Divergent trait and environment relationships among parallel radiations in Pelargonium (Geraniaceae): a role for evolutionary legacy?

Functional traits in closely related lineages are expected to vary similarly along common environmental gradients as a result of shared evolutionary and biogeographic history, or legacy effects, and as a result of biophysical tradeoffs in construction. We test these predictions in Pelargonium, a relatively recent evolutionary radiation. Bayesian phylogenetic mixed effects models assessed, at the subclade level, associations between plant height, leaf area, leaf nitrogen content and leaf mass per area (LMA), and five environmental variables capturing temperature and rainfall gradients across the Greater Cape Floristic Region of South Africa. Trait-trait integration was assessed via pairwise correlations within subclades. Of 20 trait-environment associations, 17 differed among subclades. Signs of regression coefficients diverged for height, leaf area and leaf nitrogen content, but not for LMA. Subclades also differed in trait-trait relationships and these differences were modulated by rainfall seasonality. Leave-one-out cross-validation revealed that whether trait variation was better predicted by environmental predictors or trait-trait integration depended on the clade and trait in question. Legacy signals in trait-environment and trait-trait relationships were apparently lost during the earliest diversification of Pelargonium, but then retained during subsequent subclade evolution. Overall, we demonstrate that global-scale patterns are poor predictors of patterns of trait variation at finer geographic and taxonomic scales.

Hygroscopic movements in Geraniaceae: the structural variations that are responsible for coiling or bending.

The family Geraniaceae is characterized by a beak-like fruit, consisting of five seeds appended by a tapering awn. The awns exhibit coiling or bending hygroscopic movement as part of the seed dispersal strategy. Here we explain the variation in the hygroscopic reaction based on structural principles. We examined five representative species from three genera: Erodium, Geranium, and Pelargonium. Using X-ray diffraction, and electron and polarized light microscopy, we measured the cellulose microfibril angles in relation to the cell and cellulose helix axes. The behavior of separated single cells during dehydration was also examined. A bi-layered structure characterizes all the representative genera studied, with a hygroscopically contracting inner layer, and a stiff outer layer. We found that the cellulose arrangement in the inner layer is responsible for the type of awn deformation (coiling or bending). In three of the five awns examined, we identified an additional coiling outer sublayer, which adds coiling deformation to the awn. We divide the movements into three types: bending, coiling, and coiled-bending. All movement types are found in the Geranium genus. These characteristics are of importance for understanding the evolution of seed dispersal mechanisms in the Geraniaceae family.

Erodium maritimum (Geraniaceae), a species with an uneven and fragmented distribution along the Western Mediterranean and European Atlantic coasts, has a weak genetic structure.

Erodium maritimum L. is an annual species presenting heterogeneous, sometimes very small, and distant populations, distributed along a discontinuous coastal strip of the European Atlantic and the central and western Mediterranean basin. The aim of this study is to investigate genetic variation and geographic structure changes across its large distribution. Fourteen populations of E. maritimum were studied using AFLP fingerprints, together with their population sizes, reproductive systems and flower visitors. AFLP markers revealed the genetic structure of the species to be weak. Many individuals from one population clustered together with those of other populations, showing a high degree of genetic admixture. Despite having a self-compatible reproductive system, populations (especially the largest ones) showed high levels of genetic polymorphism, and the majority of genetic variation was contained within populations. The low genetic structure suggests high levels of gene flow, which might be explained through the dispersability of the species' fruits. Finally, recommendations are provided for management strategies to facilitate the conservation of this endangered species.

Niche opportunities and invasion dynamics in a desert annual community.

Although many factors influence the ability of exotics to invade successfully, most studies focus on only a few variables to explain invasion; attempts at theoretical synthesis are largely untested. The niche opportunities framework proposes that the demographic success of an invader is largely affected by the availability of resources and the abundance of its enemies. Here, we use a 31-year study from a desert ecosystem to examine the niche opportunities framework via the invasion of the annual plant Erodium cicutarium. While the invader remained rare for two decades, a decline in granivory combined with an ideal climate window created an opportunity for E. cicutarium to escape control and become the dominant annual plant in the community. We show that fluctuations in consumption and resources can create niche opportunities for invaders and highlight the need for additional long-term studies to track the influence of changing climate and community dynamics on invasions.

Quantifying how fine-grained environmental heterogeneity and genetic variation affect demography in an annual plant population.

The ability of plant species to colonize new habitats and persist in changing environments depends on their ability to respond plastically to environmental variation and on the presence of genetic variation, thus allowing adaptation to new conditions. For invasive species in particular, the relationship between phenotypic trait expression, demography, and the quantitative genetic variation that is available to respond to selection are likely to be important determinants of the successful establishment and persistence of populations. However, the magnitude and sources of individual demographic variation in exotic plant populations remain poorly understood. How important is plasticity versus adaptability in populations of invasive species? Among environmental factors, is temperature, soil nutrients, or competition most influential, and at what scales and life stages do they affect the plants? To investigate these questions we planted seeds of the exotic annual plant Erodium brachycarpum into typical pasture habitat in a spatially nested design. Seeds were drawn from 30 inbred lines to enable quantification of genetic effects. Despite a positive population growth rate, a few plants (0.1 %) produced >50 % of the seeds, suggesting a low effective population size. Emergence and early growth varied by genotype, but as in previous studies on native plants, environmental effects greatly exceeded genetic effects, and survival was unrelated to genotype. Environmental influences shifted from microscale soil compaction and litter depth at emergence through to larger-scale soil nutrient gradients during growth and to competition during later survival and seed production. Temperature had no effect. Most demographic rates were positively correlated, but emergence was negatively correlated with other rates.

Tilted cellulose arrangement as a novel mechanism for hygroscopic coiling in the stork's bill awn.

The sessile nature of plants demands the development of seed-dispersal mechanisms to establish new growing loci. Dispersal strategies of many species involve drying of the dispersal unit, which induces directed contraction and movement based on changing environmental humidity. The majority of researched hygroscopic dispersal mechanisms are based on a bilayered structure. Here, we investigate the motility of the stork's bill (Erodium) seeds that relies on the tightening and loosening of a helical awn to propel itself across the surface into a safe germination place. We show that this movement is based on a specialized single layer consisting of a mechanically uniform tissue. A cell wall structure with cellulose microfibrils arranged in an unusually tilted helix causes each cell to spiral. These cells generate a macroscopic coil by spiralling collectively. A simple model made from a thread embedded in an isotropic foam matrix shows that this cellulose arrangement is indeed sufficient to induce the spiralling of the cells.

Linking the spatial scale of environmental variation and the evolution of phenotypic plasticity: selection favors adaptive plasticity in fine-grained environments.

Adaptive phenotypic plasticity and adaptive genetic differentiation enable plant lineages to maximize their fitness in response to environmental heterogeneity. The spatial scale of environmental variation relative to the average dispersal distance of a species determines whether selection will favor plasticity, local adaptation, or an intermediate strategy. Habitats where the spatial scale of environmental variation is less than the dispersal distance of a species are fine grained and should favor the expression of adaptive plasticity, while coarse-grained habitats, where environmental variation occurs on spatial scales greater than dispersal, should favor adaptive genetic differentiation. However, there is relatively little information available characterizing the link between the spatial scale of environmental variation and patterns of selection on plasticity measured in the field. I examined patterns of spatial environmental variation within a serpentine mosaic grassland and selection on an annual plant (Erodium cicutarium) within that landscape. Results indicate that serpentine soil patches are a significantly finer-grained habitat than non-serpentine patches. Additionally, selection generally favored increased plasticity on serpentine soils and diminished plasticity on non-serpentine soils. This is the first empirical example of differential selection for phenotypic plasticity in the field as a result of strong differences in the grain of environmental heterogeneity within habitats.

The mechanics of explosive dispersal and self-burial in the seeds of the filaree, Erodium cicutarium (Geraniaceae).

The filaree (Erodium cicutarium), a small, flowering plant related to geraniums, possesses a unique seed dispersal mechanism: the plant can fling its seeds up to half a meter away; and the seeds can bury themselves by drilling into the ground, twisting and untwisting in response to changes in humidity. These feats are accomplished using awns, helical bristles of dead but hygroscopically active tissue attached to the seeds. Here, we describe the kinematics of explosive dispersal and self-burial based on detailed high-speed and time-lapse videos. We use these observations to develop a simple mechanical model that accounts for the coiling behavior of the awn and allows comparison of the strain energy stored in the awn with the kinetic energy at launch. The model is used to examine tradeoffs between dispersal distance and reliability of the dispersal mechanism. The mechanical model may help in understanding the invasive potential of this species and provides a framework for examining other evolutionary tradeoffs in seed dispersal mechanisms among the Geraniaceae.

Characterizing selection on phenotypic plasticity in response to natural environmental heterogeneity.

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal-scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full-sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full-sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes.

Identification and characterization of the water gap in physically dormant seeds of Geraniaceae, with special reference to Geranium carolinianum.

BACKGROUND AND AIMS: Physical dormancy in seeds of species of Geraniaceae is caused by a water-impermeable palisade layer in the outer integument of the seed coat and a closed chalaza. The chalazal cleft has been reported to be the water gap (i.e. location of initial water entry) in innately permeable seeds of Geraniaceae. The primary aim of this study was to re-evaluate the location of the water gap and to characterize its morphology and anatomy in physically dormant seeds of Geraniaceae, with particular reference to G. carolinianum. METHODS: Length, width, mass, anatomy and germination of two seed types (light brown and dark brown) of G. carolinianum were compared. Location, anatomy and morphology of the water gap were characterized using free-hand and microtome tissue sectioning, light microscopy, scanning electron microscopy, dye tracking, blocking and seed-burial experiments. KEY RESULTS: Treatment with dry heat caused a colour change in the palisade cells adjacent to the micropyle. When placed in water, the 'hinged valve' (blister) erupted at the site of the colour change, exposing the water gap. The morphology and anatomy in the water-gap region differs from those of the rest of the seed coat. the morphology of the seed coat of the water-gap region is similar in G. carolinianum, G. columbinum, G. molle and G. pusillum and differs from that of the closely related species Erodium cicutarium. CONCLUSIONS: Dislodgment of swollen 'hinged valve' palisade cells adjacent to the micropyle caused the water gap to open in physically dormant seeds of G. carolinianum, and it was clear that initial water uptake takes place through this gap and not via the chalazal opening as previously reported. This water gap ('hinged valve gap') differs from water gaps previously described for other families in morphology, anatomy and location in the seed coat.

Understanding the consequences of seed dispersal in a heterogeneous environment.

Plant distributions are in part determined by environmental heterogeneity on both large (landscape) and small (several meters) spatial scales. Plant populations can respond to environmental heterogeneity via genetic differentiation between large distinct patches, and via phenotypic plasticity in response to heterogeneity occurring at small scales relative to dispersal distance. As a result, the level of environmental heterogeneity experienced across generations, as determined by seed dispersal distance, may itself be under selection. Selection could act to increase or decrease seed dispersal distance, depending on patterns of heterogeneity in environmental quality with distance from a maternal home site. Serpentine soils, which impose harsh and variable abiotic stress on non-adapted plants, have been partially invaded by Erodium cicutarium in northern California, USA. Using nearby grassland sites characterized as either serpentine or non-serpentine, we collected seeds from dense patches of E. cicutarium on both soil types in spring 2004 and subsequently dispersed those seeds to one of four distances from their maternal home site (0, 0.5, 1, or 10 m). We examined distance-dependent patterns of variation in offspring lifetime fitness, conspecific density, soil availability, soil water content, and aboveground grass and forb biomass. ANOVA revealed a distinct fitness peak when seeds were dispersed 0.5 m from their maternal home site on serpentine patches. In non-serpentine patches, fitness was reduced only for seeds placed back into the maternal home site. Conspecific density was uniformly high within 1 m of a maternal home site on both soils, whereas soil water content and grass biomass were significantly heterogeneous among dispersal distances only on serpentine soils. Structural equation modeling and multigroup analysis revealed significantly stronger direct and indirect effects linking abiotic and biotic variation to offspring performance on serpentine soils than on non-serpentine soils, indicating the potential for soil-specific selection on seed dispersal distance in this invasive species.

Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions.

Angiosperm plastid genomes are generally conserved in gene content and order with rates of nucleotide substitutions for protein-coding genes lower than for nuclear protein-coding genes. A few groups have experienced genomic change, and extreme changes in gene content and order are found within the flowering plant family Geraniaceae. The complete plastid genome sequence of Pelargonium X hortorum (Geraniaceae) reveals the largest and most rearranged plastid genome identified to date. Highly elevated rates of sequence evolution in Geraniaceae mitochondrial genomes have been reported, but rates in Geraniaceae plastid genomes have not been characterized. Analysis of nucleotide substitution rates for 72 plastid genes for 47 angiosperm taxa, including nine Geraniaceae, show that values of dN are highly accelerated in ribosomal protein and RNA polymerase genes throughout the family. Furthermore, dN/dS is significantly elevated in the same two classes of plastid genes as well as in ATPase genes. A relatively high dN/dS ratio could be interpreted as evidence of two phenomena, namely positive or relaxed selection, neither of which is consistent with our current understanding of plastid genome evolution in photosynthetic plants. These analyses are the first to use protein-coding sequences from complete plastid genomes to characterize rates and patterns of sequence evolution for a broad sampling of photosynthetic angiosperms, and they reveal unprecedented accumulation of nucleotide substitutions in Geraniaceae. To explain these remarkable substitution patterns in the highly rearranged Geraniaceae plastid genomes, we propose a model of aberrant DNA repair coupled with altered gene expression.

The effect of mean and variance in resource supply on survival of annuals from Mediterranean and desert environments.

Resource availability is often characterized by mean annual amounts, while ignoring the spatial variation within habitats and the temporal variation within a year. Yet, temporal and spatial variation may be especially important for identifying the source of stress in low productivity environments such as deserts where resources are often pulsed and resource renewal events are separated by long periods of low resource availability. Therefore, the degree of stress will be determined in part by the length of time between recharge events. Here, we investigated the effect of timing and total amount of water application on two congeneric pairs, each with a population from a low (desert) and a high (Mediterranean) productivity habitat. As expected, highest survival and greatest growth were found at low or intermediate recharge intervals, and the magnitude of response to increases in total seasonal amounts was greater for Mediterranean species than desert species. The species that had greater survival switched in the hierarchy under high total water depending on interval length. These results demonstrate that temporal variation in resource availability can be as important as annual total amounts for plant performance and that response to temporal dynamics can vary between species. This has implications for community-level processes, as competitive hierarchies may switch based on resource dynamics rather than only total availability.