MYB transcription factors drive evolutionary innovations in Arabidopsis fruit trichome patterning.

Both inter- and intra-specific diversity has been described for trichome patterning in fruits, which is presumably involved in plant adaptation. However, the mechanisms underlying this developmental trait have been hardly addressed. Here we examined natural populations of Arabidopsis (Arabidopsis thaliana) that develop trichomes in fruits and pedicels, phenotypes previously not reported in the Arabidopsis genus. Genetic analyses identified five loci, MALAMBRUNO 1-5 (MAU1-5), with MAU2, MAU3, and MAU5 showing strong epistatic interactions that are necessary and sufficient to display these traits. Functional characterization of these three loci revealed cis-regulatory mutations in TRICHOMELESS1 and TRIPTYCHON, as well as a structural mutation in GLABRA1. Therefore, the multiple mechanisms controlled by three MYB transcription factors of the core regulatory network for trichome patterning have jointly been modulated to trigger trichome development in fruits. Furthermore, analyses of worldwide accessions showed that these traits and mutations only occur in a highly differentiated relict lineage from the Iberian Peninsula. In addition, these traits and alleles were associated with low spring precipitation, which suggests that trichome development in fruits and pedicels might be involved in climatic adaptation. Thus, we show that the combination of synergistic mutations in a gene regulatory circuit has driven evolutionary innovations in fruit trichome patterning in Arabidopsis.

Differential environmental and genomic architectures shape the natural diversity for trichome patterning and morphology in different Arabidopsis organs.

Despite the adaptive and taxonomic relevance of the natural diversity for trichome patterning and morphology, the molecular and evolutionary mechanisms underlying these traits remain mostly unknown, particularly in organs other than leaves. In this study, we address the ecological, genetic and molecular bases of the natural variation for trichome patterning and branching in multiple organs of Arabidopsis (Arabidopsis thaliana). To this end, we characterized a collection of 191 accessions and carried out environmental and genome-wide association (GWA) analyses. Trichome amount in different organs correlated negatively with precipitation in distinct seasons, thus suggesting a precise fit between trichome patterning and climate throughout the Arabidopsis life cycle. In addition, GWA analyses showed small overlapping between the genes associated with different organs, indicating partly independent genetic bases for vegetative and reproductive phases. These analyses identified a complex locus on chromosome 2, where two adjacent MYB genes (ETC2 and TCL1) displayed differential effects on trichome patterning in several organs. Furthermore, analyses of transgenic lines carrying different natural alleles demonstrated that TCL1 accounts for the variation for trichome patterning in all organs, and for stem trichome branching. By contrast, two other MYB genes (TRY and GL1), mainly showed effects on trichome patterning or branching, respectively.

Ecological, genetic and evolutionary drivers of regional genetic differentiation in Arabidopsis thaliana.

BACKGROUND: Disentangling the drivers of genetic differentiation is one of the cornerstones in evolution. This is because genetic diversity, and the way in which it is partitioned within and among populations across space, is an important asset for the ability of populations to adapt and persist in changing environments. We tested three major hypotheses accounting for genetic differentiation-isolation-by-distance (IBD), isolation-by-environment (IBE) and isolation-by-resistance (IBR)-in the annual plant Arabidopsis thaliana across the Iberian Peninsula, the region with the largest genomic diversity. To that end, we sampled, genotyped with genome-wide SNPs, and analyzed 1772 individuals from 278 populations distributed across the Iberian Peninsula. RESULTS: IBD, and to a lesser extent IBE, were the most important drivers of genetic differentiation in A. thaliana. In other words, dispersal limitation, genetic drift, and to a lesser extent local adaptation to environmental gradients, accounted for the within- and among-population distribution of genetic diversity. Analyses applied to the four Iberian genetic clusters, which represent the joint outcome of the long demographic and adaptive history of the species in the region, showed similar results except for one cluster, in which IBR (a function of landscape heterogeneity) was the most important driver of genetic differentiation. Using spatial hierarchical Bayesian models, we found that precipitation seasonality and topsoil pH chiefly accounted for the geographic distribution of genetic diversity in Iberian A. thaliana. CONCLUSIONS: Overall, the interplay between the influence of precipitation seasonality on genetic diversity and the effect of restricted dispersal and genetic drift on genetic differentiation emerges as the major forces underlying the evolutionary trajectory of Iberian A. thaliana.

African genomes illuminate the early history and transition to selfing in Arabidopsis thaliana.

Over the past 20 y, many studies have examined the history of the plant ecological and molecular model, Arabidopsis thaliana, in Europe and North America. Although these studies informed us about the recent history of the species, the early history has remained elusive. In a large-scale genomic analysis of African A. thaliana, we sequenced the genomes of 78 modern and herbarium samples from Africa and analyzed these together with over 1,000 previously sequenced Eurasian samples. In striking contrast to expectations, we find that all African individuals sampled are native to this continent, including those from sub-Saharan Africa. Moreover, we show that Africa harbors the greatest variation and represents the deepest history in the A. thaliana lineage. Our results also reveal evidence that selfing, a major defining characteristic of the species, evolved in a single geographic region, best represented today within Africa. Demographic inference supports a model in which the ancestral A. thaliana population began to split by 120-90 kya, during the last interglacial and Abbassia pluvial, and Eurasian populations subsequently separated from one another at around 40 kya. This bears striking similarities to the patterns observed for diverse species, including humans, implying a key role for climatic events during interglacial and pluvial periods in shaping the histories and current distributions of a wide range of species.

Genetic rescue by distant trees mitigates qualitative pollen limitation imposed by fine-scale spatial genetic structure.

Restricted seed dispersal frequently leads to fine-scale spatial genetic structure (i.e., FSGS) within plant populations. Depending on its spatial extent and the mobility of pollinators, this inflated kinship at the immediate neighbourhood can critically impoverish pollen quality. Despite the common occurrence of positive FSGS within plant populations, our knowledge regarding the role of long-distance pollination preventing reproductive failure is still limited. Using microsatellite markers, we examined the existence of positive FSGS in two low-density populations of the tree Pyrus bourgaeana. We also designed controlled crosses among trees differing in their kinship to investigate the effects of increased local kinship on plant reproduction. We used six pollination treatments and fully monitored fruit production, fruit and seed weight, proportion of mature seeds per fruit, and seed germination. Our results revealed positive FSGS in both study populations and lower fruit initiation in flowers pollinated with pollen from highly-genetically related individuals within the neighbourhood, with this trend intensifying as the fruit development progressed. Besides, open-pollinated flowers exhibited lower performance compared to those pollinated by distant pollen donors, suggesting intense qualitative pollen limitation in natural populations. We found positive fine-scale spatial genetic structure is translated into impoverished pollen quality from nearby pollen donors which negatively impacts the reproductive success of trees in low-density populations. Under this scenario of intrapopulation genetic rescue by distant pollen donors, the relevance of highly-mobile pollinators for connecting spatially and genetically distant patches of trees may be crucial to safeguarding population recruitment.

Natural Variation Identifies ICARUS1, a Universal Gene Required for Cell Proliferation and Growth at High Temperatures in Arabidopsis thaliana.

Plants are highly sensitive to environmental changes and even small variations in ambient temperature have severe consequences on their growth and development. Temperature affects multiple aspects of plant development, but the processes and mechanisms underlying thermo-sensitive growth responses are mostly unknown. Here we exploit natural variation in Arabidopsis thaliana to identify and characterize novel components and processes mediating thermo-sensitive growth responses in plants. Phenotypic screening of wild accessions identified several strains displaying pleiotropic growth defects, at cellular and organism levels, specifically at high ambient temperatures. Positional cloning and characterization of the underlying gene revealed that ICARUS1 (ICA1), which encodes a protein of the tRNAHis guanylyl transferase (Thg1) superfamily, is required for plant growth at high temperatures. Transcriptome and gene marker analyses together with DNA content measurements show that ICA1 loss-of-function results in down regulation of cell cycle associated genes at high temperatures, which is linked with a block in G2/M transition and endoreduplication. In addition, plants with mutations in ICA1 show enhanced sensitivity to DNA damage. Characterization of additional strains that carry lesions in ICA1, but display normal growth, shows that alternative splicing is likely to alleviate the deleterious effects of some natural mutations. Furthermore, analyses of worldwide and regional collections of natural accessions indicate that ICA1 loss-of-function has arisen several times independently, and that these occur at high frequency in some local populations. Overall our results suggest that ICA1-mediated-modulation of fundamental processes such as tRNAHis maturation, modify plant growth responses to temperature changes in a quantitative and reversible manner, in natural populations.

Environmental and genetic interactions reveal FLOWERING LOCUS C as a modulator of the natural variation for the plasticity of flowering in Arabidopsis.

The timing of flowering initiation depends strongly on the environment, a property termed as the plasticity of flowering. Such plasticity determines the adaptive potential of plants because it provides phenotypic buffer against environmental changes, and its natural variation contributes to evolutionary adaptation. We addressed the genetic mechanisms of the natural variation for this plasticity in Arabidopsis thaliana by analysing a population of recombinant inbred lines derived from Don-0 and Ler accessions collected from distinct climates. Quantitative trait locus (QTL) mapping in four environmental conditions differing in photoperiod, vernalization treatment and ambient temperature detected the folllowing: (i) FLOWERING LOCUS C (FLC) as a large effect QTL affecting flowering time differentially in all environments; (ii) numerous QTL displaying smaller effects specifically in some conditions; and (iii) significant genetic interactions between FLC and other loci. Hence, the variation for the plasticity of flowering is determined by a combination of environmentally sensitive and specific QTL, and epistasis. Analysis of FLC from Don identified a new and more active allele likely caused by a cis-regulatory deletion covering the non-coding RNA COLDAIR. Further characterization of four FLC natural alleles showed different environmental and genetic interactions. Thus, FLC appears as a major modulator of the natural variation for the plasticity of flowering to multiple environmental factors.

Altitudinal and climatic associations of seed dormancy and flowering traits evidence adaptation of annual life cycle timing in Arabidopsis thaliana.

The temporal control or timing of the life cycle of annual plants is presumed to provide adaptive strategies to escape harsh environments for survival and reproduction. This is mainly determined by the timing of germination, which is controlled by the level of seed dormancy, and of flowering initiation. However, the environmental factors driving the evolution of plant life cycles remain largely unknown. To address this question we have analysed nine quantitative life history traits, in a native regional collection of 300 wild accessions of Arabidopsis thaliana. Seed dormancy and flowering time were negatively correlated, indicating that these traits have coevolved. In addition, environmental-phenotypic analyses detected strong altitudinal and climatic clines for most life history traits. Overall, accessions showing life cycles with early flowering, small seeds, high seed dormancy and slow germination rate were associated with locations exposed to high temperature, low summer precipitation and high radiation. Furthermore, we analysed the expression level of the positive regulator of seed dormancy DELAY OF GERMINATION 1 (DOG1), finding similar but weaker altitudinal and climatic patterns than seed dormancy. Therefore, DOG1 regulatory mutations are likely to provide a quantitative molecular mechanism for the adaptation of A. thaliana life cycle to altitude and climate.

Range-wide population genetics and variation in morph ratio in style-dimorphic Narcissus papyraceus.

UNLABELLED: • PREMISE OF THE STUDY: Theoretical models state that natural selection and mating patterns account for floral morph ratio in style-polymorphic plants. However, the demographic history of populations can also influence variation in morph ratios. If so, we hypothesize an association between the morph ratios and the genetic structure across populations.• METHODS: We used nuclear microsatellites to assess genetic variation and structure in populations of Narcissus papyraceus, a style-dimorphic plant whose floral morph ratios (L-morph to S-morph) gradually vary throughout its distribution range in the southwestern Mediterranean Basin. We implemented analyses to relate the genetic features of populations with their morph ratios.• KEY RESULTS: We found greater frequencies of the S-morph in central populations and declining frequencies toward the periphery. This geographic pattern was not associated with the genetic structure of populations. Instead, we found two distinct genetic groups, mainly separated by the Strait of Gibraltar, with a mixture of morph ratios within each one. Overall, there was a weak genetic structure. Genetic diversity was greater in central and southern dimorphic populations than in northern L-monomorphic populations.• CONCLUSIONS: Altogether, our results do not support the hypothesis that the demographic history of populations can account for the observed geographical pattern of morph ratios in N. papyraceus. We suggest that adaptive processes shown in previous studies in the species are the main determinant of the existing variation in the morph composition of populations.

The genetic structure of Arabidopsis thaliana in the south-western Mediterranean range reveals a shared history between North Africa and southern Europe.

BACKGROUND: Deciphering the genetic structure of Arabidopsis thaliana diversity across its geographic range provides the bases for elucidating the demographic history of this model plant. Despite the unique A. thaliana genomic resources currently available, its history in North Africa, the extreme southern limit in the biodiversity hotspot of the Mediterranean Basin, remains virtually unknown. RESULTS: To approach A. thaliana evolutionary history in North Africa, we have analysed the genetic diversity and structure of 151 individuals collected from 20 populations distributed across Morocco. Genotyping of 249 genome-wide SNPs indicated that Morocco contains substantially lower diversity than most analyzed world regions. However, IBD, STRUCTURE and PCA clustering analyses showed that genetic variation is strongly geographically structured. We also determined the genetic relationships between Morocco and the closest European region, the Iberian Peninsula, by analyses of 201 populations from both regions genotyped with the same SNPs. These analyses detected four genetic groups, but all Moroccan accessions belonged to a common Iberian/Moroccan cluster that appeared highly differentiated from the remaining groups. Thus, we identified a genetic lineage with an isolated demographic history in the south-western Mediterranean region. The existence of this lineage was further supported by the study of several flowering genes and traits, which also found Moroccan accessions similar to the same Iberian group. Nevertheless, genetic diversity for neutral SNPs and flowering genes was higher in Moroccan than in Iberian populations of this lineage. Furthermore, we analyzed the genetic relationships between Morocco and other world regions by joint analyses of a worldwide collection of 337 accessions, which detected an additional weak relationship between North Africa and Asia. CONCLUSIONS: The patterns of genetic diversity and structure of A. thaliana in Morocco show that North Africa is part of the species native range and support the occurrence of a glacial refugium in the Atlas Mountains. In addition, the identification of a genetic lineage specific of Morocco and the Iberian Peninsula indicates that the Strait of Gibraltar has been an A. thaliana migration route between Europe and Africa. Finally, the genetic relationship between Morocco and Asia suggests another migration route connecting north-western Africa and Asia.

The Roles of Drift and Selection on Short Stamen Loss in Arabidopsis thaliana along an Elevational Gradient in the Spanish Pyrenees.

Traits that have lost function sometimes persist through evolutionary time. These traits may be maintained by a lack of standing genetic variation for the trait, if selection against the trait is weak relative to drift, or if they have a residual function. To determine the evolutionary processes shaping whether nonfunctional traits are retained or lost, we investigated short stamens in 16 populations of Arabidopsis thaliana along an elevational cline in the Spanish Pyrenees. We found a cline in short stamen number from retention of short stamens in high elevation populations to incomplete loss in low elevation populations. We did not find evidence that limited genetic variation constrains the loss of short stamens at high elevations nor evidence for divergent selection on short stamens between high and low elevations. Finally, we identified loci associated with short stamens in the Spanish Pyrenees that are different from loci associated with variation in short stamen number across latitudes from a previous study. Overall, we did not identify the evolutionary mechanisms maintaining an elevational cline in short stamen number but did identify different genetic loci underlying the variation in short stamen along similar phenotypic clines.

Variation and plasticity in life-history traits and fitness of wild Arabidopsis thaliana populations are not related to their genotypic and ecological diversity.

BACKGROUND: Despite its implications for population dynamics and evolution, the relationship between genetic and phenotypic variation in wild populations remains unclear. Here, we estimated variation and plasticity in life-history traits and fitness of the annual plant Arabidopsis thaliana in two common garden experiments that differed in environmental conditions. We used up to 306 maternal inbred lines from six Iberian populations characterized by low and high genotypic (based on whole-genome sequences) and ecological (vegetation type) diversity. RESULTS: Low and high genotypic and ecological diversity was found in edge and core Iberian environments, respectively. Given that selection is expected to be stronger in edge environments and that ecological diversity may enhance both phenotypic variation and plasticity, we expected genotypic diversity to be positively associated with phenotypic variation and plasticity. However, maternal lines, irrespective of the genotypic and ecological diversity of their population of origin, exhibited a substantial amount of phenotypic variation and plasticity for all traits. Furthermore, all populations harbored maternal lines with canalization (robustness) or sensitivity in response to harsher environmental conditions in one of the two experiments. CONCLUSIONS: Overall, we conclude that the environmental attributes of each population probably determine their genotypic diversity, but all populations maintain substantial phenotypic variation and plasticity for all traits, which represents an asset to endure in changing environments.

Altitudinal and climatic adaptation is mediated by flowering traits and FRI, FLC, and PHYC genes in Arabidopsis.

Extensive natural variation has been described for the timing of flowering initiation in many annual plants, including the model wild species Arabidopsis (Arabidopsis thaliana), which is presumed to be involved in adaptation to different climates. However, the environmental factors that might shape this genetic variation, as well as the molecular bases of climatic adaptation by modifications of flowering time, remain mostly unknown. To approach both goals, we characterized the flowering behavior in relation to vernalization of 182 Arabidopsis wild genotypes collected in a native region spanning a broad climatic range. Phenotype-environment association analyses identified strong altitudinal clines (0-2600 m) in seven out of nine flowering-related traits. Altitudinal clines were dissected in terms of minimum winter temperature and precipitation, indicating that these are the main climatic factors that might act as selective pressures on flowering traits. In addition, we used an association analysis approach with four candidate genes, FRIGIDA (FRI), FLOWERING LOCUS C (FLC), PHYTOCHROME C (PHYC), and CRYPTOCHROME2, to decipher the genetic bases of this variation. Eleven different loss-of-function FRI alleles of low frequency accounted for up to 16% of the variation for most traits. Furthermore, an FLC allelic series of six novel putative loss- and change-of-function alleles, with low to moderate frequency, revealed that a broader FLC functional diversification might contribute to flowering variation. Finally, environment-genotype association analyses showed that the spatial patterns of FRI, FLC, and PHYC polymorphisms are significantly associated with winter temperatures and spring and winter precipitations, respectively. These results support that allelic variation in these genes is involved in climatic adaptation.

Novel natural alleles at FLC and LVR loci account for enhanced vernalization responses in Arabidopsis thaliana.

Vernalization, the induction of flowering by low winter temperatures, is likely to be involved in plant climatic adaptation. However, the genetic, molecular and ecological bases underlying the quantitative variation that tunes vernalization sensitivity to natural environments are largely unknown. To address these questions, we have studied the enhanced vernalization response shown by the Ll-0 accession of Arabidopsis thaliana. Quantitative trait locus (QTL) mapping for several flowering initiation traits in relation to vernalization, in a new Ler × Ll-0 recombinant inbred line (RIL) population, identified large effect alleles at FRI, FLC and HUA2, together with two small effect loci named as Llagostera vernalization response (LVR) 1 and 2. Phenotypic analyses of near isogenic lines validated LVR1 effect on flowering vernalization responses. To further characterize the FLC allele from Ll-0, we carried out genetic association analyses using a regional collection of wild genotypes. FLC-Ll-0 appeared as a low-frequency allele that is distinguished by polymorphism Del(-57), a 50-bp-deletion in the 5'-UTR. Del(-57) was significantly associated with enhanced vernalization responses and FLC RNA expression, as well as with altitude and minimum temperatures. These results are consistent with Del(-57) acting as a novel cis-regulatory FLC polymorphism that may confer climatic adaptation by increasing vernalization sensitivity.

Arabidopsis thaliana populations show clinal variation in a climatic gradient associated with altitude.

• Understanding the adaptive basis of life history variation is a central goal in evolutionary ecology. The use of model species enables the combination of molecular mechanistic knowledge with ecological and evolutionary questions, but the study of life history variation in natural environments is required to merge these disciplines. • Here, we tested for clinal variation in life history and associated traits along an environmental and altitudinal gradient in the model species Arabidopsis thaliana. Seventeen natural populations of A. thaliana were geo-referenced in north-eastern Spain on a gradient in which precipitation increases but maximum spring temperature and minimum winter temperature decrease with altitude. • One hundred and eighty-nine genotypes from the 17 populations were grown under uniform controlled conditions. Variations in traits related to biomass allocation, fecundity, phenology and vegetative growth were tested for relationships with the altitude and climatic variables associated with the home sites. Above-ground mass, number of rosette leaves at bolting, developmental time and seed weight increased with the home site's altitude. Root allocation, vegetative growth during winter and number of seeds decreased with altitude. • We suggest that the differences among home sites provide clues to the variation in adaptive strategies associated with the climatic gradient. We compared these results with adaptations and clinal relationships reported for other species and with molecular mechanisms described in Arabidopsis.

Temporal variation in genetic diversity and effective population size of Mediterranean and subalpine Arabidopsis thaliana populations.

Currently, there exists a limited knowledge on the extent of temporal variation in population genetic parameters of natural populations. Here, we study the extent of temporal variation in population genetics by genotyping 151 genome-wide SNP markers polymorphic in 466 individuals collected from nine populations of the annual plant Arabidopsis thaliana during 4 years. Populations are located along an altitudinal climatic gradient from Mediterranean to subalpine environments in NE Spain, which has been shown to influence key demographic attributes and life cycle adaptations. Genetically, A. thaliana populations were more variable across space than over time. Common multilocus genotypes were detected several years in the same population, whereas low-frequency multilocus genotypes appeared only 1 year. High-elevation populations were genetically poorer and more variable over time than low-elevation populations, which might be caused by a higher overall demographic instability at higher altitudes. Estimated effective population sizes were low but also showed a significant decreasing trend with increasing altitude, suggesting a deeper impact of genetic drift at high-elevation populations. In comparison with single-year samplings, repeated genotyping over time captured substantially higher amount of genetic variation contained in A. thaliana populations. Furthermore, repeated genotyping of populations provided novel information on the genetic properties of A. thaliana populations and allowed hypothesizing on their underlying mechanisms. Therefore, including temporal genotyping programmes into traditional population genetic studies can significantly increase our understanding of the dynamics of natural populations.

Seed germination, seedling traits, and seed bank of the tree Moringa peregrina (Moringaceae) in a hyper-arid environment.

PREMISE OF THE STUDY: Water-limited hot environments are good examples of hyper-aridity. Trees are scarce in these environments but some manage to survive, such as the tree Moringa peregrina. Understanding how trees maintain viable populations in extremely arid environments may provide insight into the adaptive mechanisms by which trees cope with extremely arid weather conditions. This understanding is relevant to the current increasing aridity in several regions of the world. METHODS: Seed germination experiments were conducted to assess variation in seed mass, seed germination, and seedling traits of Moringa peregrina plants and the correlations among these traits. A seed burial experiment was also designed to study the fate of M. peregrina seeds buried at two depths in the soil for two time periods. KEY RESULTS: On average, seeds germinated in three days and seedling shoots grew 0.7 cm per day over three weeks. Larger seeds decreased germination time and increased seedling growth rates relative to smaller seeds. Seeds remained quiescent in the soil and germination was very high at both depths and burial times. CONCLUSIONS: The after-ripening time of Moringa peregrina seeds is short and seeds germinate quickly after imbibition. Plants of M. peregrina may increase in hyper-arid environments from seeds with larger mass, shorter germination times, and faster seedling growth rates. The results also illustrate the adjustment in allocation to seed biomass and correlations among seed and seedling traits that allows M. peregrina to be successful in coping with aridity in its environment.

Characterization of microsatellite loci in Erysimum mediohispanicum (Brassicaceae) and cross-amplification in related species.

PREMISE OF THE STUDY: We have developed and optimized microsatellite loci from a genomic library of Erysimum mediohispanicum. Microsatellites were also tested for cross-amplification in 31 other Erysimum species. METHODS AND RESULTS: A total of 10 microsatellite loci were successfully amplified. They were polymorphic for 81 E. mediohispanicum individuals from two locations in Sierra Nevada (southeastern Spain), which showed similar patterns of genetic diversity. On average, microsatellites had 8.6 alleles per locus and an expected heterozygosity of 0.69. Only one locus significantly departed from Hardy-Weinberg equilibrium in both locations. Most of the markers successfully amplified in other Erysimum species. CONCLUSIONS: The genetic attributes of microsatellite loci will allow their application to population genetic studies in Erysimum, such as genetic differentiation and structure, gene flow, pollinator-mediated speciation, and hybridization studies.

Depicting the phenotypic space of the annual plant Diplotaxis acris in hyperarid deserts.

The phenotypic space encompasses the assemblage of trait combinations yielding well-suited integrated phenotypes. At the population level, understanding the phenotypic space structure requires the quantification of among- and within-population variations in traits and the correlation pattern among them. Here, we studied the phenotypic space of the annual plant Diplotaxis acris occurring in hyperarid deserts. Given the advance of warming and aridity in vast regions occupied by drylands, D. acris can indicate the successful evolutionary trajectory that many other annual plant species may follow in expanding drylands. To this end, we conducted a greenhouse experiment with 176 D. acris individuals from five Saudi populations to quantify the genetic component of variation in architectural and life history traits. We found low among-population divergence but high among-individual variation in all traits. In addition, all traits showed a high degree of genetic determination in our study experimental conditions. We did not find significant effects of recruitment and fecundity on fitness. Finally, all architectural traits exhibited a strong correlation pattern among them, whereas for life history traits, only higher seed germination implied earlier flowering. Seed weight appeared to be an important trait in D. acris as individuals with heavier seeds tended to advance flowering and have a more vigorous branching pattern, which led to higher fecundity. Population divergence in D. acris might be constrained by the severity of the hyperarid environment, but populations maintain high among-individual genetic variation in all traits. Furthermore, D. acris showed phenotypic integration for architectural traits and, to a lesser extent, for life history traits. Overall, we hypothesize that D. acris may be fine-tuned to its demanding extreme environments. Evolutionary speaking, annual plants facing increasing warming, aridity, and environmental seasonality might modify their phenotypic spaces toward new phenotypic configurations strongly dominated by correlated architectural traits enhancing fecundity and seed-related traits advancing flowering time.

Introduction to the Special Issue: The ecology and genetics of population differentiation in plants.

Population differentiation is a pervasive process in nature. At present, evolutionary studies on plant population differentiation address key questions by undertaking joint ecological and genetic approaches and employing a combination of molecular and experimental means. In this special issue, we gathered a collection of papers dealing with various ecological and genetic aspects of population differentiation in plants. In particular, this special issue encompasses eight research articles and two reviews covering a wide array of worldwide environments, plant functional types, genetic and genomic approaches, and common garden experiments to quantify molecular and/or quantitative trait differentiation in plant populations. Overall, this special issue stresses the validity of traditional evolutionary studies focused on plant populations, whilst emphasizing the integration of classical biological disciplines and state-of-the-art molecular techniques into a unique toolkit for evolutionary plant research.