Heterosis is common and inbreeding depression absent in natural populations of Arabidopsis thaliana.

The importance of genetic drift in shaping patterns of adaptive genetic variation in nature is poorly known. Genetic drift should drive partially recessive deleterious mutations to high frequency, and inter-population crosses may therefore exhibit heterosis (increased fitness relative to intra-population crosses). Low genetic diversity and greater genetic distance between populations should increase the magnitude of heterosis. Moreover, drift and selection should remove strongly deleterious recessive alleles from individual populations, resulting in reduced inbreeding depression. To estimate heterosis, we crossed 90 independent line pairs of Arabidopsis thaliana from 15 pairs of natural populations sampled across Fennoscandia and crossed an additional 41 line pairs from a subset of four of these populations to estimate inbreeding depression. We measured lifetime fitness of crosses relative to parents in a large outdoor common garden (8,448 plants in total) in central Sweden. To examine the effects of genetic diversity and genetic distance on heterosis, we genotyped parental lines for 869 SNPs. Overall, genetic variation within populations was low (median expected heterozygosity = 0.02), and genetic differentiation was high (median FST  = 0.82). Crosses between 10 of 15 population pairs exhibited significant heterosis, with magnitudes of heterosis as high as 117%. We found no significant inbreeding depression, suggesting that the observed heterosis is due to fixation of mildly deleterious alleles within populations. Widespread and substantial heterosis indicates an important role for drift in shaping genetic variation, but there was no significant relationship between fitness of crosses relative to parents and genetic diversity or genetic distance between populations.

Adaptive divergence in flowering time among natural populations of Arabidopsis thaliana: Estimates of selection and QTL mapping.

To identify the ecological and genetic mechanisms of local adaptation requires estimating selection on traits, identifying their genetic basis, and evaluating whether divergence in adaptive traits is due to conditional neutrality or genetic trade-offs. To this end, we conducted field experiments for three years using recombinant inbred lines (RILs) derived from two ecotypes of Arabidopsis thaliana (Italy, Sweden), and at each parental site examined selection on flowering time and mapped quantitative trait loci (QTL). There was strong selection for early flowering in Italy, but weak selection in Sweden. Eleven distinct flowering time QTL were detected, and for each the Italian genotype caused earlier flowering. Twenty-seven candidate genes were identified, two of which (FLC and VIN3) appear under major flowering time QTL in Italy. Seven of eight QTL in Italy with narrow credible intervals colocalized with previously reported fitness QTL, in comparison to three of four in Sweden. The results demonstrate that the magnitude of selection on flowering time differs strikingly between our study populations, that the genetic basis of flowering time variation is multigenic with some QTL of large effect, and suggest that divergence in flowering time between ecotypes is due mainly to conditional neutrality.

Seed dormancy cycling and mortality differ between two locally adapted populations of Arabidopsis thaliana.

BACKGROUND AND AIMS: Intraspecific variation in seed bank dynamics should contribute to local adaptation, but is not well studied. The extent to which genetic and environmental factors affect dormancy cycling and seed mortality was investigated in the annual herb Arabidopsis thaliana by conducting a reciprocal seed burial experiment. METHODS: Seeds from two locally adapted populations (from Italy and Sweden) were buried at both of the sites of origin, and seed mortality and germinability were determined during the following 2 years for initially non-dormant glasshouse-matured seeds and dormant field-matured seeds. KEY RESULTS: Mean soil temperature was higher at the Italian site compared with the Swedish site throughout the year, and the germination proportions were in general higher for seeds buried in Italy than in Sweden. The rate of secondary dormancy induction of the Italian genotype was faster than that of the Swedish genotype at both sites, while the opposite was true for the rate of dormancy release, at least at the Swedish site. The comparison of non-dormant glasshouse seeds with dormant field seeds demonstrated that A. thaliana seeds can adjust their dormancy levels to current environmental conditions, and suggests that maternal environmental conditions have only minor effects on dormancy cycles. At both sites, locally produced seeds had low germinability in the first year compared with the second year, suggesting that a considerable fraction of the seeds would enter the seed bank. In Italy, but not in Sweden, seed mortality increased rapidly during the second year of burial. CONCLUSIONS: This is the first demonstration of intraspecific genetic differentiation in the annual seed dormancy cycle of any species, and the documented difference is likely to contribute to local adaptation. The results suggest that the contribution of a seed bank to seedling recruitment should vary among environments due to differences in the rate of seed mortality.

Contrasting patterns of genetic structuring in natural populations of Arabidopsis lyrata Subsp. petraea across different regions in northern Europe.

Level and partitioning of genetic diversity is expected to vary between contrasting habitats, reflecting differences in strength of ecological and evolutionary processes. Therefore, it is necessary to consider processes acting on different time scales when trying to explain diversity patterns in different parts of species' distributions. To explore how historical and contemporary factors jointly may influence patterns of genetic diversity and population differentiation, we compared genetic composition in the perennial herb Arabidopsis lyrata ssp. petraea from the northernmost parts of its distribution range on Iceland to that previously documented in Scandinavia. Leaf tissue and soil were sampled from ten Icelandic populations of A. lyrata. Seedlings were grown from soil samples, and tissue from above-ground and seed bank individuals were genotyped with 21 microsatellite markers. Seed bank density in Icelandic populations was low but not significantly different from that observed in Norwegian populations. While within-population genetic diversity was relatively high on Iceland (H(E) = 0.35), among-population differentiation was low (F(ST) = 0.10) compared to Norwegian and Swedish populations. Population differentiation was positively associated with geographical distance in both Iceland and Scandinavia, but the strength of this relationship varied between regions. Although topography and a larger distribution range may explain the higher differentiation between mountainous Norwegian relative to lowland populations in Sweden, these factors cannot explain the lower differentiation in Icelandic compared to Swedish populations. We propose that low genetic differentiation among Icelandic populations is not caused by differences in connectivity, but is rather due to large historical effective population sizes. Thus, rather than contemporary processes, historical factors such as survival of Icelandic lineages in northern refugia during the last glacial period may have contributed to the observed pattern.

Seed dispersal in time can counteract the effect of gene flow between natural populations of Arabidopsis thaliana.

Plants may escape unfavorable environments by dispersing to new sites, or by remaining in an ungerminated state at a given site until environmental conditions become favorable. There is limited evidence regarding the occurrence, interplay and relative importance of dispersal processes in time and space in plant populations. Thirty-six natural populations of the annual ruderal species Arabidopsis thaliana were monitored over five consecutive years, sampling both seed bank and above-ground cohorts. We show that immigration rates are considerably higher than previously inferred, averaging 1.7% per population yr(-1). On the other hand, almost one-third of the individuals in a given above-ground cohort result from seeds shed 2 or 3 yr back in time in 10 of the studied populations. Populations that disappeared one year were recolonized by regeneration from the seed bank the subsequent year. Thus, dispersal in both time and space is an important contributor to the structuring of genetic variability in natural populations of A. thaliana, where a high dispersal rate in time may partly counteract the homogenizing effects of spatial seed and pollen dispersal.

Genetic structure in a fragmented Northern Hemisphere rainforest: large effective sizes and high connectivity among populations of the epiphytic lichen Lobaria pulmonaria.

An extraordinary diversity of epiphytic lichens is found in the boreal rainforest of central Norway, the highest-latitude rainforest in the world. These rainforest relicts are located in ravine systems, and clear cutting has increased the distance between remaining patches. We hypothesized that the relatively small lichen populations in the remaining forest stands have suffered a depletion of genetic diversity through bottlenecks and founder events. To test this hypothesis, we assessed genetic diversity and structure in the populations of the tripartite lichen Lobaria pulmonaria using eight SSR loci. We sampled thalli growing on Picea abies branches and propagules deposited in snow at three localities. Contrary to expectations, we found high genetic diversity in lichen and snow samples, and high effective sizes of the studied populations. Also, limited genetic differentiation between populations, high historical migration rates, and a high proportion of first generation immigrants were estimated, implying high connectivity across distances <30km. Almost all genetic variation was attributed to variation within sites; spatial genetic structures within populations were absent or appeared on small scales (5-10m). The high genetic diversity in the remaining old boreal rainforests shows that even relict forest patches might be suitable for conservation of genetic diversity.

Genetic consequences of seed banks in the perennial herb Arabidopsis lyrata subsp. petraea (Brassicaceae).

PREMISE OF THE STUDY: Seed banks may increase the effective population size (N(e)) of plants as a result of elevated coalescence times for alleles residing in the populations. This has been empirically demonstrated in populations of the annual Arabidopsis thaliana, whereas comparable data for perennial species are currently lacking. We studied the contribution of seed banks to effective sizes of natural populations of the self-incompatible, perennial Arabidopsis lyrata subsp. petraea, a close relative of A. thaliana. • METHODS: Fourteen populations of A. lyrata collected throughout the Norwegian distribution range were analyzed using microsatellite markers. • KEY RESULTS: The genetic composition of seed-bank and aboveground cohorts was found to be highly similar, with little genetic differentiation between cohorts in most populations. However, the proportion of private alleles was higher in aboveground than in seed-bank cohorts. The presence of seed banks significantly increased total N(e), but the contribution from seed banks to overall N(e) were lower than the contribution from aboveground cohorts in most populations. Estimated historical N(e) values, reflecting the effective sizes of populations throughout the history of the species, were considerably higher than estimates of contemporary N(e), reflecting number of reproducing individuals within the past few generations. • CONCLUSIONS: The results show that the seed bank contributes to total N(e) in the perennial herb A. lyrata. However, the contribution is similar to or lower than that of the above-ground fraction of the population and markedly weaker than that previously documented in the annual A. thaliana.

Investigating the effects of topography and clonality on genetic structuring within a large Norwegian population of Arabidopsis lyrata.

BACKGROUND AND AIMS: The gene flow through pollen or seeds governs the extent of spatial genetic structure in plant populations. Another factor that can contribute to this pattern is clonal growth. The perennial species Arabidopsis lyrata ssp. petraea (Brassicaceae) is a self-incompatible, clonal species found in disjunctive populations in central and northern Europe. METHODS: Fourteen microsatellite markers were employed to study the level of kinship and clonality in a high-altitude mountain valley at Spiterstulen, Norway. The population has a continuous distribution along the banks of the River Visa for about 1.5 km. A total of 17 (10 m x 10 m) squares were laid out in a north-south transect following the river on both sides. KEY RESULTS: It is shown that clonal growth is far more common than previously shown in this species, although the overall size of the genets is small (mean diameter = 6.4 cm). Across the whole population there is no indication of isolation by distance, and spatial genetic structure is only visible on fine spatial scales. In addition, no effect of the river on the spatial distribution of genotypes was found. CONCLUSIONS: Unexpectedly, the data show that populations of small perennials like A. lyrata can behave like panmictic units across relatively large areas at local sites, as opposed to earlier findings in central Europe.

Seed banks cause elevated generation times and effective population sizes of Arabidopsis thaliana in northern Europe.

It is commonly found that effective population sizes of natural populations are much smaller than census sizes of plants and animals. However, theoretical studies have shown that factors rarely investigated empirically, like seed banks in plants and diapause in animals, may have profound influence on effective sizes. Here we investigate whether the presence of seed banks can explain the relatively high genetic variability observed in northern European Arabidopsis thaliana populations with small census sizes. We have genotyped three above- and below- ground cohorts in 27 Norwegian populations using single nucleotide polymorphism markers. Although the populations varied extensively in levels of variability within and between cohorts, standard genetic population measures were comparable to those obtained in previous studies on above-ground cohorts using microsatellite markers. Estimated effective population sizes are larger for total populations (containing both seed bank and above-ground cohorts for 1 year) compared to each of the cohorts considered separately. Using a conservative approach, we find that the effective sizes are larger than census sizes of local populations, and that the effective generation time is higher than 1 year (3-4 years, on average), making A. thaliana a perennial semelparous plant at many northern European localities.