Anna Bucharova

Genetic differentiation and regional adaptation among seed origins used for grassland restoration: lessons from a multispecies transplant experiment

Summary One of the key questions in ecosystem restoration is the choice of seed material for restoring plant communities. More and more scientists and practitioners are currently advocating the use of regional seed sources, based on the argument that plants are often adapted to local or regional environmental conditions, and thus, regional seed sources should provide the best restoration success. However, there is still substantial debate about this approach, partly because of a lack of solid empirical data. We conducted a multispecies transplant experiment in which we compared the performance of eight seed origins of seven plant species frequently used in grassland restoration in four common gardens across Germany. We found that, on average, plants of regional origins produced 10% more inflorescences and 7% more biomass than those of foreign origins. There were substantial differences among species in the strength of these effects, but in the majority of the study species fitness decreased with increasing geographical distance of seed origins or with increasing climatic differences between plant origins and experimental sites. In addition to these effects on plant fitness, increasing geographical or climatic distances of origin were often also correlated with increasing differences in plant phenology. Since phenology is important for biotic interactions, especially with pollinators and seed predators, using foreign seed sources may have cascading effects on local ecosystems. Synthesis and applications. Genetic differentiation is widespread in grassland species and often shows the patterns of regional adaptation. Our study thus supports the use of regional seed sources in restoration. Moreover, using non-regional seed sources in grassland restoration may not only decrease the performance of plants, but it will likely also affect their biotic interactions.

Genetic differentiation within multiple common grassland plants supports seed transfer zones for ecological restoration

Summary Ecological restoration of grasslands is increasingly based on regional seeds derived from predefined seed transfer zones. However, the degree and spatial pattern of genetic differentiation among provenances of different seed transfer zones is largely unknown. We assessed the genetic differentiation among eight out of 22 German seed transfer zones for seven common grassland species (Arrhenatherum elatius, Centaurea jacea, Daucus carota, Galium album, Hypochaeris radicata, Knautia arvensis and Lychnis flos-cuculi) using AFLP markers. We analysed genetic population structure with AMOVA and Bayesian cluster analysis and tested for isolation by distance and isolation by environment. In all of the investigated species, almost all pairs of provenances were genetically differentiated. Bayesian cluster analysis revealed species-specific numbers and spatial patterns of gene pools, with between two (Arrhenatherum) and eight clusters (Lychnis). Most investigated seed transfer zones represented a unique gene pool in the majority of the species. We found isolation by distance in four species, isolation by environment, driven by climatic seasonality, in three species, and a lack of both in three species. Thus, the observed genetic differentiation appears to be caused by both neutral and adaptive processes. Synthesis and applications. Our study shows that grassland plants are indeed strongly genetically differentiated across Germany supporting the strategy of seed transfer zones for ecological restoration. Although the predefined seed transfer zones are unlikely to match the exact genetic structure of many species, they serve their purpose by capturing a substantial amount of intraspecific genetic variation across species.

Population biology of two rare fern species: long life and long-lasting stability

UNLABELLED PREMISE OF THE STUDY This study describes the population dynamics of two rare fern species and evaluates the prospects of their survival. This is the first detailed demography study of ferns using transition matrix models. The study species, Asplenium adulterinum and A. cuneifolium, are restricted to serpentine rocks and differ in ploidy level and partly in habitat requirements. Both species are of interest in nature conservation. • METHODS Single life-history traits were evaluated and transition matrix models were used to describe the dynamics of the populations. Population growth rates, elasticity values, and life-table response experiments were used to compare the dynamics between species, years, and different habitat types. Predicted population performance based on models was compared with real data on population growth. • KEY RESULTS All populations of both species are growing. Stable stage distribution based on stochastic simulation corresponds to current stage distribution. The most critical phase of the life cycle is stasis of large adult plants. Reproduction is of low importance. Extinction probability of small populations is low. Mean life span of individuals of both species is 30-50 yr. When compared with real data, the model successfully predicted population performance over 10 yr. • CONCLUSION Populations in the study region are not endangered, and current population dynamics are stable. Differences in life-history traits between species, probability of extinction between species and habitat, and different ploidy-and, thus, probably different dispersal ability-suggest the existence of metapopulation dynamics.

Gene Flow among Populations of Two Rare Co-Occurring Fern Species Differing in Ploidy Level

Differences in ploidy levels among different fern species have a vast influence on their mating system, their colonization ability and on the gene flow among populations. Differences in the colonization abilities of species with different ploidy levels are well known: tetraploids, in contrast to diploids, are able to undergo intra-gametophytic selfing. Because fertilization is a post-dispersal process in ferns, selfing results in better colonization abilities in tetraploids because of single spore colonization. Considerably less is known about the gene flow among populations of different ploidy levels. The present study examines two rare fern species that differ in ploidy. While it has already been confirmed that tetraploid species are better at colonizing, the present study focuses on the gene flow among existing populations. We analyzed the genetic structure of a set of populations in a 10×10 km study region using isoenzymes. Genetic variation in tetraploid species is distributed mainly among populations; the genetic distance between populations is correlated with the geographical distance, and larger populations host more genetic diversity than smaller populations. In the diploid species, most variability is partitioned within populations; the genetic distance is not related to geographic distance, and the genetic diversity of populations is not related to the population size. This suggests that in tetraploid species, which undergo selfing, gene flow is limited. In contrast, in the diploid species, which experience outcrossing, gene flow is extensive and the whole system behaves as one large population. Our results suggest that in ferns, the ability to colonize new habitats and the gene flow among existing populations are affected by the mating system.

Plants adapted to warmer climate do not outperform regional plants during a natural heat wave

Abstract With ongoing climate change, many plant species may not be able to adapt rapidly enough, and some conservation experts are therefore considering to translocate warm‐adapted ecotypes to mitigate effects of climate warming. Although this strategy, called assisted migration, is intuitively plausible, most of the support comes from models, whereas experimental evidence is so far scarce. Here we present data on multiple ecotypes of six grassland species, which we grew in four common gardens in Germany during a natural heat wave, with temperatures 1.4–2.0°C higher than the long‐term means. In each garden we compared the performance of regional ecotypes with plants from a locality with long‐term summer temperatures similar to what the plants experienced during the summer heat wave. We found no difference in performance between regional and warm‐adapted plants in four of the six species. In two species, regional ecotypes even outperformed warm‐adapted plants, despite elevated temperatures, which suggests that translocating warm‐adapted ecotypes may not only lack the desired effect of increased performance but may even have negative consequences. Even if adaptation to climate plays a role, other factors involved in local adaptation, such as biotic interactions, may override it. Based on our results, we cannot advocate assisted migration as a universal tool to enhance the performance of local plant populations and communities during climate change.

Are local plants the best for ecosystem restoration? It depends on how you analyze the data

Abstract One of the key questions in ecosystem restoration is the choice of the seed material for restoring plant communities. The most common strategy is to use local seed sources, based on the argument that many plants are locally adapted and thus local seed sources should provide the best restoration success. However, the evidence for local adaptation is inconsistent, and some of these inconsistencies may be due to different experimental approaches that have been used to test for local adaptation. We illustrate how conclusions about local adaptation depend on the experimental design and in particular on the method of data analysis. We used data from a multispecies reciprocal transplant experiment and analyzed them in three different ways: (1) comparing local vs. foreign plants within species and sites, corresponding to tests of the “local is best” paradigm in ecological restoration, (2) comparing sympatric vs. allopatric populations across sites but within species, and (3) comparing sympatric and allopatric populations across multiple species. These approaches reflect different experimental designs: While a local vs. foreign comparison can be done even in small experiments with a single species and site, the other two approaches require a reciprocal transplant experiment with one or multiple species, respectively. The three different analyses led to contrasting results. While the local/foreign approach indicated lack of local adaptation or even maladaptation, the more general sympatric/allopatric approach rather suggested local adaptation, and the most general cross‐species sympatric/allopatric test provided significant evidence for local adaptation. The analyses demonstrate how the design of experiments and methods of data analysis impact conclusions on the presence or absence of local adaptation. While small‐scale, single‐species experiments may be useful for identifying the appropriate seed material for a specific restoration project, general patterns can only be detected in reciprocal transplant experiments with multiple species and sites.

Priority actions to improve provenance decision-making

Selecting the geographic origin-the provenance-of seed is a key decision in restoration. The last decade has seen a vigorous debate on whether to use local or nonlocal seed. The use of local seed has been the preferred approach because it is expected to maintain local adaptation and avoid deleterious population effects (e.g., maladaptation and outbreeding depression). However, the impacts of habitat fragmentation and climate change on plant populations have driven the debate on whether the local-is-best standard needs changing. This debate has largely been theoretical in nature, which hampers provenance decision-making. Here, we detail cross-sector priority actions to improve provenance decision-making, including embedding provenance trials into restoration projects; developing dynamic, evidence-based provenance policies; and establishing stronger research–practitioner collaborations to facilitate the adoption of research outcomes. We discuss how to tackle these priority actions in order to help satisfy the restoration sector’s requirement for appropriately provenanced seed.

Evolutionary responses to climate change in a range expanding plant

To understand the biological effects of climate change, it is essential to take into account species’ evolutionary responses to their changing environments. Ongoing climate change is resulting in species shifting their geographical distribution ranges poleward. We tested whether a successful range expanding plant has rapidly adapted to the regional conditions in its novel range, and whether adaptation could be driven by herbivores. Furthermore, we investigated if enemy release occurred in the newly colonized areas and whether plant origins differed in herbivore resistance. Plants were cloned and reciprocally transplanted between three experimental sites across the range. Effects of herbivores on plant performance were tested by individually caging plants with either open or closed cages. There was no indication of (regional) adaptation to abiotic conditions. Plants originating from the novel range were always larger than plants from the core distribution at all experimental sites, with or without herbivory. Herbivore damage was highest and not lowest at the experimental sites in the novel range, suggesting no release from enemy impact. Genotypes from the core were more damaged compared to genotypes from newly colonized areas at the most northern site in the novel range, which was dominated by generalist slug herbivory. We also detected subtle shifts in chemical defenses between the plant origins. Genotypes from the novel range had more inducible defenses. Our results suggest that plants that are expanding their range with climate change may evolve increased vigor and altered herbivore resistance in their new range, analogous to invasive plants.

Mix and match: regional admixture provenancing strikes a balance among different seed-sourcing strategies for ecological restoration

One of the main questions in ecosystem restoration is where to obtain the seeds to re-establish plant communities. While the most commonly advocated approach is to use seeds from local sources, some experts argue against this because local populations may harbour little genetic variability for the restored populations to be able to adapt to and survive global change. Instead, they propose alternative strategies such as mixing seeds from various sources to increase genetic variability and adaptive potential, or using seeds from populations that have a similar climate as predicted for the target locality in the future. All these alternative seed-sourcing strategies have in common that they involve a transplanting of plant ecotypes, sometimes over large spatial scales. This is risky because plants from distant origins may be maladapted to the current local abiotic and biotic environment. In addition, introduction of non-local provenances will disrupt natural patterns of within-species biodiversity and will affect ecological networks, with unpredictable consequences. To balance the value of local adaptation with the need for future adaptation potential, we propose ‘regional admixture provenancing’ as a compromise strategy. Here seeds are sourced from multiple populations within the same region as the target locality and mixed prior to use. The mixing of seeds will increase the genetic diversity necessary for future adaptation, while restricting seed origins to a regional scale will maintain regional adaptation and reduce the risk of unintended effects on other biota. This approach is feasible in practice and has recently been implemented in Germany. We believe that it represents a compromise to reconcile opposing views on ecological restoration.

Rapid evolution in native plants cultivated for ecological restoration: not a general pattern

The growing number of restoration projects worldwide increases the demand for seed material of native species. To meet this demand, seeds are often produced through large-scale cultivation on specialised farms, using wild-collected seeds as the original sources. However, during cultivation, plants experience novel environmental conditions compared to those in natural populations, and there is a danger that the plants in cultivation are subject to unintended selection and lose their adaptation to natural habitats. Although the propagation methods are usually designed to maintain as much natural genetic diversity as possible, the effectiveness of these measures have never been tested. We obtained seed of five common grassland species from one of the largest native seed producers in Germany. For each species, the seeds were from multiple generations of seed production. We used AFLP markers and a common garden experiment to test for genetic and phenotypic changes during cultivation of these plants. The molecular markers detected significant evolutionary changes in three out of the five species and we found significant phenotypic changes in two species. The only species that showed substantial genetic and phenotypic changes was the short-lived and predominantly selfing Medicago lupulina, while in the other, mostly perennial and outcrossing species, the observed changes were mostly minor. Agricultural propagation of native seed material for restoration can cause evolutionary changes, at least in some species. We recommend caution, particularly in selfing and short-lived species, where evolution may be more rapid and effects may thus be more severe.