The radiation of nodulated Chamaecrista species from the rainforest into more diverse habitats has been accompanied by a reduction in growth form and a shift from fixation threads to symbiosomes.

All non-Mimosoid nodulated genera in the legume subfamily Caesalpinioideae confine their rhizobial symbionts within cell wall-bound 'fixation threads' (FTs). The exception is the large genus Chamaecrista in which shrubs and subshrubs house their rhizobial bacteroids more intimately within symbiosomes, whereas large trees have FTs. This study aimed to unravel the evolutionary relationships between Chamaecrista growth habit, habitat, nodule bacteroid type, and rhizobial genotype. The growth habit, bacteroid anatomy, and rhizobial symbionts of 30 nodulated Chamaecrista species native to different biomes in the Brazilian state of Bahia, a major centre of diversity for the genus, was plotted onto an ITS-trnL-F-derived phylogeny of Chamaecrista. The bacteroids from most of the Chamaecrista species examined were enclosed in symbiosomes (SYM-type nodules), but those in arborescent species in the section Apoucouita, at the base of the genus, were enclosed in cell wall material containing homogalacturonan (HG) and cellulose (FT-type nodules). Most symbionts were Bradyrhizobium genotypes grouped according to the growth habits of their hosts, but the tree, C. eitenorum, was nodulated by Paraburkholderia. Chamaecrista has a range of growth habits that allow it to occupy several different biomes and to co-evolve with a wide range of (mainly) bradyrhizobial symbionts. FTs represent a less intimate symbiosis linked with nodulation losses, so the evolution of SYM-type nodules by most Chamaecrista species may have (i) aided the genus-wide retention of nodulation, and (ii) assisted in its rapid speciation and radiation out of the rainforest into more diverse and challenging habitats.

Comparing the Predicted versus Realized Rate of Adaptation of Chamaecrista fasciculata to Climate Change.

AbstractFisher's fundamental theorem of natural selection (FTNS) can be used in a quantitative genetics framework to predict the rate of adaptation in populations. Here, we estimated the capacity for a wild population of the annual legume Chamaecrista fasciculata to adapt to future environments and compared predicted and realized rates of adaptation. We planted pedigreed seeds from one population into three prairie reconstructions along an east-to-west decreasing precipitation gradient. The FTNS predicted adaptation at all sites, but we found a response to selection that was smaller at the home and westernmost sites and maladaptive at the middle site because of changes in the selective environment between generations. However, mean fitness of the progeny generation at the home and westernmost sites exceeded population replacement, which suggests that the environment was sufficiently favorable to promote population persistence. More studies employing the FTNS are needed to clarify the degree to which predictions of the rate of adaptation are realized and its utility in the conservation of populations at risk of extinction from climate change.

Lifetime Fitness through Female and Male Function: Influences of Genetically Effective Population Size and Density.

AbstractAn individual's lifetime fitness and patterns of mating between individuals are interdependent features of sexual organisms. Mating systems (outcrossing vs. selfing or mating between close relatives) can affect the distribution of offspring fitness, which generally declines with inbreeding, which in turn is related to a population's genetically effective size (Ne). Fitness and mating patterns are also expected to vary with proximity of mates (i.e., population density). Consequently, density and Ne may influence demographic and genetic changes over generations and interact in their effects. Here, we report an experiment designed to assess the influence of these two population-level properties on mating system and lifetime fitness. In experimental arrays under quasi-natural conditions, we varied the density and Ne of the hermaphroditic annual legume Chamaecrista fasciculata. We recorded components of fitness for each individual and employed microsatellite markers to estimate outcrossing and assign paternity. We used aster analyses to estimate lifetime fitness for genetic families using female (seeds set) and male (seeds sired) reproduction as fitness measures. With estimates from these analyses, we assessed the evidence for a trade-off between fitness attained through female versus male function, but we found none. Lifetime fitness increased with density, especially under high Ne. Outcrossing rates increased with density under high Ne but declined modestly with density under low Ne. Our results show that density and Ne have strong direct effects on fitness and mating systems, with negative fitness effects of low Ne limiting the positive effects of increasing density. These findings highlight the importance of the interactive effects of density and Ne on lifetime fitness.

Detrimental effects of rhizobial inoculum early in the life of partridge pea, Chamaecrista fasciculata.

PREMISE OF THE STUDY: Mutualistic relationships with microbes may aid plants in overcoming environmental stressors and increase the range of abiotic environments where plants can persist. Rhizobia, nitrogen-fixing bacteria associated with legumes, often confer fitness benefits to their host plants by increasing access to nitrogen in nitrogen-limited soils, but effects of rhizobia on host fitness under other stresses, such as drought, remain unclear. METHODS: In this greenhouse study, we varied the application of rhizobia (Bradyrhizobium sp.) inoculum and drought to examine whether the fitness benefits of rhizobia to their host, partridge pea (Chamaecrista fasciculata), would differ between drought and well-watered conditions. Plants were harvested 9 weeks after seeds were sown. KEY RESULTS: Young C. fasciculata plants that had been inoculated had lower biomass, leaf relative growth rate, and stem relative growth rate compared to young uninoculated plants in both drought and well-watered environments. CONCLUSIONS: Under the conditions of this study, the rhizobial interaction imposed a net cost to their hosts early in development. Potential reasons for this cost include allocating more carbon to nodule and root development than to aboveground growth and a geographic mismatch between the source populations of host plants and rhizobia. If developing plants incur such costs from rhizobia in nature, they may suffer an early disadvantage relative to other plants, whether conspecifics lacking rhizobia or heterospecifics.

The success of assisted colonization and assisted gene flow depends on phenology.

Global warming will jeopardize the persistence and genetic diversity of many species. Assisted colonization, or the movement of species beyond their current range boundary, is a conservation strategy proposed for species with limited dispersal abilities or adaptive potential. However, species that rely on photoperiodic and thermal cues for development may experience conflicting signals if transported across latitudes. Relocating multiple, distinct populations may remedy this quandary by expanding genetic variation and promoting evolutionary responses in the receiving habitat--a strategy known as assisted gene flow. To better inform these policies, we planted seeds from latitudinally distinct populations of the annual legume, Chamaecrista fasciculata, in a potential future colonization site north of its current range boundary. Plants were exposed to ambient or elevated temperatures via infrared heating. We monitored several life history traits and estimated patterns of natural selection to determine the adaptive value of plastic responses. To assess the feasibility of assisted gene flow between phenologically distinct populations, we counted flowers each day and estimated the degree of temporal isolation between populations. Increased temperatures advanced each successive phenological trait more than the last, resulting in a compressed life cycle for all but the southern-most population. Warming altered patterns of selection on flowering onset and vegetative biomass. Population performance was dependent on latitude of origin, with the northern-most population performing best under ambient conditions and the southern-most performing most poorly, even under elevated temperatures. Among-population differences in flowering phenology limited the potential for genetic exchange among the northern- and southern-most populations. All plastic responses to warming were neutral or adaptive; however, photoperiodic constraints will likely necessitate evolutionary responses for long-term persistence, especially when involving populations from disparate latitudes. With strategic planning, our results suggest that assisted colonization and assisted gene flow may be feasible options for preservation.

Floral polymorphism in Chamaecrista flexuosa (Fabaceae-Caesalpinioideae): a possible case of atypical enantiostyly?

BACKGROUND AND AIMS: Reciprocal herkogamy, including enantiostyly and heterostyly, involves reciprocity in the relative positions of the sexual elements within the flower. Such systems result in morphologically and, since pollen is deposited on and captured from different parts of the pollinator, functionally distinct floral forms. Deviations from the basic pattern may modify the functionality of these mechanisms. For heterostylous species, such deviations are generally related to environmental disturbances, pollination services and/or reduced numbers of one floral morph. Deviations for enantiostylous species have not yet been reported. This study aims to investigate enantiostyly in Chamaecrista flexuosa, in particular the presence of deviations from the standard form, in an area of coastal vegetation in north-east Brazil. METHODS: Observations and investigations of floral biology, the reproductive system, pollinator behaviour, floral morphology and morphometry were performed. KEY RESULTS: In C. flexuosa flowers, anthers of different size but similar function are grouped. The flowers were self-compatible and set fruits after every treatment, except in the spontaneous self-pollination experiment, thereby indicating their dependence on pollen vectors. The flowers were pollinated by bees, especially Xylocopa cearensis and X. grisencens. Pollen is deposited and captured from the ventral portion of the pollinator's body. Variations in the spatial arrangement of floral elements allowed for the identification of floral morphs based on both morphological and functional criteria. Using morphological criteria, morphologically right (MR) and morphologically left (ML) floral morphs were identified. Three floral morphs were identified using functional criteria: functionally right (FR), functionally central (FC) and functionally left (FL). Combinations of morphologically and functionally defined morphs did not occur in equal proportions. There was a reduced frequency of the MR-FR combination. CONCLUSIONS: The results indicate the occurrence of an atypical enantiostyly in C. flexuosa. This seems to improve reproductive success by increasing the efficiency of pollen deposition and capture.

Extensive variation in cadmium tolerance and accumulation among populations of Chamaecrista fasciculata.

Plant populations may vary substantially in their tolerance for and accumulation of heavy metals, and assessment of this variability is important when selecting species to use in restoration or phytoremediation projects. We examined the population variation in cadmium tolerance and accumulation in a leguminous pioneer species native to the eastern United States, the partridge pea (Chamaecrista fasciculata). We assayed growth, reproduction and patterns of cadmium accumulation in six populations of C. fasciculata grown on a range of cadmium-contaminated soils. In general, C. fasciculata exhibited tolerance in low to moderate soil cadmium concentrations. Both tolerance and accumulation patterns varied across populations. C. fasciculata exhibited many characteristics of a hyperaccumulator species, with high cadmium uptake in shoots and roots. However, cadmium was excluded from extrafloral nectar. As a legume with tolerance for moderate cadmium contamination, C. fasciculata has potential for phytoremediation. However, our findings also indicate the importance of considering the effects of genetic variation on plant performance when screening plant populations for utilization in remediation and restoration activities. Also, there is potential for cadmium contamination to affect other species through contamination of leaves, fruits, flowers, pollen and root nodules.

Role of climate and competitors in limiting fitness across range edges of an annual plant.

It is often assumed that the geographic distributions of species match their climatic tolerances, but this assumption is not frequently tested. Moreover, few studies examine the relative importance of abiotic and biotic factors for limiting species ranges. We combined multiple approaches to assess the extent to which fitness of a widespread native annual legume, Chamaecrista fasciculata, decreases at and beyond its northern and western range edges, and how this is influenced by the presence of neighbors. First, we examined plant fitness and the effect of neighbors in natural populations at different geographic range locations for three years. Fitness decreased toward the northern range edge, but not the western edge. Neighbor removal had a consistently positive effect on seedpod production across all years and sites. Second, we established experimental populations at sites within the range, and at and beyond the northern and western range edges. We tracked individual fitness and recorded seedling recruitment in the following year (a complete generation) to estimate population growth rate. Individual fitness and population growth declined to near zero beyond both range edges, indicating that C. fasciculata with its present genetic composition will not establish in these regions, given conditions currently. We also carried out a neighbor removal treatment. Consistent with the natural populations, neighbors reduced seedpod production of reproductive adults. However, neighbors also increased early-season survival, and this positive effect early in life history resulted in a net positive effect of neighbors on lifetime fitness at most range locations. Our data show that the population growth rate of C. fasciculata includes values above replacement, and populations are well adapted to conditions up to the edge of the range, whereas the severely compromised fitness at sites beyond the edge precludes immediate establishment of populations and thereby impedes adaptation to these conditions.

Interactions between soil habitat and geographic range location affect plant fitness.

Populations are often found on different habitats at different geographic locations. This habitat shift may be due to biased dispersal, physiological tolerances or biotic interactions. To explore how fitness of the native plant Chamaecrista fasciculata depends on habitat within, at and beyond its range edge, we planted seeds from five populations in two soil substrates at these geographic locations. We found that with reduced competition, lifetime fitness was always greater or equivalent in one habitat type, loam soils, though early-season survival was greater on sand soils. At the range edge, natural populations are typically found on sand soil habitats, which are also less competitive environments. Early-season survival and fitness differed among source populations, and when transplanted beyond the range edge, range edge populations had greater fitness than interior populations. Our results indicate that even when the optimal soil substrate for a species does not change with geographic range location, the realized niche of a species may be restricted to sub-optimal habitats at the range edge because of the combined effects of differences in abiotic and biotic effects (e.g. competitors) between substrates.

Population variation in plant traits associated with ant attraction and herbivory in Chamaecrista fasciculata (Fabaceae).

The benefits of ant-plant-herbivore interactions for the plant depend on the abundance of ants and herbivores and the selective pressures these arthropods exert. In plants bearing extrafloral nectaries (EFN), different mean trait values may be selected for by different populations in response to local herbivore pressure, ultimately resulting in the evolution of differences in plant traits that attract ants as defensive agents against herbivory. To determine if variation in traits that mediate ant-plant interactions reflect herbivore selective pressures, we quantified intra- and inter-population variation in plant traits for eight populations of the EFN-bearing annual Chamaecrista fasciculata (Michx.) (Fabaceae). Censuses in rural and urban areas of Missouri and Illinois (USA) showed population differences in ant attendance and herbivore pressure. Seeds were collected from each population, and plants were grown in a common greenhouse environment to measure sugar production, nectar volume and composition, EFN size and time of emergence, leaf pubescence, and leaf quality throughout plant development. Populations varied mainly in terms of nectary size, sugar production, and nectar volume, but to a lesser degree in leaf pubescence. Populations of C. fasciculata within urban areas (low in insect abundance) had small nectaries and the lowest nectar production. There was a positive correlation across populations between herbivore density and leaf damage by those herbivores on the one hand and sugar production and nectar volume on the other. These results, in conjunction with lack of evidence for maternally based environmental effects, suggest that population differences in herbivore damage have promoted differential evolution of EFN-related traits among populations.

Test of local adaptation to biotic interactions and soil abiotic conditions in the ant-tended Chamaecrista fasciculata (Fabaceae).

Few previous studies have assessed the role of herbivores and the third trophic level in the evolution of local adaptation in plants. The overall objectives of this study were to determine (1) whether local adaptation is present in the ant-defended plant, Chamaecrista fasciculata, and (2) the contribution of ant-plant-herbivore interactions and soil source to such adaptation. We used three C. fasciculata populations and performed both a field and a greenhouse experiment. The first involved reciprocally transplanting C. fasciculata seedlings from each population-source to each site, and subsequently applying one of three treatments to one-third of the seedlings of each population-source at each site: control, reduced ant density and reduced folivory. The greenhouse experiment involved reciprocal transplants of population-sources with soil sources to test for a soil-source effect on flower production and local adaptation to soil conditions. Field results showed that ant and herbivore treatments reduced ant density (increasing folivory) and herbivore damage relative to controls, respectively; however, these manipulations did not impact C. fasciculata reproduction or the likelihood of survival. In contrast, greenhouse results showed that soil source significantly affected flower production. Overall, plants in both experiments, regardless of population-source, always had higher reproductive output at one specific site. Native populations did not outperform nonnative ones, causing us to reject the hypothesis of local adaptation. The absence of treatment effects on plant reproduction and the likelihood of survival suggest a limited effect of ants and folivores on C. fasciculata fitness and local adaptation during the study year. Temporally inconsistent effects of biotic forces across years, coupled with the young age of populations, relative proximity of populations and possible counter effects of seed predators may reduce the likelihood of local adaptation in the populations studied.

Post-zygotic reproductive isolation between sympatric taxa in the Chamaecrista desvauxii complex (Leguminosae-Caesalpinioideae).

BACKGROUND AND AIMS: Differences in the mating systems and the mechanisms of reproductive isolation between Chamaecrista desvauxii var. graminea and C. desvauxii var. latistipula were examined in the Chapada Diamantina, Brazil. These taxa occur sympatrically, and their populations demonstrate marked morphological differences. The objective of the present work was to determine if reproductive isolation mechanisms exist between these two populations of C. desvauxii, and to determine the influence of these putative mechanisms on their genetic differentiation. METHODS: Field observations were made of floral biology, phenology and floral visitation, and experiments on intra- and interpopulation pollination and germination rates of the resultant seeds were performed. A genetic examination of the populations was undertaken using four allozyme loci. KEY RESULTS: The varieties examined demonstrated overlapping of flowering periods during the months of June to September. The main pollinator for both varieties was the bee Bombus brevivillus. Both varieties are self-compatible, and a large number of fruits are formed in cross-pollinations with high seed germination rates. Inter-taxa pollinations result in high levels of fruit production, but no seeds are formed. Two of the four loci examined were diagnostic for the varieties, and exclusive high-frequency alleles were encountered at the other loci, leading to a high genetic distance between the two populations (0.495). CONCLUSIONS: Pre-zygotic barriers were not found between the two varieties, and these remain isolated due to post-zygotic events. The two varieties demonstrate marked differences in their morphology, floral biology, phenology and genetic make-up, all of which indicate that they should be treated as two distinct species. A complete revision involving the other varieties of the C. desvauxii complex will be necessary in order to define these two taxa formally.

Intraspecific hybridization and the recovery of fitness in the native legume Chamaecrista fasciculata.

Genetic incompatibilities and low offspring fitness are characteristic outcomes of hybridization between species. Yet, the creative potential of recombination following hybridization continues to be debated. Here we quantify the outcome of hybridization and recombination between adaptively divergent populations of the North American legume Chamaecrista fasciculata in a large-scale field experiment. Previously, hybrids between these populations demonstrated hybrid breakdown, suggesting the expression of adaptive epistatic interactions underlying population genetic differentiation. However, the outcome of hybridization ultimately rests on the performance of even later generation recombinants. In experiments that compared the performance of recombinant F6 and F2 generations with nonrecombinant F1 and parental genotypes, we observed that increasing recombination had contrasting effects on different life-history components. Lifetime fitness, defined as the product of survivorship and reproduction, showed a strong recovery of fitness in the F6. The overall gain in fitness with increased recombination suggests that hybridization and recombination may provide the necessary genetic variation for adaptive evolution within species. We discuss the mechanisms that may account for the gain in fitness with recombination, and explore the implications for hybrid speciation and phenotypic evolution.

Evolutionary potential of Chamaecrista fasciculata in relation to climate change. I. Clinal patterns of selection along an environmental gradient in the great plains.

Climate change will alter natural selection on native plant populations. Little information is available to predict how selection will change in the future and how populations will respond. Insight can be obtained by comparing selection regimes in current environments to selection regimes in environments similar to those predicted for the future. To mimic predicted temporal change in climate, three natural populations of the annual legume Chamaecrista fasciculata were sampled from a climate gradient in the Great Plains and progeny of formal crosses were reciprocally planted back into common gardens across this climate gradient. In each garden, native populations produced significantly more seed than the other populations, providing strong evidence of local adaptation. Phenotypic selection analysis conducted by site showed that plants with slower reproductive development, more leaves, and thicker leaves were favored in the most southern garden. Evidence of clinal variation in selection regimes was also found; selection coefficients were ordered according to the latitude of the common gardens. The adaptive value of native traits was indicated by selection toward the mean of local populations. Repeated clinal patterns in linear and nonlinear selection coefficients among populations and within and between sites were found. To the extent that temporal change in climate into the future will parallel the differences in selection across this spatial gradient, this study suggests that selection regimes will be displaced northward and different trait values will be favored in natural populations.

Evolutionary potential of Chamaecrista fasciculata in relation to climate change. II. Genetic architecture of three populations reciprocally planted along an environmental gradient in the great plains.

Climate change will test the evolutionary potential of populations. Information regarding the genetic architecture within and among populations is essential for prediction of evolutionary outcomes. However, little is known about the distribution of genetic variation for relevant traits in natural populations or alteration of genetic architecture in a changing environment. In this study, pedigreed families from three populations of the annual prairie legume Chamaecrista fasciculata were reciprocally transplanted in three environments across a broad latitudinal range in the Great Plains. The underlying premise of this work is that northern populations will in the future experience climates similar to current-day climates further south. Estimates of narrow-sense heritability ranged from 0.053 to 0.481, suggesting the potential for evolutionary change is possible for most traits. In general, the northern population harbored less genetic variation and had lower heritability for traits than the southern population. This population also experienced large reductions in fitness, as measured by estimated lifetime fecundity, when raised in either the intermediate or the southern climate, whereas the difference between the intermediate and southern population was less extreme. For fecundity, the pattern of cross-environment additive genetic correlations was antagonistic to evolutionary change in four of six cases when native and nonnative sites were compared. Six additional antagonistic positive correlations were found for the rate of phenological development and leaf thickness. Overall, the data suggest that if climate changes as predicted, the northern population will face a severe evolutionary challenge in the future because of low heritabilities, cross-environment genetic correlations antagonistic to selection, and demographic instability due to lower seed production in a hotter and drier climate.