Nuclear and cytoplasmic contributions to intraspecific divergence in an annual legume.

The genetic architecture of trait differentiation was evaluated between two ecologically distinct populations of Chamaecrista fasciculata. Individuals from Maryland and Illinois populations were crossed to create 10 types of seed: Maryland and Illinois parents, reciprocal F1 and F2 hybrids, and backcrosses to Maryland and to Illinois on reciprocal F1 hybrids. Reciprocal crosses created hybrid generation seeds with both Maryland and Illinois cytoplasmic backgrounds. Experimental individuals were grown in a common garden near the site of the Maryland population. In the garden, plants from the Illinois population flowered, set fruit, and died earlier than those from Maryland, likely reflecting adaptations to differences in growing season length between the two populations. Although reproductive components at the flower and whole plant level differed between the two populations, reproductive output as measured by fruit and seed production was similar. Cytoplasmic genes had a subtle but pervasive effect on population differentiation; hybrids with Maryland cytoplasm were significantly differentiated from those with Illinois cytoplasm when all characters were evaluated jointly. The nuclear genetic architecture of population differentiation was evaluated with joint scaling tests. Depending on the trait, both additive and nonadditive genetic effects contributed to population differentiation. Intraspecific genetic differentiation in this wild plant species appears to reflect a complex genetic architecture that includes the contribution of additive, dominance, and epistatic components in addition to subtle cytoplasmic effects.

The role of breeding system and inbreeding depression in the maintenance of an outcrossing mating strategy in Silene virginica (Caryophyllaceae).

The goal of this study was to understand the interaction among breeding system, mating system, and expression of inbreeding depression in the hermaphroditic, primarily hummingbird-pollinated, iteroparous, short-lived perennial Silene virginica. We performed hand-selfed and hand-outcrossed pollinations in the field, conducted detailed floral observations within individual flowers and plants, and assayed adult tissue from flowering plants for a genetic estimate of population outcrossing rate. We quantified the opportunity for geitonogamy as the proportion of days each plant exhibited simultaneous male and female function, i.e., asynchronous expression of male- and female-phased flowers. Expression of cumulative inbreeding depression based on germination rate and total flower production in the glasshouse was ∼40% and was congruent with the estimated high outcrossing rate of 0.89. Floral observations demonstrated strong temporal protandry within each flower (dichogamy) as well as complete spatial separation between male and female function within each flower (herkogamy). On average, 29% of the time there were both male- and female-phased flowers present on an individual plant. We conclude that our estimate of inbreeding depression is compatible with a largely outcrossing mating system and the amount of selfing observed, likely results from geitonogamy. This study illustrates the utility of examining both the causes and the consequences of inbreeding via selfing to provide additional insights into the evolution of plant mating systems.

Population differentiation in an annual legume: genetic architecture.

The presence or absence of epistasis, or gene interaction, is explicitly assumed in many evolutionary models. Although many empirical studies have documented a role of epistasis in population divergence under laboratory conditions, there have been very few attempts at quantifying epistasis in the native environment where natural selection is expected to act. In addition, we have little understanding of the frequency with which epistasis contributes to the evolution of natural populations. In this study we used a quantitative genetic design to quantify the contribution of epistasis to population divergence for fitness components of a native annual legume, Chamaecrista fasciculata. The design incorporated the contrast of performance of F2 and F3 segregating progeny of 18 interpopulation crosses with the F1 and their parents. Crosses were conducted between populations from 100 m to 2000 km apart. All generations were grown for two seasons in the natural environment of one of the parents. The F1 often outperformed the parents. This F1 heterosis reveals population structure and suggests that drift is a major contributor to population differentiation. The F2 generation demonstrated that combining genes from different populations can sometimes have unexpected positive effects. However, the F3 performance indicated that combining genes from different populations decreased vigor beyond that due to the expected loss of heterozygosity. Combined with previous data, our results suggest that both selection and drift contribute to population differentiation that is based on epistatic genetic divergence. Because only the F3 consistently expressed hybrid breakdown, we conclude that the epistasis documented in our study reflects interactions among linked loci.

Population differentiation in an annual legume: local adaptation.

Studies of many plants species have demonstrated adaptive genetic differentiation to local environmental conditions. Typically these studies are conducted to evaluate adaptation to contrasting environments. As a consequence, although local adaptation has been frequently demonstrated, we have little information as to the spatial scale of adaptive evolution. We evaluated adaptive differentiation between populations of the annual legume Chamaecrista fasciculata using a replicated common-garden design. Study sites were established in three field locations that are home to native populations of C. fasciculata. Each location was planted for two years with seed from the population native to the study site (home population) and populations located six distances (0.1-2000 km) from each site (transplanted populations). Seeds were planted into the study sites with minimum disturbance to determine the scale of local adaptation, as measured by a home-site fitness advantage, for five fitness components: germination, survival, vegetative biomass, fruit production, and the number of fruit produced per seed planted (an estimate of cumulative fitness). For all characters there was little evidence for local adaptation, except at the furthest spatial scales. Patterns of adaptive differentiation were fairly consistent in two of the three sites, but varied between years. Little genetic variation was expressed at the third site. These results, combined with previous estimates of limited gene flow, suggest that metapopulation processes and temporal environmental variation act together to reduce local adaptation, except over long distances.

Ecological and genetic factors contributing to the low frequency of male sterility in Chamaecrista Fasciculata (Fabaceae).

Bumble bee pollinated Chamaecrista fasciculata provides pollen as the sole reward to its pollinators. Male sterility, expressed as an absence or nearly complete absence of pollen production, occurs in low frequency in populations of C. fasciculata. Here we describe experiments, using C. fasciculata, to examine frequently cited determinants of the spread and maintenance of male sterility: compensation and the genetic basis of male sterility. In addition, we examine the role the pollination system plays in determining the reproductive success of the male steriles. Seventeen populations in Maryland, Illinois, and Kansas were surveyed and found to range from 0 to 6% male sterility per population. An artificial population of male-sterile simulants and hermaphrodites was created to examine how the local frequency of nonrewarding male steriles might affect male-sterile female reproductive success. Male steriles performed equally poorly, with respect to seed production, whether surrounded by other male-sterile simulants or hermaphrodites. Compensation was examined by comparison of male steriles and hermaphrodites with respect to several reproductive and nonreproductive characters. Male steriles outperformed hermaphrodites in terms of nonreproductive biomass, but performed equally in terms of ovule number and produced many fewer flowers. The genetic basis of male sterility was examined by performing both intra- and interpopulational crosses of male steriles to hermaphrodites and indicate that male sterility is not purely cytoplasmic. The low frequency of male sterility in C. fasciculata populations may reflect reduced female reproductive success because of pollinator avoidance, lack of reproductive compensation, and a mode of inheritance that is not purely cytoplasmic.

Epistasis and its consequences for the evolution of natural populations.

Throughout the neodarwinian synthesis, theorists have debated the role of gene interactions, or epistasis, in the evolutionary process. Unfortunately, empirical measurement of the role of epistasis in the evolution of natural populations has, until now, been difficult. Two developments in empirical approaches have occurred: (1) application of theory to the evolution of natural populations, and (2) the concurrent development of molecular marker-assisted techniques to understand the architecture of quantitative genetic variation. Thus, exciting developments in both theory and empirical data collection provide the stimulus for documenting the role of epistasis in the evolutionary process.