was assessed in a laboratory inoculation experiment at three different scales: in sympatric host populations, in sympatric host metapopulations and in allopatric host metapopulations. I found evidence for adaptation to sympatric host populations, as well as evidence indicating that local adaptation may extend to the scale of the sympatric host metapopulation. There was also variation among the metapopulations in the degree of pathogen local adaptation. This may be explained by regional differences in the rate of migration.     

Habitat selection and grouping of beetles (Coleoptera)

Beetles were collected by pitfall trapping for a two-year period in seven adjacent habitats in an upland site in North Wales. Positive correlations were demonstrated between number of beetle species and number and diversity of plant species. Similar correlations were shown between beetle numbers and plant species. However, only 15% of the beetle species were herbivores requiring host plants. The degree of habitat selection by individual beetle species was demonstrated, ranging from habitat specialist, being found in one habitat, lo habitat generalist, being found in most habitats. Herbivores were significantly more habitat specialist than predators or scavengers. The grouping of beetles, demonstrated by ordination analysis, was similar to, but less precise than, the grouping of plant species. The beetle groups reflect habitat selection preferences by individual species rather than a functional relationship between beetle species. They provide an example of the centrifugal structure of habitat selection theory.     

Prevailing negative soil biota effect and no evidence for local adaptation in a widespread Eurasian grass

Background

Soil biota effects are increasingly accepted as an important driver of the abundance and distribution of plants. While biogeographical studies on alien invasive plant species have indicated coevolution with soil biota in their native distribution range, it is unknown whether adaptation to soil biota varies among populations within the native distribution range. The question of local adaptation between plants and their soil biota has important implications for conservation of biodiversity and may justify the use of seed material from local provenances in restoration campaigns.

Methodology/Principal Findings

We studied soil biota effects in ten populations of the steppe grass Stipa capillata from two distinct regions, Europe and Asia. We tested for local adaptation at two different scales, both within (ca. 10–80 km) and between (ca. 3300 km) regions, using a reciprocal inoculation experiment in the greenhouse for nine months. Generally, negative soil biota effects were consistent. However, we did not find evidence for local adaptation: both within and between regions, growth of plants in their ‘home soil’ was not significantly larger relative to that in soil from other, more distant, populations.

Conclusions/Significance

Our study suggests that negative soil biota effects can prevail in different parts of a plant species'' range. Absence of local adaptation points to the possibility of similar rhizosphere biota composition across populations and regions, sufficient gene flow to prevent coevolution, selection in favor of plasticity, or functional redundancy among different soil biota. From the point of view of plant - soil biota interactions, our findings indicate that the current practice of using seeds exclusively from local provenances in ecosystem restoration campaigns may not be justified.     

The Importance of Plant Provenance and Genotypic Diversity of Seed Material Used for Ecological Restoration

The increased translocation of plant species for biodiversity restoration and habitat creation has provoked a debate on provenance and genotypic diversity of the used plant material. Nonlocal provenances are often not adapted to the local environmental conditions, and low population genotypic diversity may result in genetic bottlenecks hampering successful establishment. We tested provenance differentiation of four plant species used in agri‐environment schemes to increase biodiversity of agricultural landscapes (wildflower strips). Provenances were collected close to the experimental field and at four further sites of different distances ranging from 120 to 900 km. In two of these provenances, different levels of genotypic diversity were simulated by sowing seed from a high and low number of mother plants. We found a large provenance differentiation in fitness‐related traits, particularly in seedling emergence. There was no evidence for a general superiority of the local population. The productivity was greater in populations of high genotypic diversity than in those of low diversity, but the effect was only significant in one species. Productivity was also more constant among populations of high diversity, reducing the risk of establishment failure. Our results indicate that the choice of an appropriate provenance and a sufficient genotypic diversity are important issues in ecological restoration. The use of local provenances does not always guarantee the best performance, but a spread of superior alien genotypes can be avoided. A sufficient genotypic diversity of the sown plants might be a biological insurance against fluctuations in ecosystem processes increasing the reliability of restoration measures.     

Restoration of species‐rich grasslands by transfer of local plant material and its impact on species diversity and genetic variation—Findings of a practical restoration project in southeastern Germany

Restoration of species‐rich grasslands is a key issue of conservation. The transfer of seed‐containing local plant material is a proven technique to restore species‐rich grassland, since it potentially allows to establish genetically variable and locally adapted populations. In our study, we tested how the transfer of local plant material affected the species diversity and composition of restored grasslands and the genetic variation of the typical grassland plant species Knautia arvensis and Plantago lanceolata.For our study, we selected fifteen study sites in southeastern Germany. We analyzed species diversity and composition and used molecular markers to investigate genetic variation within and among populations of the study species from grasslands that served as source sites for restoration and grasslands, which were restored by transfer of green hay and threshed local plant material.The results revealed no significant differences in species diversity and composition between grasslands at source and restoration sites. Levels of genetic variation within populations of the study species Knautia arvensis and Plantago lanceolata were comparable at source and restoration sites and genetic variation among populations at source and their corresponding restoration sites were only marginal different.Our study suggests that the transfer of local plant material is a restoration approach highly suited to preserve the composition of species‐rich grasslands and the natural genetic pattern of typical grassland plant species.     

Genetic differentiation of three endangered wild roses in northeastern Germany: Rosa inodora Fries, Rosa sherardii Davies and Rosa subcollina (H. Christ) Keller

Because of increased interest in the use of local provenances for restoration or landscaping projects, information about the genetic differentiation of plant species is required to delineate provenances for seed collection. To obtain information about population distinctiveness of endangered Rosa species occurring in Brandenburg (northeast Germany), we investigated the genetic differentiation of Rosa inodora, R. sherardii and R. subcollina using RAPD markers. All three species were uncommon in our study region. Φ-statistics, estimated by amova, revealed a low interpopulation differentiation for R. inodora (Φ(PT) = 0.19, P < 0.0001) and higher values for R. sherardii and R. subcollina (Φ(PT) = 0.29 and 0.30, P < 0.0001). UPGMA dendrograms and NMDS showed clear spatial differentiation for all species and a correlation between geographic and genetic distances. Due to predominantly high values of genetic differentiation and spatial patterns of ordination, we suggest small provenance regions for endangered Rosa species for seed collection.     

Native range variation in Capsella bursa-pastoris (Brassicaceae) along a 2500 km latitudinal transect

Capsella bursa-pastoris (L.) Medik. is a self compatible tetraploid annual species which has successfully spread to most continents and is mostly confined to man-made habitats. The colonising success may be associated with fine-scaled ecotypic differentiation, and regional adaptation. Seeds of 377 individuals from 40 provenances were collected over a distance of more than 2500 km from the Kola Peninsula in the north to the Caspian Sea in the south in Russia and from northern to southern Scandinavia. 3558 progenies were investigated in common garden field experiments in order to distinguish between phenotypic variability and genetic variation of quantitative life-history traits (onset of flowering, rosette diameter, leaf type, plant height, and branching and fruit characters). Genetic diversity and population structure was examined with isozyme analysis. Along both transects, Capsella showed clinal differentiation in phenotypic traits: e.g., the most northern and most southern provenances flowered earlier than the provenances from in between. A highly significant quadratic correlation exists between morphological traits and the degree of latitude. Distribution of leaf types showed no geographical pattern, unlike that observed for other regions. Allozyme variation follows a pattern of isolation by distance.     

Species specific responses of common grassland plants to a generalist root herbivore (Agriotes spp. larvae)

Insect root herbivores can alter plant community structure by affecting the competitive ability of single plants. Our study aims at increasing knowledge on the impact of click beetle larvae (Elateridae, genus Agriotes) on grassland plant communities, by determining biomass responses as well as responses of the arbuscular mycorrhizal fungi (AMF) symbiosis to this widespread generalist root herbivore for eight common grassland plant species (Festuca rubra, Holcus lanatus, Poa pratensis, Achillea millefolium, Plantago lanceolata, Veronica arvensis, Medicago lupulina, Trifolium repens), belonging to three functional groups (grasses, herbs, legumes).The presence of larvae in the rhizosphere of individual plants had an overall negative effect on root biomass, which varied in degree between plant species, with more root biomass being removed from larger root systems. The effect of larvae on shoot biomass, total plant biomass and shoot/root ratio also differed in strength between plant species. Relative changes in root and total plant biomass ranged from a 71% and 55% loss, respectively, in V. arvensis to an 11% and 1% increase in T. repens, but were not related to root- or plant size. Root colonization by AMF and the length of extraradical AMF hyphae were not affected by larvae. The plant's functional group did not determine the response of the plant to feeding by larvae. Growth of larvae was positively correlated with root biomass, but did not depend on plant species or group identity.The results confirm the generalist nature of Agriotes spp. larvae, which depend on sufficient root quantity and are likely to feed most on those plant species whose roots are most abundant in their habitat. Their effect on the plant community may be generated through the ability of the respective plant species to cope with the herbivore damage, with tolerances being plant species rather than plant group specific.     

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.     

Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa

Widespread species often occur across a range of climatic conditions, through a combination of local genetic adaptations and phenotypic plasticity. Species with greater phenotypic plasticity are likely to be better positioned to cope with rapid anthropogenic climate changes, while those displaying strong local adaptations might benefit from translocations to assist the movement of adaptive genes as the climate changes. Eucalyptus tricarpa occurs across a climatic gradient in south‐eastern Australia, a region of increasing aridity, and we hypothesized that this species would display local adaptation to climate. We measured morphological and physiological traits reflecting climate responses in nine provenances from sites of 460 to 1040 mm annual rainfall, in their natural habitat and in common gardens near each end of the gradient. Local adaptation was evident in functional traits and differential growth rates in the common gardens. Some traits displayed complex combinations of plasticity and genetic divergence among provenances, including clinal variation in plasticity itself. Provenances from drier locations were more plastic in leaf thickness, whereas leaf size was more plastic in provenances from higher rainfall locations. Leaf density and stomatal physiology (as indicated by δ¹³C and δ¹⁸O) were highly and uniformly plastic. In addition to variation in mean trait values, genetic variation in trait plasticity may play a role in climate adaptation.     

Species-specific effects of live roots and shoot litter on soil decomposer abundances do not forecast plant litter-nitrogen uptake

Plant species produce litter of varying quality and differ in the quality and quantity of compounds they release from live roots, which both can induce different decomposer growth in the soil. To test whether differences in decomposer growth can forecast the amount of N species acquire from plant litter, as suggested by theory, we grew individuals of three grassland plants—Holcus lanatus, Plantago lanceolata and Lotus corniculatus—in soils into which ¹⁵N-labelled litter of either Holcus, Plantago or Lotus was added. We measured the effects of live roots and litter of each species on soil microbes and their protozoan and nematode feeders, and to link decomposer growth and plant nutrient uptake, we measured the amount of N taken up by plants from the added litter. We hypothesised that those species that induce the highest growth of microbes, and especially that of microbial feeders, will also take up the highest amount of N from the litter. We found, however, that although numbers of bacterial-feeding Protozoa and nematodes were on average lower after addition of Holcus than Plantago or Lotus litter, N uptake was higher from Holcus litter. Further, although the effects on Protozoa and bacterial- and fungal-feeding nematodes did not differ between the live plants, litter-N uptake differed, with Holcus being the most efficient compared to Plantago and Lotus. Hence, although microbes and their feeders unquestionably control N mineralization in the soil, and their growth differs among plant species, these differences cannot predict differences in litter-N uptake among plant species. A likely reason is that for nutrient uptake, other species-specific plant traits, such as litter chemistry, root proliferation ability and competitiveness for soil N, override in significance the species-specific ability of plants to induce decomposer growth.     

Evidence for genetic differentiation and divergent selection in an autotetraploid forage grass (Arrhenatherum elatius)

The use of local provenances in restoration, agriculture and forestry has been identified as measure to sustain biological diversity and to improve local productivity. However, the delineation of regional provenances is challenging because it requires the identification of well-defined groups based on spatiogenetic differentiation and/or the evidence of local adaptation. In this study, we investigate genetic variation at 186 AFLP loci in 46 European accessions of the important grassland species Arrhenatherum elatius and ask (1) whether genetic variation within accessions differs between European geographical regions; (2) at which spatial scale populations are structured across Europe and (3) whether putatively adaptive markers contribute to this pattern and whether these markers can be related to climatic site conditions. Basic expectations of population genetics are likely to be altered in autotetraploid species, thus, we adopted a band-based approach to estimate genetic diversity and structuring. Compared to other grasses A. elatius showed high genetic diversity and considerable differentiation among accessions (Φ_ST = 0.24). Accessions separated in a Western European and a Central/Eastern European group, without further structure within groups. A genome scan approach identified four potentially adaptive loci, whose band frequencies correlated significantly with climatic parameters, suggesting that genetic differentiation in A. elatius is also the result of adaptive processes. Knowledge on adaptive loci might in the long run also help to adapt ecosystems to adverse climate change effects through assisted migration of ecotypes rather than introduction of new species.     

Seed provenance matters — Effects on germination of four plant species used for ecological restoration

The use of local seed provenances is often recommended in restoration and habitat creation because they are thought to be better adapted to local habitat conditions. However, spatial scales and the degree of population differentiation are not well known and germination is often not included in comparisons between provenances. We analysed germination as a key trait of plant development in five provenances of four species used for ecological restoration on arable land (wildflower strips). Germination was tested under different conditions in growth chambers (early vs. late spring) and in the field (non-competition vs. competition). We also examined the contribution of non-genetic (maternal) effects to population differentiation.Large differences in germination traits were found between the provenances in growth chambers and in the field. The ranking was species-specific, but largely consistent across all tested environments. Local provenances did not generally exhibit higher germination percentages in the field relative to non-local provenances. Due to the high stability of germination traits across various environments, growth chamber tests provided a reliable prediction for provenance differences in the field. The differences among provenances seemed to be largely genetically determined as the inclusion of seed mass in the analysis to control for maternal effects did not decrease the degree differences between-provenance differences. In one species, however, non-genetic contributions to population differentiation were found by comparing F1 seeds grown under homogeneous conditions and original seed material. We conclude that potentially large between-provenance differences in germination traits need to be considered in ecological restoration projects, particularly in non-permanent systems where they may determine vegetation development.