Kenny Helsen

Rapid genetic adaptation precedes the spread of an exotic plant species.

Human activities have increasingly introduced plant species far outside their native ranges under environmental conditions that can strongly differ from those originally met. Therefore, before spreading, and potentially causing ecological and economical damage, non-native species may rapidly evolve. Evidence of genetically based adaptation during the process of becoming invasive is very scant, however, which is due to the lack of knowledge regarding the historical genetic makeup of the introduced populations and the lack of genomic resources. Capitalizing on the availability of old non-native herbarium specimens, we examined frequency shifts in genic SNPs of the Pyrenean Rocket (Sisymbrium austriacum subsp. chrysanthum), comparing the (i) native, (ii) currently spreading non-native and (iii) historically introduced gene pool. Results show strong divergence in flowering time genes during the establishment phase, indicating that rapid genetic adaptation preceded the spread of this species and possibly assisted in overcoming environmental constraints.

Spatial isolation slows down directional plant functional group assembly in restored semi-natural grasslands

Summary 1. Ecological restoration schemes often assume that after reinstating appropriate abiotic conditions, plant communities will assemble following a single predictable pathway towards a fixed target state. This idea has recently been challenged, with increasing evidence that plant community assembly can only be considered deterministic at the plant trait level, rather than at the species level, and that the assembly outcome is largely influenced by the spatial context of the restoration site. 2. We surveyed 147 vegetation plots across a chronosequence of 22 restored semi-natural grassland patches to quantify the effects of spatial isolation on both plant species and plant trait assembly. Trait level assembly was analysed using an emergent group approach, based on 28 functional plant traits. Additionally, we examined the effects of several dispersal-related plant traits on species recolonization capacities. 3. Whereas total plant species richness of the restoration patches did not change through space or through time, progressing assembly was found to consist of a sequential replacement of generalist species with specialist species, which was reflected by a directional assembly at the plant trait level. Grassland isolation was found to slow down community assembly at both the species and the trait level without changing the general direction of assembly. This slowdown became less pronounced with increasing time since restoration. 4. Spatial isolation of the restoration patches was found to act as a trait filter, independent of assembly age. We found a proportionally higher occurrence of species with light seeds and a high seed attachment potential in more isolated restoration patches, suggesting that colonization is more limited in isolated grasslands. 5. Synthesis and applications. We demonstrate that the assembly process, at both the species and the trait level, is influenced by the position of the restoration patch in the landscape. Monitoring schemes following ecological restoration should therefore include the spatial context of the system while using both a trait-based and a species-based plant community analysis. Successful restoration requires physically interconnecting grassland fragments and probably the introduction of seeds or seedlings of species with low dispersability.

Increasing Soil Nutrient Loads of European Semi-natural Grasslands Strongly Alter Plant Functional Diversity Independently of Species Loss

Anthropogenically increased input of nitrogen (N) and phosphorous (P) have led to a severe reduction of plant species richness in European semi-natural grasslands. Although it is well established that this species loss is not trait neutral, a thorough analysis of the effects of nutrient addition on trait based functional diversity and functional composition, independently of species loss, is lacking so far. We compiled data on the plant species abundance (relevé’s) of 279 Nardus grasslands from nine European countries, across a gradient of soil N and P content. Functional diversity (Petchy and Gaston’s FDc, weighted FDc and quadratic entropy) and mean trait composition were calculated for each relevé, based on 21 functional traits. Differences in functional diversity and functional composition were related to differences in soil N, atmospheric N deposition, soil P and pH, while controlling for geographic location and species richness. All functional diversity measures decreased with increasing soil N, with wFDc also decreased by soil P, independent of species loss. This was accompanied by clear shifts in functional trait composition, associated with shifts from below-ground competition for nutrients to above-ground competition for light. This resulted in a decrease in insect-pollinated therophytes and chamaephytes and an increase in long-lived, clonal graminoids and hemicryptophytes under increasing soil N and P. These functional community changes can be expected to alter both ecosystem functioning and service provisioning of the studied grasslands. Our research emphasizes the importance of a reduction of both N and P emission throughout Europe for sustainable conservation of these communities.

Impact of land-use intensity on the conservation of functional and phylogenetic diversity in temperate semi-natural plant communities

The earth is facing a worldwide decline in biodiversity, with land-use change identified as one of the most important drivers. There is evidence that the loss of diversity has a significant impact on ecosystem functioning. Earlier research focused on species richness, but more recent, functional and phylogenetic diversity came into the picture as the stronger determinants of ecosystem processes. The effects of increasing land-use intensity on functional (FD) and phylogenetic diversity (PD), however, are still poorly understood. We studied how FD and PD are affected by land-use intensity in temperate plant communities. Our results show that land-use intensity has a clear impact on species richness, but also affects functional and phylogenetic diversity. Intensive agricultural areas fail to support high and sustainable levels of functional and phylogenetic diversity. These results highlight the need for the protection of biodiversity in nature reserves and the conservation of areas with extensive agricultural practices. Because species richness may influence the measures of functional and phylogenetic diversity, we compared the observed FD and PD values with random values generated with a matrix-swap null model. The observed discrepancy between species loss and the loss of FD and PD calls for an integrated approach to biodiversity conservation, in which the different components of biodiversity are considered together.

Rapid Buildup of Genetic Diversity in Founder Populations of the Gynodioecious Plant Species Origanum vulgare after Semi-Natural Grassland Restoration

In most landscapes the success of habitat restoration is largely dependent on spontaneous colonization of plant species. This colonization process, and the outcome of restoration practices, can only be considered successful if the genetic makeup of founding populations is not eroded through founder effects and subsequent genetic drift. Here we used 10 microsatellite markers to investigate the genetic effects of recent colonization of the long-lived gynodioecious species Origanum vulgare in restored semi-natural grassland patches. We compared the genetic diversity and differentiation of fourteen recent populations with that of thirteen old, putative source populations, and we evaluated the effects of spatial configuration of the populations on colonization patterns. We did not observe decreased genetic diversity in recent populations, or inflated genetic differentiation among them. Nevertheless, a significantly higher inbreeding coefficient was observed in recent populations, although this was not associated with negative fitness effects. Overall population genetic differentiation was low (FST = 0.040). Individuals of restored populations were assigned to on average 6.1 different source populations (likely following the ‘migrant pool’ model). Gene flow was, however, affected by the spatial configuration of the grasslands, with gene flow into the recent populations mainly originating from nearby source populations. This study demonstrates how spontaneous colonization after habitat restoration can lead to viable populations in a relatively short time, overcoming pronounced founder effects, when several source populations are nearby. Restored populations can therefore rapidly act as stepping stones and sources of genetic diversity, likely increasing overall metapopulation viability of the study species.

A direct assessment of realized seed and pollen flow within and between two isolated populations of the food-deceptive orchid Orchis mascula

Gene flow can counteract the loss of genetic diversity caused by genetic drift in small populations. For this reason, clearly understanding gene flow patterns is of the highest importance across fragmented landscapes. However, gene flow patterns are not only dependent upon the degree of spatial isolation of fragmented populations, but are also dependent upon the life-history traits of the species. Indeed, habitat fragmentation effects appear especially unpredictable for food-deceptive orchid species, because of their highly specialised seed and pollen dispersal mechanisms. In this study we used amplified fragment length polymorphism markers and subsequent parentage and spatial autocorrelation analysis to quantify the extent and the patterns of realized gene flow within and between two adjacent fragmented populations of the food-deceptive Orchis mascula. We observed considerable gene flow between both populations, occurring mainly through pollen dispersal. Seed dispersal, on the other hand, was mainly limited to the first few meters from the mother plant in both populations, although at least one among-population seed dispersal event was observed. This, in turn, resulted in a significant spatial genetic structure for both populations. Although genetic diversity was high in both populations and mainly outcrossing occurred, reproductive output was strongly skewed toward a limited number of successful adult plants. These observed patterns are likely due to the different pollinator behaviour associated with food-deceptive plants. We conclude that these populations can be considered viable under their current fragmented state.

Hidden founder effects: small‐scale spatial genetic structure in recently established populations of the grassland specialist plant Anthyllis vulneraria

The long‐term establishment success of founder plant populations has been commonly assessed based on the measures of population genetic diversity and among population genetic differentiation, with founder populations expected to carry sufficient genetic diversity when population establishment is the result of many colonists from multiple source populations (the ‘migrant pool’ colonization model). Theory, however, predicts that, after initial colonization, rapid population expansion may result in a fast increase in the extent of spatial genetic structure (SGS), independent of extant genetic diversity. This SGS can reduce long‐term population viability by increasing inbreeding. Using 12 microsatellite markers, we inferred colonization patterns in four recent populations of the grassland specialist plant Anthyllis vulneraria and compared the extent of SGS between recently established and old populations. Assignment analyses of the individuals of recent population based on the genetic composition of nine adjacent putative source populations suggested the occurrence of the ‘migrant pool’ colonization model, further confirmed by high genetic diversity within and low genetic differentiation among recent populations. Population establishment, however, resulted in the build‐up of strong SGS, most likely as a result of spatially restricted recruitment of the progeny of initial colonists. Although reduced, significant SGS was nonetheless observed to persist in old populations. The presence of SGS was in all populations associated with elevated inbreeding coefficients, potentially affecting the long‐term viability of these populations. In conclusion, this study illustrates the importance of studying SGS next to population genetic diversity and differentiation to adequately infer colonization patterns and long‐term establishment success of plant species.

Evolutionary trends in the distylous genus Pulmonaria (Boraginaceae): Evidence of ancient hybridization and current interspecific gene flow.

The distylous genus Pulmonaria contains approximately 18 species that are widely distributed across Eurasia. Previous studies have shown that species delimitation in the genus is problematic, but have not yet explored the evolutionary history of the genus. Premating reproductive barriers between European species appear to be weak, as several species have strongly overlapping distribution areas, flower at the same time and share the same pollinators, suggesting that hybridization may have contributed to the evolutionary history of Pulmonaria. To test this hypothesis, phylogenetic analyses of nuclear ITS and plastid data (rps16, trnH-psbA, rpl16) from 48 allopatric and four sympatric populations were performed to (1) provide a molecular phylogeny for nine of the most common Pulmonaria species in Europe, (2) detect current and ancient hybridization events, and (3) assess the contribution of hybridization versus incomplete lineage sorting to the inferred phylogenetic patterns. Our results showed that gene trees displayed widespread, strongly supported incongruence associated with the conflicting position of hybrid samples rather than incomplete lineage sorting. Evidence was found of different degrees of hybridization, ranging from current interspecific gene flow at secondary contact zones to introgression at the population level and at least one event of hybrid speciation. Overall, these results suggest that hybridization and introgression were - and could still be - important processes affecting speciation in the genus Pulmonaria.

Impacts of an invasive plant on primary production: testing a functional trait-based framework with a greenhouse experiment

Questions Predicting when invasive species will affect ecosystem functioning remains problematic, with strong contingency upon both the invasive species and the recipient communitys identities. Adopting a functional trait-based approach might overcome this context-dependence. As an early exploration of this approach, we used a greenhouse experiment to assess the potential invasion effects on community trait composition and biomass production. Location We introduced seeds of the invasive plant Impatiens glandulifera from three distant European origins, namely northern France (50.1 °N 2.0 °E), southern Sweden (55.9 °N 12.9 °E) and central Norway (63.5 °N 10.9 °E) to transplanted vegetation turves from the Trondheim area in central Norway. Methods At the end of the greenhouse experiment, we measured plant height, specific leaf area (SLA), leaf dry matter content (LDMC) and standing biomass of both the invasive plant and the turf communities. With this data we evaluated invasion effects on community trait composition and standing biomass (as a first test of ecosystem function effects), including its dependence on invasive species origin and recipient community composition. Results Invasion by I. glandulifera introduced divergent trait values (high plant height and SLA, low LDMC) to the recipient community. The trait set of both the invader and, to a lesser extent, the community were altered following invasion, seemingly driven by increased light competition. Competitive and graminoid-dominated communities showed stronger changes in LDMC following invasion. Functional traits of both the communities and the invasive species helped explain the increase in standing biomass. Southern invader plants more strongly affected the recipient community than their northern counterparts, resulting in stronger biomass reduction of the recipient community. Conclusions This study shows how invasion induced increases in productivity are effectuated through both the introduction of different invader traits and shifts in the co-occurring species trait set, illustrating the potential of a functional trait-based approach. This article is protected by copyright. All rights reserved.

Retention of gene diversity during the spread of a non-native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.