Plants exhibit adaptive responses to light, but it is not known whether parental plants transmit environmental cues that elicit adaptive responses in offspring. We show that offspring life history (annual versus biennial) is influenced by the maternal light environment (understory versus light gap). This transgenerational plasticity is adaptive when offspring are grown in their maternal light environment, where seeds typically disperse. Projections of population growth show that plants that are appropriately cued for their light environment through maternal effects have 3.4 times greater fitness than otherwise. Transgenerational plasticity has evolved in response to natural variation in light and provides a flexible mechanism by which sedentary organisms cope with heterogeneous environments.
SummaryIn outcrossing plants, seed dispersal distance is often less than pollen movement. If the scale of environmental heterogeneity within a population is greater than typical seed dispersal distances but less than pollen movement, an individual's environment will be similar to that of its mother but not necessarily its father. Under these conditions, environmental maternal effects may evolve as a source of adaptive plasticity between generations, enhancing offspring fitness in the environment that they are likely to experience. This idea is illustrated using Campanula americana , an herb that grows in understory and light-gap habitats. Estimates of seed dispersal suggest that offspring typically experience the same light environment as their mother. In a field experiment testing the effect of open vs understory maternal light environments, maternal light directly influenced offspring germination rate and season, and indirectly affected germination season by altering maternal flowering time. Results to date indicate that these maternal effects are adaptive; further experimental tests are ongoing. Evaluating maternal environmental effects in an ecological context demonstrates that they may provide phenotypic adaptation to local environmental conditions. New Phytologist (2005) 166 : 93-100 © New Phytologist (2005)
Abstract. 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.
The deleterious consequences of inbreeding have been well documented. There are, however, few empirical studies that have examined the consequences of restoring heterozygosity and hence the fitness of inbred populations by conducting interpopulation crosses and measuring the performance of later‐generation hybrids under field conditions. We conducted interpopulation crosses of 100 m to 2000 km, which spans the range of Chamaecrista fasciculata ( Fabaceae) in eastern North America. We then contrasted the performance of the F1 and later‐segregating F3 hybrids with the parental generation. We found almost universal F1 superiority over the parents. The F3 hybrids suffered a loss of fitness compared to the F1 hybrids. The drop off in fitness of the F3 reflects both the loss of heterozygosity and the disruption of coadapted gene complexes. The F3 performance, however, was still often equal to that of the parents, suggesting that heterosis can outweigh the loss of coadaptation except for the longest‐distance crosses. In a subset of environments, the F3 performance of long‐distance (≥1000 km) interpopulation crosses was less than that of both parents and indicated true outbreeding depression. For C. fasciculata, it appears that crossing populations of up to intermediate distances of hundreds of kilometers has a short‐term beneficial effect on progeny performance through F1, and that longer‐term effects are not necessarily disruptive of fitness, at least relative to parental performance. The degree of F1 heterosis and F3 outbreeding depression varied between site and year, however, indicating an important role for the environment in the expression of these effects.
Maternal environments typically influence the phenotype of their offspring. However, the effect of the paternal environment or the potential for joint effects of both parental environments on offspring characters is poorly understood. Two populations of Campanula americana, a woodland herb with a variable life history, were used to determine the influence of maternal and paternal light and nutrient environments on offspring seed characters. Families were grown in the greenhouse in three levels of light or three levels of nutrients. Crosses were conducted within each environmental gradient to produce seeds with all combinations of maternal and paternal environments. On average, increasing maternal nutrient and light levels increased seed mass and decreased percentage germination. The paternal environment affected seed mass, germination time, and percentage germination. However, the influence of the paternal environment varied across maternal environments, suggesting that paternal environmental effects should be evaluated in the context of maternal environments. Significant interactions between family and the parental environments for offspring characters suggest that parental environmental effects are genetically variable. In C. americana, the timing of germination determines life history. Therefore parental environmental effects on germination timing, and genetic variation in those parental effects, suggest that parental environments may influence life history evolution in this system.
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 F 2 and F 3 segregating progeny of 18 interpopulation crosses with the F 1 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 F 1 often outperformed the parents. This F 1 heterosis reveals population structure and suggests that drift is a major contributor to population differentiation. The F 2 generation demonstrated that combining genes from different populations can sometimes have unexpected positive effects. However, the F 3 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 F 3 consistently expressed hybrid breakdown, we conclude that the epistasis documented in our study reflects interactions among linked loci.
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