Stomata control gas exchanges between the plant and the atmosphere. How natural variation in stomata size and density contributes to resolve trade-offs between carbon uptake and water loss in response to local climatic variation is not yet understood. We developed an automated confocal microscopy approach to characterize natural genetic variation in stomatal patterning in 330 fully sequenced Arabidopsis thaliana accessions collected throughout the European range of the species. We compared this to variation in water-use efficiency, measured as carbon isotope discrimination (δ C). We detect substantial genetic variation for stomata size and density segregating within Arabidopsis thaliana. A positive correlation between stomata size and δ C further suggests that this variation has consequences on water-use efficiency. Genome wide association analyses indicate a complex genetic architecture underlying not only variation in stomatal patterning but also to its covariation with carbon uptake parameters. Yet, we report two novel QTL affecting δ C independently of stomatal patterning. This suggests that, in A. thaliana, both morphological and physiological variants contribute to genetic variance in water-use efficiency. Patterns of regional differentiation and covariation with climatic parameters indicate that natural selection has contributed to shape some of this variation, especially in Southern Sweden, where water availability is more limited in spring relative to summer. These conditions are expected to favour the evolution of drought avoidance mechanisms over drought escape strategies.
A b s t r a c t Stomata control gas exchanges between the plant and the atmosphere. How natural variation in stomata size and density contributes to resolve trade-offs between carbon uptake and water-loss in response to local climatic variation is not yet understood. We developed an automated confocal microscopy approach to characterize natural genetic variation in stomatal patterning in 330 fully-sequenced Arabidopsis thaliana ecotypes collected throughout the European range of the species. We compared this to variation in water-use efficiency, measured as carbon isotope discrimination (δ 13 C). Combined with public genomic and environmental resources, we show that genetic variation for stomata size and density is pervasive in Arabidopsis thaliana. A positive correlation between stomata size and δ 13 C further shows that this variation has consequences on water-use efficiency. Genome-wide association analyses reveal that many loci of small effect contribute not only to variation in stomata patterning but also to its co-variation with carbon uptake parameters. Yet, we report two novel QTL affecting δ 13 C independently of stomata patterning. This suggests that, in A. thaliana, both morphological and physiological variants contribute to genetic variance in water-use efficiency. Patterns of regional differentiation and co-variation with climatic parameters indicate that natural selection has contributed to shape some of this variation, especially in Southern Sweden, where water availability is comparatively more limited in Spring.
Rapid evolution of traits and of plasticity may enable adaptation to climate change, yet solid experimental evidence under natural conditions is scarce. Here, we imposed rainfall manipulations (+30%, control, À30%) for 10 years on entire natural plant communities in two Eastern Mediterranean sites. Additional sites along a natural rainfall gradient and selection analyses in a greenhouse assessed whether potential responses were adaptive. In both sites, our annual target species Biscutella didyma consistently evolved earlier phenology and higher reproductive allocation under drought. Multiple arguments suggest that this response was adaptive: it aligned with theory, corresponding trait shifts along the natural rainfall gradient, and selection analyses under differential watering in the greenhouse. However, another seven candidate traits did not evolve, and there was little support for evolution of plasticity. Our results provide compelling evidence for rapid adaptive evolution under climate change. Yet, several non-evolving traits may indicate potential constraints to full adaptation.
During range expansion, edge populations are expected to face increased genetic drift, which in turn can alter and potentially compromise adaptive dynamics, preventing the removal of deleterious mutations and slowing down adaptation. Here, we contrast populations of the European sub-species Arabidopsis lyrata ssp petraea, which expanded its Northern range after the last glaciation. We document a sharp decline in effective population size in the range-edge population and observe that non-synonymous variants segregate at higher frequencies. We detect a 4.9% excess of derived non-synonymous variants per individual in the range-edge population, suggesting an increase of the genomic burden of deleterious mutations. Inference of the fitness effects of mutations and modeling of allele frequencies under the explicit demographic history of each population predicts a depletion of rare deleterious variants in the range-edge population, but an enrichment for fixed ones, consistent with the bottleneck effect. However, the demographic history of the range-edge population predicts a small net decrease in per-individual fitness. Consistent with this prediction, the range-edge population is not impaired in its growth and survival measured in a common garden experiment. We further observe that the allelic diversity at the self-incompatibility locus, which ensures strict outcrossing and evolves under negative frequency-dependent selection, has remained unchanged. Genomic footprints indicative of selective sweeps are broader in the Northern population but not less frequent. We conclude that the outcrossing species A. lyrata ssp petraea shows a strong resilience to the effect of range expansion.
Achieving high intraspecific genetic diversity is a critical goal in ecological restoration as it increases the adaptive potential and long-term resilience of populations. Thus, we investigated genetic diversity within and between pristine sites in a fossil floodplain and compared it to sites restored by hay-transfer between 1997 and 2014. RAD-seq genotyping revealed that the stenoecious flood-plain species Arabis nemorensis is co-occurring with individuals that, based on ploidy, ITS-sequencing and morphology, probably belong to the close relative Arabis sagittata, which has a documented preference for dry calcareous grasslands but has not been reported in floodplain meadows. We show that hay-transfer maintains genetic diversity for both species. Additionally, in A. sagittata, transfer from multiple genetically isolated pristine sites resulted in restored sites with increased diversity and admixed local genotypes. In A. nemorensis, transfer did not create novel admixture dynamics because genetic diversity between pristine sites was less differentiated. Thus, the effects of hay-transfer on genetic diversity also depend on the genetic makeup of the donor communities of each species, especially when local material is mixed. Our results demonstrate the efficiency of hay-transfer for habitat restoration and emphasize the importance of pre-restoration characterization of micro-geographic patterns of intraspecific diversity of the community to guarantee that restoration practices reach their goal, i.e. maximize the adaptive potential of the entire restored plant community. Overlooking these patterns may alter the balance between species in the community. Additionally, our comparison of summary statistics obtained from de novo and reference-based RAD-seq pipelines shows that the genomic impact of restoration can be reliably monitored in species lacking prior genomic knowledge.
In plants, local adaptation across species range is frequent. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Genome scans are popular to uncover outlier loci potentially involved in the genetic architecture of local adaptation, however links between outliers and phenotypic variation are rarely addressed. Here we focused on adaptation of teosinte populations along two elevation gradients in Mexico that display continuous environmental changes at a short geographical scale. We used two common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed excess of allele differentiation between pairs of lowland and highland populations and/or correlation with environmental variables. Our results revealed that phenotypic differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation along the elevation gradient indicated that adaptation to altitude results from the assembly of multiple co-adapted traits into a complex syndrome: as elevation increases, plants flower earlier, produce less tillers, display lower stomata density and carry larger, longer and heavier grains. The proportion of outlier SNPs associating with phenotypic variation, however, largely depended on whether we considered a neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating that population stratification greatly affected our results. Finally, chromosomal inversions were enriched for both SNPs whose allele
Achieving high intraspecific genetic diversity is a critical goal in ecological restoration as it increases the adaptive potential and long‐term resilience of populations. Thus, we investigated genetic diversity within and between pristine sites in a fossil floodplain and compared it to sites restored by hay transfer between 1997 and 2014. RAD‐seq genotyping revealed that the stenoecious floodplain species Arabis nemorensis is co‐occurring with individuals that, based on ploidy, ITS‐sequencing and morphology, probably belong to the close relative Arabis sagittata, which has a documented preference for dry calcareous grasslands but has not been reported in floodplain meadows. We show that hay transfer maintains genetic diversity for both species. Additionally, in A. sagittata, transfer from multiple genetically isolated pristine sites resulted in restored sites with increased diversity and admixed local genotypes. In A. nemorensis, transfer did not create novel admixture dynamics because genetic diversity between pristine sites was less differentiated. Thus, the effects of hay transfer on genetic diversity also depend on the genetic make‐up of the donor communities of each species, especially when local material is mixed. Our results demonstrate the efficiency of hay transfer for habitat restoration and emphasize the importance of prerestoration characterization of microgeographic patterns of intraspecific diversity of the community to guarantee that restoration practices reach their goal, that is maximize the adaptive potential of the entire restored plant community. Overlooking these patterns may alter the balance between species in the community. Additionally, our comparison of summary statistics obtained from de novo‐ and reference‐based RAD‐seq pipelines shows that the genomic impact of restoration can be reliably monitored in species lacking prior genomic knowledge.
Rapid evolution of traits and of plasticity may enable adaptation to climate change, yet solid experimental evidence under natural conditions is scarce. Here, we imposed rainfall manipulations (+30%, control, -30%) for ten years on entire natural plant communities in two Eastern Mediterranean sites. Additional sites along a natural rainfall gradient and controlled selection analyses assessed whether potential responses were adaptive. In both sites, our annual target species Biscutella didyma consistently evolved earlier phenology and higher reproductive allocation in dry plots. This response was adaptive, as it aligned with theory, corresponding trait shifts along the natural rainfall gradient, and selection analyses under differential watering in the greenhouse. However, another seven candidate traits did not evolve, and there was little support for evolution of plasticity. Our results provide compelling evidence for rapid adaptive evolution under climate change; yet, they also call attention to potential constraints for full adaptation.
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