Lisa A. Dorn

Plasticity to light cues and resources in Arabidopsis thaliana: testing for adaptive value and costs.

Plants shaded by neighbors or overhead foliage experience both a reduction in the ratio of red to far red light (R:FR), a specific cue perceived by phytochrome, and reduced photosynthetically active radiation (PAR), an essential resource. We tested the adaptive value of plasticity to crowding and to the cue and resource components of foliage shade in the annual plant Arabidopsis thaliana by exposing 36 inbred families from four natural populations to four experimental treatments: (1) high density, full sun; (2) low density, full sun; (3) low density, neutral shade; and (4) low density, low R:FR‐simulated foliage shade. Genotypic selection analysis within each treatment revealed strong environmental differences in selection on plastic life‐history traits. We used specific contrasts to measure plasticity to density and foliage shade, to partition responses to foliage shade into phytochrome‐mediated responses to the R:FR cue and responses to PAR, and to test whether plasticity was adaptive (i.e., in the same direction as selection in each environment). Contrary to expectation, we found no evidence for adaptive plasticity to density. However, we observed both adaptive and maladaptive responses to foliage shade. In general, phytochrome‐mediated plasticity to the R:FR cue of foliage shade was adaptive and counteracted maladaptive growth responses to reduced PAR. These results support the prediction that active developmental responses to environmental cues are more likely to be adaptive than are passive resource‐mediated responses. Multiple regression analysis detected a few costs of adaptive plasticity and adaptive homeostasis, but such costs were infrequent and their expression depended on the environment. Thus, costs of plasticity may occasionally constrain the evolution of adaptive responses to foliage shade in Arabidopsis, but this constraint may differ among environments and is far from ubiquitous.

THE EVOLUTIONARY ECOLOGY OF SEED GERMINATION OF ARABIDOPSIS THALIANA: VARIABLE NATURAL SELECTION ON GERMINATION TIMING

Abstract Germination timing of Arabidopsis thaliana displays strong plasticity to geographic location and seasonal conditions experienced by seeds. We identified which plastic responses were adaptive using recombinant inbred lines in a field manipulation of geographic location (Kentucky, KY; Rhode Island, RI), maternal photoperiod (14‐h and 10‐ h days), and season of dispersal (June and November). Transgressive segregation created novel genotypes that had either higher fitness or lower fitness in certain environments than either parent. Natural selection on germination timing and its variation explained 72% of the variance in fitness among genotypes in KY, 30% in June‐dispersed seeds in RI, but only 4% in November‐dispersed seeds in RI. Therefore, natural selection on germination timing is an extremely efficient sieve that can determine which genotypes can persist in some locations, and its efficiency is geographically variable and depends on other aspects of life history. We found no evidence for adaptive responses to maternal photoperiod during seed maturation. We did find adaptive plasticity to season of seed dispersal in RI. Seeds dispersed in June postponed germination, which was adaptive, while seeds dispersed in November accelerated germination, which was also adaptive. We also found maladaptive plasticity to geographic location for seeds dispersed in June, such that seeds dispersed in KY germinated much sooner than the optimum time. Consequently, bet hedging in germination timing was favorable in KY; genotypes with more variation in germination timing had higher fitness because greater variation was associated with postponed germination. Selection on germination timing varied across geographic location, indicating that germination timing can be a critical stage in the establishment of genotypes in new locations. The rate of evolution of germination timing may therefore strongly influence the rate at which species can expand their range.

ENVIRONMENTAL AND GENETIC INFLUENCES ON THE GERMINATION OF ARABIDOPSIS THALIANA IN THE FIELD

Abstract Seasonal germination timing strongly influences lifetime fitness and can affect the ability of plant populations to colonize and persist in new environments. To quantify the influence of seasonal environmental factors on germination and to test whether pleiotropy or close linkage are significant constraints on the evolution of germination in different seasonal conditions, we dispersed novel recombinant genotypes of Arabidopsis thaliana into two geographic locations. To decouple the photoperiod during seed maturation from the postdispersal season that maternal photoperiod predicts, replicates of recombinant inbred lines were grown under short days and long days under controlled conditions, and their seeds were dispersed during June in Kentucky (KY) and during June and November in Rhode Island (RI). We found that postdispersal seasonal conditions influenced germination more strongly than did the photoperiod during seed maturation. Genetic variation was detected for germination responses to all environmental factors. Transgressive segregation created novel germination phenotypes, revealing a potential contribution of hybridization of ecotypes to the evolution of germination. A genetic trade‐off in germination percentage across sites indicated that determinants of fitness at or before the germination stage may constrain the geographic range that a given genotype can inhabit. However, germination timing exhibited only weak pleiotropy across treatments, suggesting that different sets of genes contribute to variation in germination behavior in different seasonal conditions and geographic locations. Thus, the genetic potential exists for rapid evolution of appropriate germination responses in novel environments, facilitating colonization across a broad geographic range.

The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy

Colonizing species may often encounter strong selection during the initial stages of adaptation to novel environments. Such selection is particularly likely to act on traits expressed early in development since early survival is necessary for the expression of adaptive phenotypes later in life. Genetic studies of fitness under field conditions, however, seldom include the earliest developmental stages. Using a new set of recombinant inbred lines, we present a study of the genetic basis of fitness variation in Arabidopsis thaliana in which genotypes, environments, and geographic location were manipulated to study total lifetime fitness, beginning with the seed stage. Large‐effect quantitative trait loci (QTLs) for fitness changed allele frequency and closely approached 90% in some treatments within a single generation. These QTLs colocated with QTLs for germination phenology when seeds were dispersed following a schedule of a typical winter annual, and they were detected in two geographic locations at different latitudes. Epistatically interacting loci affected both fitness and germination in many cases. QTLs for field germination phenology colocated with known QTLs for primary dormancy induction as assessed in laboratory tests, including the candidate genes DOG1 and DOG6. Therefore fitness, germination phenology, and primary dormancy are genetically associated at the level of specific chromosomal regions and candidate loci. Genes associated with the ability to arrest development at early life stages and assess environmental conditions are thereby likely targets of intense natural selection early in the colonization process.

The effect of maternal photoperiod on seasonal dormancy in Arabidopsis thaliana (Brassicaceae)

The maternal photoperiod at the time of seed maturation can predict the seasonal conditions of newly dispersed seeds. We investigated the effects of maternal photoperiod on seasonal dormancy in Arabidopsis thaliana using a set of F6 recombinant inbred lines derived from a cross between individuals from two natural populations (Cal-0 and Tac-0) differing in cold requirements for germination. We grew 40 Cal × Tac lines in a long-day photoperiod (8 h of full spectrum light plus 8 h of low-fluence incandescent light) and a short-day photoperiod (8 h full spectrum light). We then exposed seeds from each family and maternal photoperiod to either a cold stratification treatment (4°C, 21 d) or no cold stratification. Both maternal photoperiod and progeny stratification influenced the percentage of seeds that germinated and the speed of germination. The short-day photoperiod caused increased responsiveness to stratification, with higher germination percentages and speeds in stratified seeds. Stratification influenced the expression of maternal photoperiod effects, such that short days increased germination percentage and speed in stratified seeds but inhibited germination in unstratified seeds. Families differed significantly in their plasticity to maternal photoperiod and stratification, but genetic variation for plasticity to maternal photoperiod was expressed only in unstratified seeds. Because the expression of maternal photoperiod effects and genetic variation for photoperiod effects depended on progeny stratification, the evolution of these maternal effects will depend on the seasonal environment experienced by progeny.

NICHE CONSTRUCTION THROUGH GERMINATION CUEING: LIFE-HISTORY RESPONSES TO TIMING OF GERMINATION IN ARABIDOPSIS THALIANA

Abstract Germination responses to seasonal conditions determine the environment experienced by postgermination life stages, and this ability has potential consequences for the evolution of plant life histories. Using recombinant inbred lines of Arabidopsis thaliana, we tested whether life‐history characters exhibited plasticity to germination timing, whether germination timing influenced the strength and mode of natural selection on life‐history traits, and whether germination timing influenced the expression of genetic variation for life‐history traits. Adult life‐history traits exhibited strong plasticity to season of germination, and season of germination significantly altered the strength, mode, and even direction of selection on life‐history traits under some conditions. None of the average plastic responses to season of germination or season of dispersal were adaptive, although some genotypes within our sample did exhibit adaptive responses. Thus, recombination between inbred lineages created some novel adaptive genotypes with improved responses to the seasonal timing of germination under some, but not all, conditions. Genetically based variation in germination time tended to augment genetic variances of adult life‐history traits, but it did not increase the heritabilities because it also increased environmentally induced variance. Under some conditions, plasticity of life‐history traits in response to genetically variable germination timing actually obscured genetic variation for those traits. Therefore, the evolution of germination responses can influence the evolution of life histories in a general manner by altering natural selection on life‐history traits and the genetic variation of these traits.

REDUCING ENVIRONMENTAL BIAS WHEN MEASURING NATURAL SELECTION

Abstract.— Crucial to understanding the process of natural selection is characterizing phenotypic selection. Measures of phenotypic selection can be biased by environmental variation among individuals that causes a spurious correlation between a trait and fitness. One solution is analyzing genotypic data, rather than phenotypic data. Genotypic data, however, are difficult to gather, can be gathered from few species, and typically have low statistical power. Environmental correlations may act through traits other than through fitness itself. A path analytic framework, which includes measures of such traits, may reduce environmental bias in estimates of selection coefficients. We tested the efficacy of path analysis to reduce bias by re‐analyzing three experiments where both phenotypic and genotypic data were available. All three consisted of plant species (Impatiens capensis, Arabidopsis thaliana, and Raphanus sativus) grown in experimental plots or the greenhouse. We found that selection coefficients estimated by path analysis using phenotypic data were highly correlated with those based on genotypic data with little systematic bias in estimating the strength of selection. Although not a panacea, using path analysis can substantially reduce environmental biases in estimates of selection coefficients. Such confidence in phenotypic selection estimates is critical for progress in the study of natural selection.

Maternal Effects and Germination Timing Mediate the Expression of Winter and Spring Annual Life Histories in Arabidopsis thaliana

In natural populations of the annual plant Arabidopsis thaliana, season of germination determines life history. Spring annuals overwinter as seeds and germinate and flower in spring. Winter annuals germinate in fall, overwinter as rosettes, and flower in spring. In many plant species, germination is affected by the maternal phenotype during seed production. In those that produce seeds on branches from the main stem and branches from basal nodes, like A. thaliana, there may be positional effects on germination. This study examines the effects of maternal branch type on germination in artificial seasonal spring and fall environments. Seeds from apical and basal branches of 41 accessions of A. thaliana were weighed and divided between spring (low temperature for 21 d) and fall (ambient temperature) germination environments. Maternal branch type had significant effects on germination fraction and seed mass, but the direction of the effect differed among accessions. The genetic correlation between seed mass and germination fraction was positive for seeds in the spring germination environment and negative in the fall germination environment. There was a positive longitudinal cline for seed mass, a negative longitudinal cline for germination fraction, and a latitudinal cline for germination fraction that depended on the germination environment. These results show that there is geographic variation in germination traits and suggest that genetic variation in mass can lead to variation in season of germination for A. thaliana.