Rapid evolution of selfing syndrome traits in Viola arvensis revealed by resurrection ecology.

PREMISE: As part of global change, climate warming and pollinator decline are expected to affect plant phenology and plant-pollinator interactions. This paper aims at characterizing rapid evolution of life history traits and floral traits over two decades in the wild pansy (Viola arvensis), a common weed in agrosystems. METHODS: We used a resurrection ecology approach with genotypes sampled in 1991 and 2012 from a population in Burgundy (France). The species has a mixed mating system (hereafter: mixed selfer) and presents a floral polymorphism. To correct for maternal effects, we measured plant traits in the second generation in a common garden (after a refreshing generation) to characterize plant evolution during the two decades. In addition, historical population selfing rates in 1991 and 2012 were inferred from microsatellites markers through heterozygote deficiency and identity disequilibrium. RESULTS: Phenotypic data revealed a significant advance in flowering date, reduced flower sizes and a higher propensity of plants to set seed by autonomous selfing. Moreover, we detected a change in color morph frequency with an increase of the pale morph frequency. In accordance with phenotypic data, the neutral genetic data revealed an increase in historical selfing rates from 0.68 in 1991 to 0.86 in 2012. CONCLUSIONS: Taken together, such data suggest that the wild pansy, a mixed selfer, is evolving a selfing syndrome that may be the consequence of reduced pollinator activity in agrosystems.

Mutation bias reflects natural selection in Arabidopsis thaliana.

Since the first half of the twentieth century, evolutionary theory has been dominated by the idea that mutations occur randomly with respect to their consequences1. Here we test this assumption with large surveys of de novo mutations in the plant Arabidopsis thaliana. In contrast to expectations, we find that mutations occur less often in functionally constrained regions of the genome-mutation frequency is reduced by half inside gene bodies and by two-thirds in essential genes. With independent genomic mutation datasets, including from the largest Arabidopsis mutation accumulation experiment conducted to date, we demonstrate that epigenomic and physical features explain over 90% of variance in the genome-wide pattern of mutation bias surrounding genes. Observed mutation frequencies around genes in turn accurately predict patterns of genetic polymorphisms in natural Arabidopsis accessions (r = 0.96). That mutation bias is the primary force behind patterns of sequence evolution around genes in natural accessions is supported by analyses of allele frequencies. Finally, we find that genes subject to stronger purifying selection have a lower mutation rate. We conclude that epigenome-associated mutation bias2 reduces the occurrence of deleterious mutations in Arabidopsis, challenging the prevailing paradigm that mutation is a directionless force in evolution.

Rapid divergent evolution of an annual plant across a latitudinal gradient revealed by seed resurrection.

Global change is expected to drive short-term evolution of natural populations. However, it remains unclear whether different populations are changing in unison. Here, we study contemporary evolution of growth-related and reproductive traits of three populations of Cyanus segetum facing warming and pollinator decline across a latitudinal gradient in France. We resurrected stored seeds sampled up to 24 years apart from northern, central-western, and southern populations and conducted an in situ common-garden experiment. To disentangle neutral from selection-driven differentiation, we calculated neutral genetic differentiation (FST ) and quantitative trait differentiation (QST ) between temporal samples. We found that phenotypic evolution was divergent across populations exhibiting different trends for rosette size, date of flowering, and capitula size. By measuring seed set as a proxy of fitness, we showed that samples with larger mean capitula size outperformed samples with smaller mean capitula size in the western and southern populations. Regression of traits on seed set showed that flowering date and capitula size are the primary determinants of fitness, and QST -FST comparisons indicated that natural selection has likely contributed to the shifts in flowering phenology and rosette size. These findings outline the potential for rescue of natural populations through contemporary evolution and emphasize the complex interplay between spatial and temporal variation in species' responses to global change.

Fitness effects of mutation in natural populations of Arabidopsis thaliana reveal a complex influence of local adaptation.

Little is empirically known about the contribution of mutations to fitness in natural environments. However, Fisher's Geometric Model (FGM) provides a conceptual foundation to consider the influence of the environment on mutational effects. To quantify mutational properties in the field, we established eight sets of MA lines (7-10 generations) derived from eight founders collected from natural populations of Arabidopsis thaliana from French and Swedish sites, representing the range margins of the species in Europe. We reciprocally planted the MA lines and their founders at French and Swedish sites, allowing us to test predictions of FGM under naturally occurring environmental conditions. The performance of the MA lines relative to each other and to their respective founders confirmed some and contradicted other predictions of the FGM: the contribution of mutation to fitness variance increased when the genotype was in an environment where its fitness was low, that is, in the away environment, but mutations were more likely to be beneficial when the genotype was in its home environment. Consequently, environmental context plays a large role in the contribution of mutations to the evolutionary process and local adaptation does not guarantee that a genotype is at or close to its optimum.

Reproductive isolation between populations of Iris atropurpurea is associated with ecological differentiation.

Background and Aims Speciation is often described as a continuous dynamic process, expressed by different magnitudes of reproductive isolation (RI) among groups in different levels of divergence. Studying intraspecific partial RI can shed light on mechanisms underlying processes of population divergence. Intraspecific divergence can be driven by spatially stochastic accumulation of genetic differences following reduced gene flow, resulting in increased RI with increased geographical distance, or by local adaptation, resulting in increased RI with environmental difference. Methods We tested for RI as a function of both geographical distance and ecological differentiation in Iris atropurpurea, an endemic Israeli coastal plant. We crossed plants in the Netanya Iris Reserve population with plants from 14 populations across the species' full distribution, and calculated RI and reproductive success based on fruit set, seed set and fraction of seed viability. Key Results We found that total RI was not significantly associated with geographical distance, but significantly increased with ecological distance. Similarly, reproductive success of the crosses, estimated while controlling for the dependency of each component on the previous stage, significantly reduced with increased ecological distance. Conclusions Our results indicate that the rise of post-pollination reproductive barriers in I. atropurpurea is more affected by ecological differentiation between populations than by geographical distance, supporting the hypothesis that ecological differentiation is predominant over isolation by distance and by reduced gene flow in this species. These findings also affect conservation management, such as genetic rescue, in the highly fragmented and endangered I. atropurpurea.

Neutral processes contribute to patterns of spatial variation for flower colour in the Mediterranean Iris lutescens (Iridaceae).

BACKGROUND AND AIMS: Flower colour polymorphism in plants has been used as a classic model for understanding the importance of neutral processes vs. natural selection in population differentiation. However, current explanations for the maintenance of flower colour polymorphism mainly rely on balancing selection, while neutral processes have seldom been championed. Iris lutescens (Iridaceae) is a widespread species in the northern Mediterranean basin, which shows a stable and striking purple-yellow flower colour polymorphism. To evaluate the roles of neutral processes in the spatial variation for flower colour in this species, patterns of neutral genetic variation across its distribution range were quantified, and phenotypic differentiation was compared with neutral genetic differentiation. METHODS: Genetic diversity levels and population genetic structure were investigated through the genotyping of a collection of 1120 individuals in 41 populations ranging from Spain to France, using a set of eight newly developed microsatellite markers. In addition, phenotypic differentiation for flower colour was also quantified by counting colour morph frequency in each population, and measuring the reflectance spectra of sampled individuals. KEY RESULTS: Populations in Spain present a sharp colour transition from solely purple to solely yellow. The results provide evidence that genetic drift through limited gene flow is important in the evolution of monomorphic populations. In contrast, most populations in France are polymorphic with both phenotypes, and the colour frequencies vary geographically without any spatial gradients observed. A pattern of isolation by distance is detected in France, and gene flow between adjacent populations seems to be an important factor maintaining populations polymorphic. CONCLUSIONS: Overall, neutral processes contribute to patterns of spatial variation for flower colour in I. lutescens, but it cannot be excluded that natural selection is also operating. An interaction between neutral processes and natural selection is suggested to explain the spatial variation for flower colour in I. lutescens.

Flower color polymorphism in Iris lutescens (Iridaceae): biochemical analyses in light of plant-insect interactions.

We describe a flower color polymorphism in Iris lutescens, a species widespread in the Northern part of the Mediterranean basin. We studied the biochemical basis of the difference between purple and yellow flowers, and explored the ecological and evolutionary consequences of such difference, in particular visual discrimination by insects, a potential link with scent emitted and the association between color and scent. Anthocyanins were found to be present in much greater concentrations in purple flowers than in yellow ones, but the anthocyanin composition did not differ between color morphs. Likewise, no quantitative difference in anthocyanin content was found between vegetative tissues of the two morphs. Floral anthocyanins were dominated by delphinidin 3-O-(p-coumaroylrutinoside)-5-O-glucoside (also called delphanin) and its aliphatic derivatives. Small amounts of delphinidin 3-O-(p-caffeoylrutinoside)-5-O-glucoside and its aliphatic derivatives were also characterized. Based on a description of bumblebees' (one of the main pollinators of I. lutescens) color perception, purple and yellow flowers of I. lutescens could be visually discriminated as blue and blue-green, respectively, and likely by a wide variety of other insects. The overall chemical composition of the scent produced was not significantly different between morphs, being dominated by terpenoids, mainly myrcene, (E)-ß-ocimene and limonene. A slight color-scent correlation was nevertheless detected, consistent with the shared biosynthetic origin of both pigments and volatile compounds. Therefore in this species, the difference in the amounts of pigments responsible for flower color difference seems to be the major difference between the two morphs. Pollinators are probably the main selective agent driving the evolution of flower color polymorphism in I. lutescens, which represents a suitable species for investigating how such polymorphism is maintained.

Flowering plants under global pollinator decline.

There is now compelling evidence of a reduction of pollinator richness and density at a global scale. In this opinion article, we argue that such pollinator decline intensifies pollen limitation and reduces plant reproductive success, threatening natural populations of extinction. We use genetic architecture and selection experiments on floral traits and evaluate the potential for plant reproductive strategies to adapt rapidly to new pollination environments. We propose that plant reproductive strategies could adapt to the current pollinator decline by decreasing or increasing their reliance to pollinators, for example, increasing autonomous selfing or reinforcing interactions with pollinators. We further discuss if and how adaptation of plant reproductive strategies can buffer the demographic consequences of pollinator decline, and possibly rescue plant populations from extinction.

Darwin's wind hypothesis: does it work for plant dispersal in fragmented habitats?

Using the wind-dispersed plant Mycelis muralis, we examined how landscape fragmentation affects variation in seed traits contributing to dispersal. Inverse terminal velocity (Vt(-1)) of field-collected achenes was used as a proxy for individual seed dispersal ability. We related this measure to different metrics of landscape connectivity, at two spatial scales: in a detailed analysis of eight landscapes in Spain and along a latitudinal gradient using 29 landscapes across three European regions. In the highly patchy Spanish landscapes, seed Vt(-1)increased significantly with increasing connectivity. A common garden experiment suggested that differences in Vt(-1) may be in part genetically based. The Vt(-1) was also found to increase with landscape occupancy, a coarser measure of connectivity, on a much broader (European) scale. Finally, Vt(-1)was found to increase along a south-north latitudinal gradient. Our results for M. muralis are consistent with 'Darwin's wind dispersal hypothesis' that high cost of dispersal may select for lower dispersal ability in fragmented landscapes, as well as with the 'leading edge hypothesis' that most recently colonized populations harbour more dispersive phenotypes.

Ecophysiological differences among Leymus mollis populations across a subarctic dune system caused by environmental, not genetic, factors.

Plant species that persist during succession, from the colonization to the stabilization stages, face major environmental changes. Such changes are believed to have significant effects on species performance. In subarctic coastal dune systems, Leymus mollis colonizes the embryo dunes, on the upper limit of the beach. It reaches its maximum density on the foredune, but also grows on older, stabilized ridges. This paper reports on the phenotypic variations of some ecophysiological traits associated with the persistence of L. mollis on a dune system on the east coast of Hudson Bay (northern Quebec). Leymus mollis ramets tend to have a lower net carbon assimilation rate and water use efficiency, and a higher substomatal CO2 concentration on the stabilized dune than on the foredune. However, these physiological differences cannot be explained by differences in leaf morphology or nitrogen content. Under controlled conditions, ecophysiological differences observed in the field disappear, suggesting that these are not genetic but determined by environmental changes along the foredune-stabilized dune gradient. We propose that higher net carbon assimilation rate on the foredune might be related to higher sink strength in relation to the growth-stimulating effect of sand burial.