Microgeographic variation in early fitness traits of Pinus sylvestris from contrasting soils.

PREMISE: The possibility of fine-scale intraspecific adaptive divergence under gene flow is established by theoretical models and has been confirmed empirically in tree populations distributed along steep altitudinal clines or across extreme edaphic discontinuities. However, the possibility of microgeographic adaptive divergence due to less severe but more frequent kinds of soil variation is unclear. METHODS: In this study, we looked for evidence of local adaptation to calcareous versus siliceous soil types in two nearby Mediterranean Pinus sylvestris populations connected via pollen flow. Using a greenhouse experiment, we tested for variation in early (up to three years of age) seedling performance among open-pollinated maternal families originating from each edaphic provenance when experimentally grown on both types of natural local substrate. RESULTS: Although seedlings were clearly affected by the edaphic environment, exhibiting lower and slower emergence as well as higher mortality on the calcareous than in the siliceous substrate, neither the performance on each substrate nor the plasticity among substrates varied significantly with seedling edaphic provenance. CONCLUSIONS: We found no evidence of local adaptation to a non-extreme edaphic discontinuity over a small spatial scale, at least during early stages of seedling establishment. Future studies on microgeographic soil-driven adaptation should consider long-term experiments to minimize maternal effects and allow a potentially delayed expression of edaphic adaptive divergence.

Genetic variation in early fitness traits across European populations of silver birch (Betula pendula).

Given that the ecological niche of tree species is typically narrower for earlier life stages, intraspecific genetic variation at early fitness traits may greatly influence the adaptive response of tree populations to changing environmental conditions. In this study, we evaluated genetic variation in early fitness traits among 12 populations of Betula pendula from a wide latitudinal range in Europe (41-55°N). We first conducted a chamber experiment to test for population differences in germination and the effect of pre-chilling treatment on seed dormancy release. We then established three common gardens spread across the species latitudinal range in order to evaluate levels of quantitative genetic variation and genotype-by-environment interaction at different early life traits. Our results showed significant variation in chamber germination rates among populations (0-60 %), with southern populations exhibiting lower germination. Pre-chilling treatments did not generally improve germination success. Population seedling emergence rates in the field were correlated with chamber germination rates, though being an order of magnitude lower, with an average ranging from 0 to 1.3 % across gardens. Highly significant variation was found in field emergence rates among populations, and between seed-crop years within populations, but not among families within populations. Populations differed in seedling height, diameter, slenderness and budburst date, with significant among-family variation. Population latitude was positively associated with chamber germination rate and with seedling emergence rate in one of the central field sites. Overall, genetic, environmental and demographic factors seem to influence the observed high levels of variation in early fitness traits among B. pendula populations. Our results suggest limited regeneration capacity for the study species under drier conditions, but further field trials with sufficient replication over environments and seed crops will improve our understanding of its vulnerability to climate change.

Measuring viability selection from prospective cohort mortality studies: A case study in maritime pine.

By changing the genetic background available for selection at subsequent life stages, stage-specific selection can define adaptive potential across the life cycle. We propose and evaluate here a neutrality test and a Bayesian method to infer stage-specific viability selection coefficients using sequential random genotypic samples drawn from a longitudinal cohort mortality study, within a generation. The approach is suitable for investigating selective mortality in large natural or experimental cohorts of any organism in which individual tagging and tracking are unfeasible. Numerical simulation results indicate that the method can discriminate loci under strong viability selection, and provided samples are large, yield accurate estimates of the corresponding selection coefficients. Genotypic frequency changes are largely driven by sampling noise under weak selection, however, compromising inference in that case. We apply the proposed methods to analyze viability selection operating at early recruitment stages in a natural maritime pine (Pinus pinaster Ait.) population. We measured temporal genotypic frequency changes at 384 candidate-gene SNP loci among seedlings sampled from the time of emergence in autumn until the summer of the following year, a period with high elimination rates. We detected five loci undergoing allele frequency changes larger than expected from stochastic mortality and sampling, with putative functions that could influence survival at early seedling stages. Our results illustrate how new statistical and sampling schemes can be used to conduct genomic scans of contemporary selection on specific life stages.

Assessing early fitness consequences of exotic gene flow in the wild: a field study with Iberian pine relicts.

Gene flow from plantations of nonlocal (genetically exotic) tree provenances into natural stands of the same species is probably a widespread phenomenon, but its effects remain largely unexamined. We investigated early fitness consequences of intraspecific exotic gene flow in the wild by assessing differences in survival among native, nonlocal, and F1 intraspecific hybrid seedlings naturally established within two native pine relicts (one of Pinus pinaster and the other of P. sylvestris) surrounded by nonlocal plantations. We obtained broad-scale temporally sequential genotypic samples of a cohort of recruits in each pine relict, from seeds before dispersal to established seedlings months after emergence, tracking temporal changes in the estimated proportion of each parental cross-type. Results show significant proportions of exotic male gametes before seed dispersal in the two pine relicts. Subsequently to seedling establishment, the frequency of exotic male gametes became nonsignificant in P. pinaster, and dropped by half in P. sylvestris. Exotic zygotic gene flow was significantly different from zero among early recruits for P. sylvestris, decreasing throughout seedling establishment. Seedling mortality resulted in small late sample sizes, and temporal differences in exotic gene flow estimates were not significant, so we could not reject the null hypothesis of invariant early viability across parental cross types in the wild.

Assessing intraspecific variation in effective dispersal along an altitudinal gradient: a test in two Mediterranean high-mountain plants.

BACKGROUND: Plant recruitment depends among other factors on environmental conditions and their variation at different spatial scales. Characterizing dispersal in contrasting environments may thus be necessary to understand natural intraspecific variation in the processes underlying recruitment. Silene ciliata and Armeria caespitosa are two representative species of cryophilic pastures above the tree line in Mediterranean high mountains. No explicit estimations of dispersal kernels have been made so far for these or other high-mountain plants. Such data could help to predict their dispersal and recruitment patterns in a context of changing environments under ongoing global warming. METHODS: We used an inverse modelling approach to analyse effective seed dispersal patterns in five populations of both Silene ciliata and Armeria caespitosa along an altitudinal gradient in Sierra de Guadarrama (Madrid, Spain). We considered four commonly employed two-dimensional seedling dispersal kernels exponential-power, 2Dt, WALD and log-normal. KEY RESULTS: No single kernel function provided the best fit across all populations, although estimated mean dispersal distances were short (<1 m) in all cases. S. ciliata did not exhibit significant among-population variation in mean dispersal distance, whereas significant differences in mean dispersal distance were found in A. caespitosa. Both S. ciliata and A. caespitosa exhibited among-population variation in the fecundity parameter and lacked significant variation in kernel shape. CONCLUSIONS: This study illustrates the complexity of intraspecific variation in the processes underlying recruitment, showing that effective dispersal kernels can remain relatively invariant across populations within particular species, even if there are strong variations in demographic structure and/or physical environment among populations, while the invariant dispersal assumption may not hold for other species in the same environment. Our results call for a case-by-case analysis in a wider range of plant taxa and environments to assess the prevalence and magnitude of intraspecific dispersal variation.

Space, time and complexity in plant dispersal ecology.

Dispersal of pollen and seeds are essential functions of plant species, with far-reaching demographic, ecological and evolutionary consequences. Interest in plant dispersal has increased with concerns about the persistence of populations and species under global change. We argue here that advances in plant dispersal ecology research will be determined by our ability to surmount challenges of spatiotemporal scales and heterogeneities and ecosystem complexity. Based on this framework, we propose a selected set of research questions, for which we suggest some specific objectives and methodological approaches. Reviewed topics include multiple vector contributions to plant dispersal, landscape-dependent dispersal patterns, long-distance dispersal events, spatiotemporal variation in dispersal, and the consequences of dispersal for plant communities, populations under climate change, and anthropogenic landscapes.

Long-distance gene flow and adaptation of forest trees to rapid climate change.

Forest trees are the dominant species in many parts of the world and predicting how they might respond to climate change is a vital global concern. Trees are capable of long-distance gene flow, which can promote adaptive evolution in novel environments by increasing genetic variation for fitness. It is unclear, however, if this can compensate for maladaptive effects of gene flow and for the long-generation times of trees. We critically review data on the extent of long-distance gene flow and summarise theory that allows us to predict evolutionary responses of trees to climate change. Estimates of long-distance gene flow based both on direct observations and on genetic methods provide evidence that genes can move over spatial scales larger than habitat shifts predicted under climate change within one generation. Both theoretical and empirical data suggest that the positive effects of gene flow on adaptation may dominate in many instances. The balance of positive to negative consequences of gene flow may, however, differ for leading edge, core and rear sections of forest distributions. We propose future experimental and theoretical research that would better integrate dispersal biology with evolutionary quantitative genetics and improve predictions of tree responses to climate change.

Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata, Née).

For plant populations, gene movement through pollen and seed dispersal governs the size of local genetic neighbourhoods and shapes the opportunities for natural selection and genetic drift. A critical question is how together these two processes influence the evolutionary dynamics of local populations. To assess the respective contributions of pollen and seed flow, we propose a novel indirect assessment of the separate male and female gametic contributions to total effective parental size (N(e)), based on parental correlations estimated via kinship coefficients, that can be applied to data sets that include unambiguous genotypes for male and female gametic contributions. Using the endemic Californian valley oak (Quercus lobata) as our study species, we apply this method to a set of microsatellite genotypes for two distinct ecological sets of naturally recruiting seedlings with acorns attached. We found that the effective numbers of contributing male parents (N(ep)) exceed effective numbers of female parents (N(em)) for seedlings established beneath adult trees (N(ep) = 8.1 and N(em) = 1.1), as well as for seedlings established away from adult trees (N(ep) = 15.4 and N(em) = 2.7), illustrating that seed dispersal enhances pollen dispersal and increases the effective number of seed sources in open seedling patches. The resulting effective parental size of seedling populations translates into smaller effective numbers of parents for undispersed vs. dispersed seedlings (N(e) = 3.6 and N(e) = 6.7, respectively). This study introduces a novel statistic method and provides important new evidence that, on a short-term temporal scale, seed dispersal shapes the local neighbourhood size of new recruits.

Estimation of the seed dispersal kernel from exact identification of source plants.

The exact identification of individual seed sources through genetic analysis of seed tissue of maternal origin has recently brought the full analytical potential of parentage analysis to the study of seed dispersal. No specific statistical methodology has been described so far, however, for estimation of the dispersal kernel function from categorical maternity assignment. In this study, we introduce a maximum-likelihood procedure to estimate the seed dispersal kernel from exact identification of seed sources. Using numerical simulations, we show that the proposed method, unlike other approaches, is independent of seed fecundity variation, yielding accurate estimates of the shape and range of the seed dispersal kernel under varied sampling and dispersal conditions. We also demonstrate how an obvious estimator of the dispersal kernel, the maximum-likelihood fit of the observed distribution of dispersal distances to seed traps, can be strongly biased due to the spatial arrangement of seed traps relative to source plants. Finally, we illustrate the use of the proposed method with a previously published empirical example for the animal-dispersed tree species Prunus mahaleb.

Pollen dispersal in spatially aggregated populations.

We perform a theoretical study of effective pollen dispersal within plant populations exhibiting intraspecific spatial aggregation. We simulate nonuniform distributions of individuals by means of a Poisson cluster process and use an individual-based spatially explicit model of pollen dispersal to assess the effects of different aggregation patterns on the effective pollen pool size (N(ep)) and the axial variance of pollen dispersal (sigma (p)). Results show clear interactions between clumping and both N(ep) and sigma (p), whose precise form and intensity depend on the relative spatial scale of aggregation to pollen dispersal range. If clump size is small relative to dispersal range, clumping results in lower N(ep) and sigma (p) than in randomly distributed populations. Interestingly, by contrast, aggregation may actually enlarge N(ep) and has minimum impact on sigma (p) if clump size is near or above the scale of dispersal. High intraclump to global density ratios enhance the sensitivity of both N(ep) and sigma (p) to clumping, while leptokurtic pollen dispersal generates sharper reductions of both N(ep) and sigma (p) for small clump sizes and stronger increments of N(ep) for larger clump sizes. Overall, our results indicate that isolation-by-distance models in plants should not ignore the effects of intraspecific spatial aggregation on effective dispersal.

A new method of estimating the pollen dispersal curve independently of effective density.

We introduce a novel indirect method of estimating the pollen dispersal curve from mother-offspring genotypic data. Unlike an earlier indirect approach (TwoGener), this method is based on a normalized measure of correlated paternity between female pairs whose expectation does not explicitly depend on the unknown effective male population density (d(e)). We investigate the statistical properties of the new method, by comparison with those of TwoGener, considering the sensitivity to reductions of d(e), relative to census density, resulting from unequal male fecundity and asynchronous flowering. Our main results are: (i) it is possible to obtain reliable estimates of the average distance of pollen dispersal, delta, from indirect methods, even under nonuniform male fecundity and variable flowering phenology; (ii) the new method yields more accurate and more precise delta-estimates than TwoGener under a wide range of sampling and flowering scenarios; and (iii) TwoGener can be used to obtain approximate d(e) estimates, if needed for other purposes. Our results also show that accurately estimating the shape of the tail of the pollen dispersal function by means of indirect methods remains a very difficult challenge.