Joint estimation of contemporary seed and pollen dispersal rates among plant populations

There are few statistical methods for estimating contemporary dispersal among plant populations. A maximum-likelihood procedure is introduced here that uses pre- and post-dispersal population samples of biparentally inherited genetic markers to jointly estimate contemporary seed and pollen immigration rates from a set of discrete external sources into a target population. Monte Carlo simulations indicate that accurate estimates and reliable confidence intervals can be obtained using this method for both pollen and seed migration rates at modest sample sizes (100 parents/population and 100 offspring) when population differentiation is moderate (F(ST) ≥ 0.1), or by increasing pre-dispersal samples (to about 500 parents/population) when genetic divergence is weak (F(ST) = 0.01). The method exhibited low sensitivity to the number of source populations and achieved good accuracy at affordable genetic resolution (10 loci with 10 equifrequent alleles each). Unsampled source populations introduced positive biases in migration rate estimates from sampled sources, although they were minor when the proportion of immigration from the latter was comparatively low. A practical application of the method to a metapopulation of the Australian resprouter shrub Banksia attenuata revealed comparable levels of directional seed and pollen migration among dune groups, and the estimate of seed dispersal was higher than a previous estimate based on conservative assignment tests. The method should be of interest to researchers and managers assessing broad-scale nonequilibrium seed and pollen gene flow dynamics in plants.     

The meaning and measurement of size hierarchies in plant populations

Summary The term size hierarchy has been used frequently by plant population biologists but it has not been defined. Positive skewness of the size distribution, which has been used to evaluate size hierarchies, is inappropriate. We suggest that size hierarchy is equivalent to size inequality. Methods developed by economists to evaluate inequalities in wealth and income, the Lorenz curve and Gini Coefficient, provide a useful quantification of inequality and allow us to compare populations. A measure of inequality such as the Gini Coefficient will usually be more appropriate than a measure of skewness for addressing questions concerning plant population structure.     

A model-based method for estimating effective dispersal distance in tropical plant populations

Dispersal is a key mechanism to help populations propagate across space and thus is important in helping to understand spatial patterns. However, it is often difficult to quantify empirically as it requires intensive and detailed field study. Here we describe a method for estimating the effective dispersal distance of tropical plant populations. The method integrates a simple spatially explicit, individual-based dynamic model and spatial statistical analysis. The model is partly parameterized from spatial point pattern data as well as time series data from a 50 ha tropical forest plot in Barro Colorado Island (BCI) in Panama. Correlation between our estimated dispersal distances and those from inverse modeling based on field studies to date on BCI raises some questions about the match between our methods and those previously used. The method we propose can be generalized to any population for which spatial point pattern data are available. Additional field studies would be useful to further validate our method.     

Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons

The diversification of the teleost suborder Notothenioidei (Perciformes) in Antarctic waters provides one of the most striking examples of a marine adaptive radiation. Along with a number of adaptations to the cold environment, such as the evolution of antifreeze glycoproteins, notothenioids diversified into eight families and at least 130 species. Here, we investigate the genetic population structure of the humped rockcod ( Gobionotothen gibberifrons ), a benthic notothenioid fish. Six populations were sampled at different locations around the Scotia Sea, comprising a large part of the species' distribution range ( N  = 165). Our analyses based on mitochondrial DNA sequence data (352 bp) and eight microsatellite markers reveal a lack of genetic structuring over large geographic distances (Φ_ST ≤ 0.058, F _ST ≤ 0.005, P values nonsignificant). In order to test whether this was due to passive larval dispersal, we used GPS-tracked drifter trajectories, which approximate movement of passive surface particles with ocean currents. The drifter data indicate that the Antarctic Circumpolar Current (ACC) connects the sampling locations in one direction only (west–east), and that passive transport is possible within the 4-month larval period of G. gibberifrons . Indeed, when applying the isolation-with-migration model in IMA, strong unidirectional west-east migration rates are detected in the humped rockcod. This leads us to conclude that, in G. gibberifrons , genetic differentiation is prevented by gene flow via larval dispersal with the ACC.     

Gene flow among small populations of a self-incompatible plant: an interaction between demography and genetics

We assessed the effects of population size and genetic relatedness on rates of pollen gene flow into experimental populations of the insect-pollinated, self-incompatible plant Raphanus sativus. We created synthetic populations of sizes 2, 5, 10, and 20 with three genetic structures (full siblings, half siblings, and unrelated plants). Following pollination in a natural setting, we conducted a simple paternity exclusion analysis using the allozyme genotypes of progeny to measure apparent gene flow and Monte Carlo simulations to estimate total gene flow. Estimates of apparent pollen gene flow rates ranged from 0 to 100% and were similar in rank to estimates of total gene flow. There were significant effects of population size and relatedness on the rate of apparent gene flow, and there were significant population size by relatedness interactions. Populations of size 2 had higher gene flow rates than larger populations, gene flow being negatively associated with the level of cross-compatibility (as measured by hand pollinations). Gene flow into populations of size 2 was also negatively associated with the distance to the nearest population of size 10 or 20. These results suggest that interactions among demography (population size), genetics (cross-compatibility), and ecology (pollinator behavior) are important influences on pollen gene flow rates into small plant populations.     

Gene flow between populations of two invertebrates in springs

1. Using allozymes, we analysed genetic structure of the freshwater gastropod Bythinella dunkeri and the freshwater flatworm Crenobia alpina. The two species are habitat specialists, living almost exclusively in springs. The sampled area in Hesse (Germany) covers a spatial scale of 20 km and includes two river drainages. From the biology of the two species we expected little dispersal along rivers. However, the possibility exists that groundwater provide suitable pathways for dispersal. 2. In B. dunkeri heterozygosity decreased from west to east. For some alleles we found clines in this geographic direction. These clines generated a positive correlation between geographic distance and genetic differentiation. Furthermore patterns of genetic variation within populations suggested that populations may have been faced with bottlenecks and founder effects. If populations are not in population genetic equilibrium, such founder effects would also explain the rather high amount of genetic differentiation between populations (10%). 3. For C. alpina the mean number of alleles decreased with increasing isolation of populations. Genetic differentiation between populations contributed 19% to the total genetic variation. Genetic differentiation was not correlated to geographic distance, but compared with B. dunkeri variability of pairwise differentiation between pairs of populations was higher in C. alpina. 4. Overall B. dunkeri appears to be a fairly good disperser, which may use groundwater as dispersal pathway. Furthermore populations seem to be not in equilibrium. In contrast C. alpina forms rather isolated populations with little dispersal between springs and groundwater seems to play no important role for dispersal.     

The importance of dispersal in determining seed versus safe site limitation of plant populations

The traditional dichotomy of seed versus safe site limitation of plant populations is an oversimplification. While most plant models implicitly assume that the number of safe sites colonized will increase directly with increased seed production by each plant, the number of sites colonized may also strongly depend on patterns of seed dispersal relative to the parent plant, since the majority of a plant’s seeds are deposited very close to it and so not all safe sites are equally accessible. I created a series of spatially explicit individual based plant population models exploring how seed versus safe site limitation is jointly affected by the number of seeds produced per plant and mean dispersal distances. While increased dispersal distance led to reduced seed limitation (more saturation of available safe sites) when a parent plant’s site was temporarily unsuitable following its death, increased dispersal distances could increase seed limitation, especially at low per-plant fecundities, if safe sites did not turn over through time. Models comparing localized to global seed dispersal indicated substantially different degrees of seed limitation for constant per-plant fecundities. Thus seed addition experiments need to be designed to add seeds in realistic spatial patterns to yield meaningful results.     

Gene flow and melanism in Lake Erie garter snake populations

Melanistic garter snakes ( Thamnophis sirtalis ) are unusually common near Lake Erie, apparently because selection for thermoregulatory ability in cool lake-shore habitats (which favours melanistic morphs) outweighs selection for crypsis (which favours striped morphs). However, morph frequencies are highly variable among sites, suggesting that random genetic drift also influences colour pattern. In an effort to better understand the evolutionary processes influencing garter snake colour patterns, we estimated Fx and Nm (the number of migrants per generation) among island and mainland populations from patterns of allozymic variation detected using electrophoresis. Estimates of Nm were high, ranging from 2.7 to 37.6 between pairs of study sites and making it unlikely that differences in morph frequencies among sites were solely the result of random genetic drift. Furthermore, differences in F _st estimates between colour pattern (a one-locus two-allele trait) and allozyme loci suggest that colour pattern alleles are not in Hardy-Weinberg equilibrium, most likely as a result of natural selection. Comparison of allozymic data from Lake Erie with those from more distant sites suggests that gene flow occurs over long distances in T. sirtalis.     

The dispersal success and persistence of populations with asymmetric dispersal

Asymmetric dispersal is a common trait among populations, often attributed to heterogeneity and stochasticity in both environment and demography. The cumulative effects of population dispersal in space and time have been described with some success by Van Kirk and Lewis’s average dispersal success approximation (Bull Math Biol 59(1): 107–137 1997), but this approximation has been demonstrated to perform poorly when applied to asymmetric dispersal. Here we provide a comparison of different characterizations of dispersal success and demonstrate how to capture the effects of asymmetric dispersal. We apply these different methods to a variety of integrodifference equation population models with asymmetric dispersal, and examine the methods’ effectiveness in approximating key ecological traits of the models, such as the critical patch size and the critical speed of climate change for population persistence.     

Gene flow from foreign provenances into local plant populations: Fitness consequences and implications for biodiversity restoration

Long-distance transplantation of seed material as done in restoration programs has raised concerns about the risks associated with the introduction of maladapted genotypes that may hybridize with neighboring native conspecifics and decrease local population fitness (outbreeding depression). We studied the consequences of gene flow from foreign provenances into local populations in the common grassland species Plantago lanceolata (Plantaginaceae). Three generations of intraspecific hybrids (F(1), F(2), and backcross to the local plants) were produced by controlled crossings between local plants and plants from geographically or environmentally distant populations. Their performance was compared to that of within-population crosses in a field experiment. Early growth in some interpopulation hybrids was significantly reduced, and this decrease in performance was higher in progeny of crosses with the local population from a different habitat than with geographically distant populations. At the end of the growing season, most fitness-related traits of the interpopulation hybrids were close to the average of their parents. Crosses with low-performing foreign parents therefore resulted in reduced fitness of the hybrids compared to the local plants and dilution of local adaptation. We conclude that the introduction of maladapted populations from distant or ecologically distinct environments might, at least temporarily, decrease the fitness of neighboring local plants.     

Cautions on direct gene flow estimation in plant populations

Through simulations we have investigated the statistical properties of two of the main approaches for directly estimating pollen gene flow (m) in plant populations: genotypic exclusion and mating models. When the assumptions about accurately known background pollen pool allelic frequencies are met, both methods provide unbiased results with comparable variances across a range of true m values. However, when presumed allelic frequencies differ from actual ones, which is more likely in research practice, both estimators are biased. We demonstrate that the extent and direction of bias largely depend on the difference (measured as genetic distance) between the presumed and actual pollen pools, and on the degree of genetic differentiation between the local population and the actual background pollen sources. However, one feature of the mating model is its ability to estimate pollen gene flow simultaneously with background pollen pool allelic frequencies. We have found that this approach gives nearly unbiased pollen gene flow estimates, and is practical because it eliminates the necessity of providing independent estimates of background pollen pool allelic frequencies. Violations of the mating model assumptions of random mating within local population affect the precision of the estimates only to a limited degree.     

Conditions for protected polymorphism in subdivided plant populations: 1. Uniform pollen dispersal

Pollen and seed migration patterns are not the same in most plant populations, and the differences affect conditions for protection of alleles. We analyzed conditions for protectedness when pollen is freely exchanged along all demes, while seeds are deposited within the female parents' deme. Protectedness was analyzed at the boundary of fixation and necessary conditions were derived.If no selection among female genotypes exists, then simple average heterozygote superiority in the males can guarantee protection. However, regardless of the form of selection in females, simply doubling the male heterozygote superiority can still guarantee protectedness. Conditions for guaranteeing protectedness with female selection were also derived but are more complicated.The effect of inter-demic variability on protectedness of a biallelic polymorphim is studied for a particular method of reducing the variances of the selection values. It is shown that decreasing the variance of the female selection values also decreases protectedness. This is not necessarily true for the male selection values.     

Gene flow and natal dispersal in the Siberian flying squirrel based on direct and indirect data

Dispersal is a key determinant of the evolution and ecology of species. For a comprehensive picture of dispersal, a combination of both field observations and indirect genetic measures are required, as both of these have strengths that may mitigate the other’s limitations. Here, we used microsatellite markers and radio-telemetry data to study dispersal and gene flow in Siberian flying squirrels. Genetic data confirmed our empirical results that dispersal is female biased in the flying squirrel. Female bias in dispersal is exceptional among mammals and in flying squirrels is probably explained by competition for food resources and nesting cavities among mothers and daughters. The individual-level genetic pattern was influenced by isolation by distance. Using this information fairly comparable dispersal distances were derived using indirect data as observed directly with radio telemetry. Thus, our results support the recent conclusion that individual-level genetic data can be useful in inferring dispersal distances for species for which direct data are lacking.     

Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations

There is accumulating evidence that individuals leave their natal area and select a breeding habitat non-randomly by relying upon information about their natal and future breeding environments. This variation in dispersal is not only based on external information (condition dependence) but also depends upon the internal state of individuals (phenotype dependence). As a consequence, not all dispersers are of the same quality or search for the same habitats. In addition, the individual's state is characterized by morphological, physiological or behavioural attributes that might themselves serve as a cue altering the habitat choice of conspecifics. These combined effects of internal and external information have the potential to generate complex movement patterns and could influence population dynamics and colonization processes. Here, we highlight three particular processes that link condition-dependent dispersal, phenotype-dependent dispersal and habitat choice strategies: (1) the relationship between the cause of departure and the dispersers' phenotype; (2) the relationship between the cause of departure and the settlement behaviour and (3) the concept of informed dispersal, where individuals gather and transfer information before and during their movements through the landscape. We review the empirical evidence for these processes with a special emphasis on vertebrate and arthropod model systems, and present case studies that have quantified the impacts of these processes on spatially structured population dynamics. We also discuss recent literature providing strong evidence that individual variation in dispersal has an important impact on both reinforcement and colonization success and therefore must be taken into account when predicting ecological responses to global warming and habitat fragmentation.     

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.     

Understanding plant dispersal and migration

The Plant Dispersal and Migration workshop was held in Montpellier, France, from 19 to 23 June 2001.     

Pollen dispersal and gene flow within and into a population of the alpine monocarpic plant Campanula thyrsoides

Background and Aims

Gene flow by seed and pollen largely shapes the genetic structure within and among plant populations. Seed dispersal is often strongly spatially restricted, making gene flow primarily dependent on pollen dispersal within and into populations. To understand distance-dependent pollination success, pollen dispersal and gene flow were studied within and into a population of the alpine monocarpic perennial Campanula thyrsoides.

Methods

A paternity analysis was performed on sampled seed families using microsatellites, genotyping 22 flowering adults and 331 germinated offspring to estimate gene flow, and pollen analogues were used to estimate pollen dispersal. The focal population was situated among 23 genetically differentiated populations on a subalpine mountain plateau (<10 km²) in central Switzerland.

Key Results

Paternity analysis assigned 110 offspring (33·2 %) to a specific pollen donor (i.e. ‘father’) in the focal population. Mean pollination distance was 17·4 m for these offspring, and the pollen dispersal curve based on positive LOD scores of all 331 offspring was strongly decreasing with distance. The paternal contribution from 20–35 offspring (6·0–10·5 %) originated outside the population, probably from nearby populations on the plateau. Multiple potential fathers were assigned to each of 186 offspring (56·2 %). The pollination distance to ‘mother’ plants was negatively affected by the mothers'' degree of spatial isolation in the population. Variability in male mating success was not related to the degree of isolation of father plants.

Conclusions

Pollen dispersal patterns within the C. thyrsoides population are affected by spatial positioning of flowering individuals and pollen dispersal may therefore contribute to the course of evolution of populations of this species. Pollen dispersal into the population was high but apparently not strong enough to prevent the previously described substantial among-population differentiation on the plateau, which may be due to the monocarpic perenniality of this species.