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1.  The effect of drought stress on heterozygosity–fitness correlations in pedunculate oak (Quercus robur) 
Annals of Botany  2014;113(6):1057-1069.
Background and Aims
The interaction between forest fragmentation and predicted climate change may pose a serious threat to tree populations. In small and spatially isolated forest fragments, increased homozygosity may directly affect individual tree fitness through the expression of deleterious alleles. Climate change-induced drought stress may exacerbate these detrimental genetic consequences of forest fragmentation, as the fitness response to low levels of individual heterozygosity is generally thought to be stronger under environmental stress than under optimal conditions.
To test this hypothesis, a greenhouse experiment was performed in which various transpiration and growth traits of 6-month-old seedlings of Quercus robur differing in multilocus heterozygosity (MLH) were recorded for 3 months under a well-watered and a drought stress treatment. Heterozygosity–fitness correlations (HFC) were examined by correlating the recorded traits of individual seedlings to their MLH and by studying their response to drought stress.
Key Results
Weak, but significant, effects of MLH on several fitness traits were obtained, which were stronger for transpiration variables than for the recorded growth traits. High atmospheric stress (measured as vapour pressure deficit) influenced the strength of the HFCs of the transpiration variables, whereas only a limited effect of the irrigation treatment on the HFCs was observed.
Under ongoing climate change, increased atmospheric stress in the future may strengthen the negative fitness responses of trees to low MLH. This indicates the necessity to maximize individual multilocus heterozygosity in forest tree breeding programmes.
PMCID: PMC3997642  PMID: 24638819
Climate change; drought stress; forest fragmentation; greenhouse experiment; growth traits; heterozygosity–fitness correlations; pedunculate oak; Quercus robur; transpiration
2.  The impact of extensive clonal growth on fine-scale mating patterns: a full paternity analysis of a lily-of-the-valley population (Convallaria majalis) 
Annals of Botany  2013;111(4):623-628.
Background and Aims
The combination of clonality and a mating system promoting outcrossing is considered advantageous because outcrossing avoids the fitness costs of selfing within clones (geitonogamy) while clonality assures local persistence and increases floral display. The spatial spread of genetically identical plants (ramets) may, however, also decrease paternal diversity (the number of sires fertilizing a given dam) and fertility, particularly towards the centre of large clumped clones. This study aimed to quantify the impact of extensive clonal growth on fine-scale paternity patterns in a population of the allogamous Convallaria majalis.
A full analysis of paternity was performed by genotyping all flowering individuals and all viable seeds produced during a single season using AFLP. Mating patterns were examined and the spatial position of ramets was related to the extent of multiple paternity, fruiting success and seed production.
Key Results
The overall outcrossing rate was high (91 %) and pollen flow into the population was considerable (27 %). Despite extensive clonal growth, multiple paternity was relatively common (the fraction of siblings sharing the same father was 0·53 within ramets). The diversity of offspring collected from reproductive ramets surrounded by genetically identical inflorescences was as high as among offspring collected from ramets surrounded by distinct genets. There was no significant relationship between the similarity of the pollen load received by two ramets and the distance between them. Neither the distance of ramets with respect to distinct genets nor the distance to the genet centre significantly affected fruiting success or seed production.
Random mating and considerable pollen inflow most probably implied that pollen dispersal distances were sufficiently high to mitigate local mate scarcity despite extensive clonal spread. The data provide no evidence for the intrusion of clonal growth on fine-scale plant mating patterns.
PMCID: PMC3605957  PMID: 23439847
Paternity analysis; mate diversity; outcrossing; mating opportunities; AFLP; reproductive success; seed set; ramet; lily-of-the-valley; Convallaria majalis
3.  Differences in fine-scale spatial genetic structure across the distribution range of the distylous forest herb Pulmonaria officinalis (Boraginaceae) 
BMC Genetics  2013;14:101.
Geographical ranges of plants and their pollinators do not always entirely overlap and it has been suggested that the absence of specialized pollinators at range margins may induce changes in mating systems. Because a species’ mating system is known to have a considerable effect on within-population pollen movement, the extent of fine-scale spatial genetic structure (SGS) can be expected to differ between populations located at different parts of their geographical range. To test this prediction, we compared the fine-scale SGS between two core and two disjunct populations of the distylous forest herb Pulmonaria officinalis. Because in disjunct populations of this species the heteromorphic self-incompatibility system showed relaxation in the long-styled morph, but not in the short-styled morph, we also hypothesized that the extent of fine-scale SGS and clustering differed between morphs.
Spatial autocorrelation analyses showed a significant decrease in genetic relatedness with spatial distance for both core and disjunct populations with the weakest SGS found in one of the core populations (Sp = 0.0014). No evidence of stronger SGS in the long-styled morph was found in the center of the range whereas one disjunct population showed a significantly (P = 0.029) higher SGS in the long-styled morph (SpL = 0.0070) than in the short-styled morph (SpS = 0.0044).
Consistent with previous analyses on distylous plant species, we found weak, but significant spatial genetic structure. However, the extent of SGS varied substantially between populations within regions, suggesting that population characteristics other than mating system (e.g. local pollinator assemblages, population history) may be as important in determining variation in SGS.
PMCID: PMC4015958  PMID: 24134743
Fine-scale spatial genetic structure; Disjunct; Core; Mating system; Morph clustering; Spatial autocorrelation
4.  The role of seed traits in determining the phylogenetic structure of temperate plant communities 
Annals of Botany  2012;110(3):629-636.
Background and Aims
Phylogenetic clustering of species within plant communities can be expected to result from environmental filtering acting on an evolutionary-conserved plant trait. One such a candidate trait is the embryo to seed-size ratio (E:S). A high E:S may allow faster germination immediately after imbibition, and is therefore assumed to be advantageous in dry habitats. In this study the hypothesis was tested that habitat filtering driven by soil moisture conditions and acting on seed germination and seedling establishment is an important ecological mechanism in structuring temperate plant communities.
Vegetation samplings were performed in three habitats located within 200 km of each other in western Europe: Ellenberg indicator values showed that the habitats selected differed substantially in terms of soil moisture and light availability. E.S ratio and seed mass data for all genera were obtained from literature. Data were analysed using recently developed phylogenetic methods.
Key Results
Genera with a similar E:S tend to co-occur, as low and high E:S genera dominate in moist and dry habitats, respectively. A phylogenetically clustered pattern of community structure was evident, and dispersion of E:S was positively related to phylogenetic dispersion.
The phenotypically and phylogenetically clustered pattern indicates that E:S-mediated habitat filtering is an important assembly process structuring the plant community of the temperate climate habitats studied.
PMCID: PMC3400449  PMID: 22684681
Calcareous grassland; dune slacks; embryo size; habitat filtering; phylogenetic structure; plant community structure; seed mass; temperate forest
5.  Rapid Buildup of Genetic Diversity in Founder Populations of the Gynodioecious Plant Species Origanum vulgare after Semi-Natural Grassland Restoration 
PLoS ONE  2013;8(6):e67255.
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.
PMCID: PMC3686717  PMID: 23840642
6.  Among-Population Variation in Microbial Community Structure in the Floral Nectar of the Bee-Pollinated Forest Herb Pulmonaria officinalis L 
PLoS ONE  2013;8(3):e56917.
Microbial communities in floral nectar have been shown to be characterized by low levels of species diversity, yet little is known about among-plant population variation in microbial community composition.
Methodology/Principal Findings
We investigated the microbial community structure (yeasts and bacteria) in floral nectar of ten fragmented populations of the bee-pollinated forest herb Pulmonaria officinalis. We also explored possible relationships between plant population size and microbial diversity in nectar, and related microbial community composition to the distance separating plant populations. Culturable bacteria and yeasts occurring in the floral nectar of a total of 100 plant individuals were isolated and identified by partially sequencing the 16S rRNA gene and D1/D2 domains of the 26S rRNA gene, respectively. A total of 9 and 11 yeast and 28 and 39 bacterial OTUs was found, taking into account a 3% (OTU0.03) and 1% sequence dissimilarity cut-off (OTU0.01). OTU richness at the plant population level (i.e. the number of OTUs per population) was low for yeasts (mean: 1.7, range: 0–4 OTUs0.01/0.03 per population), whereas on average 6.9 (range: 2–13) OTUs0.03 and 7.9 (range 2–16) OTUs0.01 per population were found for bacteria. Both for yeasts and bacteria, OTU richness was not significantly related to plant population size. Similarity in community composition among populations was low (average Jaccard index: 0.14), and did not decline with increasing distance between populations.
We found low similarity in microbial community structure among populations, suggesting that the assembly of nectar microbiota is to a large extent context-dependent. Although the precise factors that affect variation in microbial community structure in floral nectar require further study, our results indicate that both local and regional processes may contribute to among-population variation in microbial community structure in nectar.
PMCID: PMC3594240  PMID: 23536759
7.  Reproductive isolation and hybridization in sympatric populations of three Dactylorhiza species (Orchidaceae) with different ploidy levels 
Annals of Botany  2011;109(4):709-720.
Background and Aims
The potential for gene exchange between species with different ploidy levels has long been recognized, but only a few studies have tested this hypothesis in situ and most of them focused on not more than two co-occurring species. In this study, we examined hybridization patterns in two sites containing three species of the genus Dactylorhiza (diploid D. incarnata and D. fuchsii and their allotetraploid derivative D. praetermissa).
To compare the strength of reproductive barriers between diploid species, and between diploid and tetraploid species, crossing experiments were combined with morphometric and molecular analyses using amplified fragment length polymorphism markers, whereas flow cytometric analyses were used to verify the hybrid origin of putative hybrids.
Key Results
In both sites, extensive hybridization was observed, indicating that gene flow between species is possible within the investigated populations. Bayesian assignment analyses indicated that the majority of hybrids were F1 hybrids, but in some cases triple hybrids (hybrids with three species as parents) were observed, suggesting secondary gene flow. Crossing experiments showed that only crosses between pure species yielded a high percentage of viable seeds. When hybrids were involved as either pollen-receptor or pollen-donor, almost no viable seeds were formed, indicating strong post-zygotic reproductive isolation and high sterility.
Strong post-mating reproductive barriers prevent local breakdown of species boundaries in Dactylorhiza despite frequent hybridization between parental species. However, the presence of triple hybrids indicates that in some cases hybridization may extend the F1 generation.
PMCID: PMC3286275  PMID: 22186278
AFLP; Dactylorhiza incarnata; Dactylorhiza praetermissa; genetic analysis; hybridization; morphology; polyploidy; reproductive isolation; triple hybrid
8.  Genetic variation and risks of introgression in the wild Coffea arabica gene pool in south-western Ethiopian montane rainforests 
Evolutionary Applications  2012;6(2):243-252.
The montane rainforests of SW Ethiopia are the primary centre of diversity of Coffea arabica and the origin of all Arabica coffee cultivated worldwide. This wild gene pool is potentially threatened by forest fragmentation and degradation, and by introgressive hybridization with locally improved coffee varieties. We genotyped 703 coffee shrubs from unmanaged and managed coffee populations, using 24 microsatellite loci. Additionally, we genotyped 90 individuals representing 23 Ethiopian cultivars resistant to coffee berry disease (CBD). We determined population genetic diversity, genetic structure, and admixture of cultivar alleles in the in situ gene pool. We found strong genetic differentiation between managed and unmanaged coffee populations, but without significant differences in within-population genetic diversity. The widespread planting of coffee seedlings including CBD-resistant cultivars most likely offsets losses of genetic variation attributable to genetic drift and inbreeding. Mixing cultivars with original coffee genotypes, however, leaves ample opportunity for hybridization and replacement of the original coffee gene pool, which already shows signs of admixture. In situ conservation of the wild gene pool of C. arabica must therefore focus on limiting coffee production in the remaining wild populations, as intensification threatens the genetic integrity of the gene pool by exposing wild genotypes to cultivars.
PMCID: PMC3689350  PMID: 23798974
admixture; Afromontane rainforest; coffee; crop wild relative; ecosystem services; genetic erosion
9.  Biased morph ratios and skewed mating success contribute to loss of genetic diversity in the distylous Pulmonaria officinalis 
Annals of Botany  2011;109(1):227-235.
Background and Aims
In heterostylous plant species, skewed morph ratios are not uncommon and may arise from a range of factors. Despite the recognized importance of skewed morph ratios on overall reproductive success within populations, little is known about the impact of skewed morph ratios on population genetic diversity and differentiation in heterostylous species. This study specifically aimed to clarify the effect of population size and morph bias on population genetic diversity and differentiation in the temperate forest herb Pulmonaria officinalis. This species is characterized by a distylous breeding system and shows morph-specific differences in reproductive success.
Genetic diversity was determined for 27 P. officinalis populations in northern Belgium by using eight recently developed microsatellite markers. Multiple regressions were used to assess the relationship between genetic diversity, morph bias and population size, and FST-values were calculated for short- and long-styled morphs separately to study genetic differentiation as a function of morph type.
Key Results
For all genetic measures used, morph bias was more important in explaining patterns of genetic diversity than population size, and in all cases patterns of population genetic diversity followed a quadratic function, which showed a symmetrical decrease in genetic diversity with increasing morph bias. However, probably due to the reproductive advantage of L-morphs relative to S-morphs, maximum genetic diversity was found in populations showing an excess of L-morphs (60·7 % L-morph). On the other hand, no significant difference in pairwise genetic distances between populations was observed between L- (0·107) and S-morphs (0·106).
Our results indicate that significant deviations from equal morph ratios not only affect plant reproductive success but also population genetic diversity of heterostylous plant species. Hence, when defining conservation measures for populations of heterostylous plant species, morph ratios should be considered as an important trait affecting their long-term population viability.
PMCID: PMC3241589  PMID: 22021814
Boraginaceae; distyly; FST; genetic diversity; microsatellite analysis; morph bias; Pulmonaria officinalis; skewed mating success
10.  Asymmetric gene introgression in two closely related Orchis species: evidence from morphometric and genetic analyses 
In food-deceptive orchids of the genera Anacamptis, Neotinea and Orchis floral isolation has been shown to be weak, whereas late-acting reproductive barriers are mostly strong, often restricting hybridization to the F1 generation. Only in a few species hybridization extends beyond the F1 generation, giving rise to hybrid swarms. However, little is known about the abundance of later-generation hybrids and what factors drive their occurrence in hybrid populations. In this study, molecular analyses were combined with detailed morphological measurements in a hybrid population of two closely related Orchis species (Orchis militaris and O. purpurea) to investigate the hypothesis that the abundance of later-generation hybrids is driven by changes in floral characters after hybridization that exert selective pressures that in turn affect hybridization.
Both the molecular and morphological data point to extensive genetic and morphological homogenization and asymmetric introgression. Estimating genomic clines from the multi-locus genotype data and testing for deviation from neutrality revealed that 30 out of 113 (27%) AFLP markers significantly deviated from neutral expectations. Plants with large floral displays or plant with flowers that resembled more O. purpurea had higher female fitness than plants with small floral displays or plants with flowers resembling more O. militaris, suggesting that directional selection may have contributed to the observed patterns of introgression.
These results indicate that in closely related orchid species hybridization and gene introgression may be partly driven by selection for floral traits of one of the parental types. However, because some pure individuals were still present in the studied population, the parental species appeared to be sufficiently isolated to survive the challenge of sympatry.
PMCID: PMC3523012  PMID: 22967086
Admixture; Hybrid swarm; Orchis; Orchidaceae; Reproductive isolation
11.  Mycorrhizal associations and reproductive isolation in three closely related Orchis species 
Annals of Botany  2010;107(3):347-356.
Background and Aims
The maintenance of species boundaries in sympatric populations of closely related species requires some kind of reproductive isolation that limits gene flow among species and/or prevents the production of viable progeny. Because in orchids mycorrhizal fungi are needed for seed germination and subsequent seedling establishment, orchid–mycorrhizal associations may be involved in acting as a post-mating barrier.
We investigated the strength of post-mating barriers up to the seed germination stage acting between three closely related Orchis species (Orchis anthropophora, O. militaris and O. purpurea) and studied the role of mycorrhizal fungi in hybridization by burying seed packets of pure and hybrid seeds. After retrieval and assessment of seed germination, the fungi associating with protocorms originating from hybrid and pure seeds were determined and compared with those associating with adult individuals using DNA array technology.
Whereas pre-zygotic post-mating barriers were rather weak in most crosses, post-zygotic post-mating barriers were stronger, particularly when O. purpurea was crossed with O. anthropophora. Germination trials in the field showed that seed germination percentages of hybrid seeds were in most cases lower than those originating from pure crosses. In all species pair combinations, total post-mating reproductive isolation was asymmetric. Protocorms associated with a smaller range of fungal symbionts than adult plants, but there was considerable overlap in mycorrhizal associations between protocorms and their respective parents.
Our results suggest that mycorrhizal associations contribute little to reproductive isolation. Pre-mating barriers are probably the main factors determining hybridization rates between the investigated species.
PMCID: PMC3043927  PMID: 21186239
DNA array; gene flow; hybrid zones; mycorrhizal associations; reproductive barriers; seed germination
12.  Forest restoration, biodiversity and ecosystem functioning 
BMC Ecology  2011;11:29.
Globally, forests cover nearly one third of the land area and they contain over 80% of terrestrial biodiversity. Both the extent and quality of forest habitat continue to decrease and the associated loss of biodiversity jeopardizes forest ecosystem functioning and the ability of forests to provide ecosystem services. In the light of the increasing population pressure, it is of major importance not only to conserve, but also to restore forest ecosystems.
Ecological restoration has recently started to adopt insights from the biodiversity-ecosystem functioning (BEF) perspective. Central is the focus on restoring the relation between biodiversity and ecosystem functioning. Here we provide an overview of important considerations related to forest restoration that can be inferred from this BEF-perspective.
Restoring multiple forest functions requires multiple species. It is highly unlikely that species-poor plantations, which may be optimal for above-ground biomass production, will outperform species diverse assemblages for a combination of functions, including overall carbon storage and control over water and nutrient flows. Restoring stable forest functions also requires multiple species. In particular in the light of global climatic change scenarios, which predict more frequent extreme disturbances and climatic events, it is important to incorporate insights from the relation between biodiversity and stability of ecosystem functioning into forest restoration projects. Rather than focussing on species per se, focussing on functional diversity of tree species assemblages seems appropriate when selecting tree species for restoration. Finally, also plant genetic diversity and above - below-ground linkages should be considered during the restoration process, as these likely have prominent but until now poorly understood effects at the level of the ecosystem.
The BEF-approach provides a useful framework to evaluate forest restoration in an ecosystem functioning context, but it also highlights that much remains to be understood, especially regarding the relation between forest functioning on the one side and genetic diversity and above-ground-below-ground species associations on the other. The strong emphasis of the BEF-approach on functional rather than taxonomic diversity may also be the beginning of a paradigm shift in restoration ecology, increasing the tolerance towards allochthonous species.
PMCID: PMC3234175  PMID: 22115365
13.  Extremely low genotypic diversity and sexual reproduction in isolated populations of the self-incompatible lily-of-the-valley (Convallaria majalis) and the role of the local forest environment 
Annals of Botany  2010;105(5):769-776.
Background and Aims
Clonal growth is a common phenomenon in plants and allows them to persist when sexual life-cycle completion is impeded. Very low levels of recruitment from seed will ultimately result in low levels of genotypic diversity. The situation can be expected to be exacerbated in spatially isolated populations of obligated allogamous species, as low genotypic diversities will result in low availability of compatible genotypes and low reproductive success. Populations of the self-incompatible forest herb lily-of-the-valley (Convallaria majalis) were studied with the aim of inferring the relative importance of sexual and asexual recruitment. Then the aim was to establish a relationship between genotypic diversity, sexual reproduction and the local forest environment.
Highly polymorphic microsatellite markers were used to investigate clonal diversities and population genetic structure of 20 populations of C. majalis in central Belgium.
Key Results
Most of the populations studied consisted of a single genotype and linkage disequilibrium within populations was high, manifesting clonal growth as the main mode of reproduction. A population consisting of multiple genotypes mainly occurred in locations with a thin litter layer and high soil phosphorus levels, suggesting environment-mediated sporadic recruitment from seed. Highly significant genetic differentiation indicated that populations are reproductively isolated. In agreement with the self-incompatibility of C. majalis, monoclonal populations showed very low or even absent fruit set.
Lack of sexual recruitment in spatially isolated C. majalis populations has resulted in almost monoclonal populations with reduced or absent sexual reproduction, potentially constraining their long-term persistence. The local forest environment may play an important role in mediating sexual recruitment in clonal forest plant species.
PMCID: PMC2859916  PMID: 20228091
Convallaria majalis; clonal; genotypic diversity; population genetics; remnant populations; SSR; forest herb; rhizomatous; self-incompatible; reproductive success
14.  Large population sizes mitigate negative effects of variable weather conditions on fruit set in two spring woodland orchids 
Biology Letters  2009;5(4):495-498.
Global circulation models predict increased climatic variability, which could increase variability in demographic rates and affect long-term population viability. In animal-pollinated species, pollination services, and thus fruit and seed set, may be highly variable among years and sites, and depend on both local environmental conditions and climatic variables. Orchid species may be particularly vulnerable to disruption of their pollination services, as most species depend on pollinators for successful fruit set and because seed germination and seedling recruitment are to some extent dependent on the amount of fruits and seeds produced. Better insights into the factors determining fruit and seed set are therefore indispensable for a better understanding of population dynamics and viability of orchid populations under changing climatic conditions. However, very few studies have investigated spatio-temporal variation in fruit set in orchids. Here, we quantified fruit production in eight populations of the orchid Orchis purpurea that does not reward pollinators and 13 populations of the rewarding Neottia (Listera) ovata during five consecutive years (2002–2006). Fruit production in large populations showed much higher stability than that in small populations and was less affected by extreme weather conditions. Our results highlight the potential vulnerability of small orchid populations to an increasingly variable climate through highly unpredictable fruit-set patterns.
PMCID: PMC2781932  PMID: 19457885
environmental stochasticity; female reproductive success; orchids; pollination; temporal variability
15.  Rapid loss of genetic variation in a founding population of Primula elatior (Primulaceae) after colonization 
Annals of Botany  2008;103(5):777-783.
Background and Aims
Land-use changes and associated extinction/colonization dynamics can have a large impact on population genetic diversity of plant species. The aim of this study was to investigate genetic diversity in a founding population of the self-incompatible forest herb Primula elatior and to elucidate the processes that affect genetic diversity shortly after colonization.
AFLP markers were used to analyse genetic diversity across three age classes and spatial genetic structure within a founding population of P. elatior in a recently established stand in central Belgium. Parentage analyses were used to assess the amount of gene flow from outside the population and to investigate the contribution of mother plants to future generations.
The genetic diversity of second and third generation plants was significantly reduced compared with that of first generation plants. Significant spatial genetic structure was observed. Parentage analyses showed that <20 % of the youngest individuals originated from parents outside the study population and that >50 % of first and second generation plants did not contribute to seedling recruitment.
These results suggest that a small effective population size and genetic drift can lead to rapid decline of genetic diversity of offspring in founding populations shortly after colonization. This multigenerational study also highlights that considerable amounts of gene flow seem to be required to counterbalance genetic drift and to sustain high levels of genetic diversity after colonization in recently established stands.
PMCID: PMC2707865  PMID: 19106180
AFLP; colonization; forest regeneration; genetic diversity; genetic drift; parentage analysis; spatial genetic structure

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