Impacts of seed and pollen flow on population genetic structure for plant genomes with three contrasting modes of inheritance

The classical island and one-dimensional stepping-stone models of population genetic structure developed for animal populations are extended to hermaphrodite plant populations to study the behavior of biparentally inherited nuclear genes and organelle genes with paternal and maternal inheritance. By substituting appropriate values for effective population sizes and migration rates of the genes concerned into the classical models, expressions for genetic differentiation and correlation in gene frequency between populations can be derived. For both models, differentiation for maternally inherited genes at migration-drift equilibrium is greater than that for paternally inherited genes, which in turn is greater than that for biparentally inherited nuclear genes. In the stepping-stone model, the change of genetic correlation with distance is influenced by the mode of inheritance of the gene and the relative values of long- and short-distance migration by seed and pollen. In situations where it is possible to measure simultaneously Fst for genes with all three types of inheritance, estimates of the relative rates of pollen to seed flow can be made for both the short- and long-distance components of migration in the stepping-stone model.     

The effects of pollen and seed migration on nuclear-dicytoplasmic systems. I. Nonrandom associations and equilibrium structure with both maternal and paternal cytoplasmic inheritance

We determine the nuclear-dicytoplasmic effects of unidirectional gene flow via pollen and seeds upon a mixed-mating plant population, focusing on nuclear-mitochondrial-chloroplast systems where mitochondria are inherited maternally and chloroplasts paternally, as in many conifers. After first delineating the general effects of admixture (via seeds or individuals) on the nonrandom associations in such systems, we derive the full dicytonuclear equilibrium structure, including when disequilibria may be indicators of gene flow. Substantial levels of permanent two- and three-locus disequilibria can be generated in adults by (i) nonzero disequilibria in the migrant pools or (ii) intermigrant admixture effects via different chloroplast frequencies in migrant pollen and seeds. Additionally, three-locus disequilibria can be generated by higher-order intermigrant effects such as different chloroplast frequencies in migrant pollen and seeds coupled with nuclear-mitochondrial disequilibria in migrant seeds, or different nuclear frequencies in migrant pollen and seeds coupled with mitochondrial-chloroplast disequilibria in migrant seeds. Further insight is provided by considering special cases with seed or pollen migration alone, complete random mating or selfing, or migrant pollen and seeds lacking disequilibria or intermigrant admixture effects. The results complete the theoretical foundation for a new method for estimating pollen and seed migration using joint cytonuclear or dicytonuclear data.     

Comparative Effects of Pollen and Seed Migration on the Cytonuclear Structure of Plant Populations. II. Paternal Cytoplasmic Inheritance

We continue our study of the effects of pollen and seed migration on the cytonuclear structure of mixed-mating plant populations by analyzing two deterministic continent-island models under the critical assumption of paternal cytoplasmic inheritance. The major results of this study that contrast with our previous conclusions based on maternal cytoplasmic inheritance are (i) pollen gene flow can significantly affect the cytonuclear structure of the island population, and in particular can help to generate cytonuclear disequilibria that greatly exceed the magnitude of those that would be produced by seed migration or mixed mating alone; (ii) with simultaneous pollen and seed migration, nonzero cytonuclear disequilibria will be maintained not only when there is disequilibrium in the immigrant pollen or seeds, but also through a variety of intermigrant admixture effects when the two pools of immigrants differ appropriately in their cytonuclear compositions; (iii) either immigrant pollen or immigrant seeds can generate disequilibria de novo in populations with initially random cytonuclear associations, but pollen migration alone generally produces lower levels of disequilibrium than does comparable seed migration, especially at high levels of self-fertilization when the overall fraction of immigrant pollen is low; (iv) the equilibrium state of the island population will be influenced by the rate of pollen gene flow whenever there is either allelic disequilibrium in the immigrant pollen or simultaneous seed migration coupled with different cytoplasmic or nuclear allele frequencies in immigrant pollen and seeds or nonzero allelic disequilibrium in either immigrant pool. The estimation of pollen migration should therefore be facilitated with paternal cytoplasmic inheritance relative to the case of maternal cytoplasmic inheritance. These basic conclusions hold whether the population is censused as seeds or as adults, but with simultaneous pollen and seed migration, the relationship between census time and the ability to detect nonrandom cytonuclear associations is complex. When migration is through pollen alone, however, the cytonuclear structure of the island population is independent of the life stage censused.     

Using genetic markers to directly estimate gene flow and reproductive success parameters in plants on the basis of naturally regenerated seedlings

Estimating seed and pollen gene flow in plants on the basis of samples of naturally regenerated seedlings can provide much needed information about "realized gene flow," but seems to be one of the greatest challenges in plant population biology. Traditional parentage methods, because of their inability to discriminate between male and female parentage of seedlings, unless supported by uniparentally inherited markers, are not capable of precisely describing seed and pollen aspects of gene flow realized in seedlings. Here, we describe a maximum-likelihood method for modeling female and male parentage in a local plant population on the basis of genotypic data from naturally established seedlings and when the location and genotypes of all potential parents within the population are known. The method models female and male reproductive success of individuals as a function of factors likely to influence reproductive success (e.g., distance of seed dispersal, distance between mates, and relative fecundity--i.e., female and male selection gradients). The method is designed to account for levels of seed and pollen gene flow into the local population from unsampled adults; therefore, it is well suited to isolated, but also wide-spread natural populations, where extensive seed and pollen dispersal complicates traditional parentage analyses. Computer simulations were performed to evaluate the utility and robustness of the model and estimation procedure and to assess how the exclusion power of genetic markers (isozymes or microsatellites) affects the accuracy of the parameter estimation. In addition, the method was applied to genotypic data collected in Scots pine (isozymes) and oak (microsatellites) populations to obtain preliminary estimates of long-distance seed and pollen gene flow and the patterns of local seed and pollen dispersal in these species.     

Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations

Plants offer excellent models to investigate how gene flow shapes the organization of genetic diversity. Their three genomes can have different modes of transmission and will hence experience varying levels of gene flow. We have compiled studies of genetic structure based on chloroplast DNA (cpDNA), mitochondrial DNA (mtDNA) and nuclear markers in seed plants. Based on a data set of 183 species belonging to 103 genera and 52 families, we show that the precision of estimates of genetic differentiation (G(ST)) used to infer gene flow is mostly constrained by the sampling of populations. Mode of inheritance appears to have a major effect on G(ST). Maternally inherited genomes experience considerably more subdivision (median value of 0.67) than paternally or biparentally inherited genomes (approximately 0.10). G(ST) at cpDNA and mtDNA markers covary narrowly when both genomes are maternally inherited, whereas G(ST) at paternally and biparentally inherited markers also covary positively but more loosely and G(ST) at maternally inherited markers are largely independent of values based on nuclear markers. A model-based gross estimate suggests that, at the rangewide scale, historical levels of pollen flow are generally at least an order of magnitude larger than levels of seed flow (median of the pollen-to-seed migration ratio: 17) and that pollen and seed gene flow vary independently across species. Finally, we show that measures of subdivision that take into account the degree of similarity between haplotypes (N(ST) or R(ST)) make better use of the information inherent in haplotype data than standard measures based on allele frequencies only.     

Comparing relative rates of pollen and seed gene flow in the island model using nuclear and organelle measures of population structure

We describe a method for comparing nuclear and organelle population differentiation (F(ST)) in seed plants to test the hypothesis that pollen and seed gene flow rates are equal. Wright's infinite island model is used, with arbitrary levels of self-fertilization and biparental organelle inheritance. The comparison can also be applied to gene flow in animals. Since effective population sizes are smaller for organelle genomes than for nuclear genomes and organelles are often uniparentally inherited, organelle F(ST) is expected to be higher at equilibrium than nuclear F(ST) even if pollen and seed gene flow rates are equal. To reject the null hypothesis of equal seed and pollen gene flow rates, nuclear and organelle F(ST)'s must differ significantly from their expected values under this hypothesis. Finite island model simulations indicate that infinite island model expectations are not greatly biased by finite numbers of populations (>/=100 subpopulations). The power to distinguish dissimilar rates of pollen and seed gene flow depends on confidence intervals for fixation index estimates, which shrink as more subpopulations and loci are sampled. Using data from the tropical tree Corythophora alta, we rejected the null hypothesis that seed and pollen gene flow rates are equal but cannot reject the alternative hypothesis that pollen gene flow is 200 times greater than seed gene flow.     

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.     

植物三种不同遗传方式基因的地理家系谱理论与应用初探

将已知用于从地理空间上离散或连续分布群体随机抽取基因样本的基因家系谱理论推广到两性异交植物上。由于存在不同的群体间基因多率,地３种不同遗传方式的植物基因组（核、叶绿体和线粒体ＤＮＡ）分别进行了研究。理论上证明对于不同遗传方式的基因,通过相应调整有效群体大小和迁移率,现有的基因家系谱理论可直接应用于植物群体上,其中一个结论就是当从离散分布群体中随机抽取ｎ个基因样本时,亚群体间的花粉流和种子流的相对比     

Estimating exotic gene flow into native pine stands: zygotic vs. gametic components

Monitoring contemporary gene flow from widespread exotic plantations is becoming an important problem in forest conservation genetics. In plants, where both seed and pollen disperse, three components of exotic gene flow with potentially unequal consequences should be, but have not been, explicitly distinguished: zygotic, male gametic and female gametic. Building on a previous model for estimating contemporary rates of zygotic and male gametic gene flow among plant populations, we present here an approach that additionally estimates the third (female gametic) gene flow component, based on a combination of uni‐ and biparentally inherited markers. Using this method and a combined set of chloroplast and nuclear microsatellites, we estimate gene flow rates from exotic plantations into two Iberian relict stands of maritime pine (Pinus pinaster) and Scots pine (Pinus sylvestris). Results show neither zygotic nor female gametic gene flow but moderate (6–8%) male gametic introgression for both species, implying significant dispersal of pollen, but not of seeds, from exotic plantations into native stands shortly after introduced trees reached reproductive maturity. Numerical simulation results suggest that the model yields reasonably accurate estimates for our empirical data sets, especially for larger samples. We discuss conservation management implications of observed levels of exposure to nonlocal genes and identify research needs to determine potentially associated hazards. Our approach should be useful for plant ecologists and ecosystem managers interested in the vectors of contemporary genetic connectivity among discrete plant populations.     

Comparative Effects of Pollen and Seed Migration on the Cytonuclear Structure of Plant Populations. I. Maternal Cytoplasmic Inheritance

We explicitly solve and analyze a series of deterministic continent-island models to delimit the effects of pollen and seed migration on cytonuclear frequencies and disequilibria in random-mating, mixed-mating and self-fertilized populations. Given the critical assumption of maternal cytoplasmic inheritance, five major findings are (i) nonzero cytonuclear disequilibria will be maintained in the island population if and only if at least some migration occurs each generation through seeds with nonrandom cytonuclear associations; (ii) immigrant seeds with no cytonuclear disequilibria can strongly affect the genetic structure of the island population by generating significant and long-lasting transient associations; (iii) with all else being equal, substantially greater admixture disequilibria are generally found with higher rates of seed migration into, or higher levels of self-fertilization within, the island population (with the possible exception of the heterozygote disequilibrium); (iv) pollen migration can either enhance or reduce the cytonuclear disequilibria caused by seed migration, or that due to mixed-mating in the absence of seed migration, but the effect is usually small and appears primarily to make a noticeable difference in predominantly outcrossing populations; and (v) pollen migration alone cannot generate even transient disequilibria de novo in populations with completely random associations. This same basic behavior is exhibited as long as there is some random outcrossing in the island population. Self-fertilized populations represent a special case, however, in that they are necessarily closed to pollen migration, and nonzero disequilibria can be maintained even in the absence of seed migration. All of these general results hold whether the population is censused as adults or as seeds, but the ability to detect nonrandom cytonuclear associations can depend strongly on the life stage censused in populations with a significant level of random outcrossing. We suggest how these models might be used for the estimation of seed and pollen migration.     

Realized gene flow within mixed stands of Quercus robur L. and Q. petraea (Matt.) L. revealed at the stage of naturally established seedling

The estimates of contemporary gene flow assessed based on naturally established seedlings provide information much needed for understanding the abilities of forest tree populations to persist under global changes through migration and/or adaptation facilitated by gene exchange among populations. Here, we investigated pollen‐ and seed‐mediated gene flow in two mixed‐oak forest stands (consisting of Quercus robur L. and Q. petraea [Matt.] Liebl.). The gene flow parameters were estimated based on microsatellite multilocus genotypes of seedlings and adults and their spatial locations within the sample plots using models that attempt to reconstruct the genealogy of the seedling cohorts. Pollen and seed dispersal were modelled using the standard seedling neighbourhood model and a modification—the 2‐component seedling neighbourhood model, with the later allowing separation of the dispersal process into local and long‐distance components. The 2‐component model fitted the data substantially better than the standard model and provided estimates of mean seed and pollen dispersal distances accounting for long‐distance propagule dispersal. The mean distance of effective pollen dispersal was found to be 298 and 463 m, depending on the stand, while the mean distance of effective seed dispersal was only 8.8 and 15.6 m, which is consistent with wind pollination and primarily seed dispersal by gravity in Quercus. Some differences observed between the two stands could be attributed to the differences in the stand structure of the adult populations and the existing understory vegetation. Such a mixture of relatively limited seed dispersal with occasional long distance gene flow seems to be an efficient strategy for colonizing new habitats with subsequent local adaptation, while maintaining genetic diversity within populations.     

The effect of volcanism on postglacial migration and seed dispersal. A case study in southern South America

During the Quaternary, southern South American temperate forests were confined to small and isolated refugia. Recolonization could be related not only with location of refugia but also with postglacial phenomena like volcanism, which could have interrupted the expansion of the forests. The aim of this study was to analyze the local effect of volcanism during the postglacial migration of Nothofagus nervosa in a particular region of Argentina were convergence of two migratory routes was suggested. The main question is whether admixture occurred or not and if the current populations are connected by pollen or seed gene flow. Two populations separated by a 3-km-width lava flow were sampled. Buds from 30 individuals of each of the two populations and from a total of 142 juveniles were analyzed. Genetic variation was detected through maternally inherited chloroplast deoxyribonucleic acid (cpDNA; polymerase chain reaction restriction fragment length polymorphisms of two fragments) and nuclear markers like isozymes (six loci) and simple sequence repeats (three loci). Population genetic parameters were estimated and the existence of a genetic structure was tested with an analysis of molecular variance. Historical gene flow was estimated through the indirect method of the genetic differentiation (F _ST). Chloroplast DNA revealed a total genetic differentiation between the two populations indicating completely isolation respecting seed gene flow. On the contrary, the degree of genetic differentiation for the nuclear markers was significantly lower, and moderate levels of historical gene flow through pollen were inferred. The results suggest that in this area, volcanism has played an important local role during the expansion of N. nervosa maintaining these two populations separated. Communicated by A. Kremer     

Seed and pollen flow and cline discordance among genes with different modes of inheritance

The relationships between seed and pollen flow and cline discordance/concordance between cytoplasmic and nuclear genes, with the incorporation of the effects of natural selection, are formulated for one locus with two alleles, under assumptions of random mating, no drift and no mutation. Results show that under certain conditions, the relative roles of seed and pollen flow in shaping cline discordance/ concordance are very similar to their roles in influencing population differentiation for selectively neutral markers with different modes of inheritance. Where the disequilibria between cytoplasmic and nuclear genes are of the order similar to selection coefficient, cline discordance/concordance can be predicted from the relative values of the ratio of pollen to seed flow and the ratio of selection coefficients. Where the disequilibria attained by seed and pollen flow are significant, the integrated cytonuclear data are recommended for cline analysis. In both cases, the relative rates of selection coefficients between cytoplasmic and nuclear genes can be roughly estimated according to their characteristic length.     

Fine-scale genetic structure and gene dispersal inferences in 10 neotropical tree species

The extent of gene dispersal is a fundamental factor of the population and evolutionary dynamics of tropical tree species, but directly monitoring seed and pollen movement is a difficult task. However, indirect estimates of historical gene dispersal can be obtained from the fine-scale spatial genetic structure of populations at drift-dispersal equilibrium. Using an approach that is based on the slope of the regression of pairwise kinship coefficients on spatial distance and estimates of the effective population density, we compare indirect gene dispersal estimates of sympatric populations of 10 tropical tree species. We re-analysed 26 data sets consisting of mapped allozyme, SSR (simple sequence repeat), RAPD (random amplified polymorphic DNA) or AFLP (amplified fragment length polymorphism) genotypes from two rainforest sites in French Guiana. Gene dispersal estimates were obtained for at least one marker in each species, although the estimation procedure failed under insufficient marker polymorphism, limited sample size, or inappropriate sampling area. Estimates generally suffered low precision and were affected by assumptions regarding the effective population density. Averaging estimates over data sets, the extent of gene dispersal ranged from 150 m to 1200 m according to species. Smaller gene dispersal estimates were obtained in species with heavy diaspores, which are presumably not well dispersed, and in populations with high local adult density. We suggest that limited seed dispersal could indirectly limit effective pollen dispersal by creating higher local tree densities, thereby increasing the positive correlation between pollen and seed dispersal distances. We discuss the potential and limitations of our indirect estimation procedure and suggest guidelines for future studies.     

Long-Distance Dispersal by Sea-Drifted Seeds Has Maintained the Global Distribution of Ipomoea pes-caprae subsp. brasiliensis (Convolvulaceae)

Ipomoea pes-caprae (Convolvulaceae), a pantropical plant with sea-drifted seeds, is found globally in the littoral areas of tropical and subtropical regions. Unusual long-distance seed dispersal has been believed to be responsible for its extraordinarily wide distribution; however, the actual level of inter-population migration has never been studied. To clarify the level of migration among populations of I. pes-caprae across its range, we investigated nucleotide sequence variations by using seven low-copy nuclear markers and 272 samples collected from 34 populations that cover the range of the species. We applied coalescent-based approaches using Bayesian and maximum likelihood methods to assess migration rates, direction of migration, and genetic diversity among five regional populations. Our results showed a high number of migrants among the regional populations of I. pes-caprae subsp. brasiliensis, which suggests that migration among distant populations was maintained by long-distance seed dispersal across its global range. These results also provide strong evidence for recent trans-oceanic seed dispersal by ocean currents in all three oceanic regions. We also found migration crossing the American continents. Although this is an apparent land barrier for sea-dispersal, migration between populations of the East Pacific and West Atlantic regions was high, perhaps because of trans-isthmus migration via pollen dispersal. Therefore, the migration and gene flow among populations across the vast range of I. pes-caprae is maintained not only by seed dispersal by sea-drifted seeds, but also by pollen flow over the American continents. On the other hand, populations of subsp. pes-caprae that are restricted to only the northern part of the Indian Ocean region were highly differentiated from subsp. brasiliensis. Cryptic barriers that prevented migration by sea dispersal between the ranges of the two subspecies and/or historical differentiation that caused local adaptation to different environmental factors in each region could explain the genetic differentiation between the subspecies.     

种子与花粉的随机迁移对植物群体遗传结构分化的影响

将Ｗｒｉｇｈｔ的经典岛屿模型拓广到植物群体上,同时考虑了含有花粉和种子随机迁移的影响。并给出了３种不同遗传方式的基因（双亲遗传,父本和母本遗传）频率的期望均值和方差。理论结果证明花粉或种子的随机迁移可增加基因频率方差,其幅度取决于迁移率和迁移基因频率的方差。同绝对迁移率一样,花粉和种子的迁移率方差及迁移基因频率的方差对群体遗传结构的分化有着同样的重要。一个重要结论就是花粉或种子的随机迁移率和随机迁     

Gene flow and the measurement of dispersal in plant populations

Despite theoretical assumptions, estimates of dispersal distance in natural plant populations have only recently been undertaken. Since plants are non-motile, gene flow depends on the dispersal of pollen and seed. Methods of estimating pollen and seed dispersal are reviewed and their implications for studies of evolutionary processes discussed. Practical advice is provided for designing exercises suitable for estimating dispersal distance in natural plant populations.     

The spatial genetic structure of cytoplasmic (cpDNA) and nuclear (allozyme) markers within and among populations of the gynodioecious Thymus vulgaris (Labiatae) in southern France

Recent advances in molecular biology have allowed the development of techniques to contrast spatial differentiation in nuclear and cytoplasmic genes and thus provide important data on relative levels of gene flow by pollen and seed in higher plants. In this paper, we compare the spatial structure of nuclear (allozymes) and cytoplasmic (cpDNA) genes among populations of the gynodioecious Thymus vulgaris in southern France. Based on a combination of three restriction enzymes (CfoI, EcoRV, and PstI), eight chlorotypes (combination of three restriction enzyme patterns revealed by Southern hybridization of Beta vulgaris cpDNA) were identified in the 13 studied populations. One chlorotype was particularly abundant and was detected in nearly all populations. Only one chlorotype was specific to a single population. Up to four different chlorotypes were observed in some populations. An FST of 0.238 (P < 0.002) for cpDNA haplotypes indicates spatial structure of cytoplasmic genes among the studied populations. Similar patterns were found within a single young population (CAB) structured in patches and surrounded by a continuous cover of T. vulgaris where the FST is 0.546 (P < 0.002). No significant correlation between sex and chlorotype nor between cpDNA diversity and female frequency was detected. Allozyme markers showed markedly less spatial structure (FST = 0.021 among populations and 0.019 in the CAB population, P < 0.001). This difference between cpDNA and nuclear allozyme markers suggests that pollen dispersal is more important than seed dispersal both among and within populations.     

Migration load in plants: role of pollen and seed dispersal in heterogeneous landscapes

Evolution of local adaptation depends critically on the level of gene flow, which, in plants, can be due to either pollen or seed dispersal. Using analytical predictions and individual-centred simulations, we investigate the specific influence of seed and pollen dispersal on local adaptation in plant populations growing in patchy heterogeneous landscapes. We study the evolution of a polygenic trait subject to stabilizing selection within populations, but divergent selection between populations. Deviations from linkage equilibrium and Hardy-Weinberg equilibrium make different contributions to genotypic variance depending on the dispersal mode. Local genotypic variance, differentiation between populations and genetic load vary with the rate of gene flow but are similar for seed and pollen dispersal, unless the landscape is very heterogeneous. In this case, genetic load is higher in the case of pollen dispersal, which appears to be due to differences in the distribution of genotypic values before selection.     

Inbreeding depression and heterosis in a subdivided population: influence of the mating system

We investigate the joint effects of gene flow and selfing on the level of inbreeding depression, heterosis and genetic load in a subdivided population at equilibrium. Low gene flow reduces inbreeding depression and substantially increases heterosis. However, in highly self-fertilizing populations, inbreeding depression is independent of the amount of gene flow. When migration occurs via pollen, consanguinity of the reproductive system could have a negative influence on subpopulation persistence, in contrast to the case of isolated populations. However, with only seed migration, genetic load and heterosis depend mildly on the mating system. From an evolutionary point of view, we reach two main conclusions: first, outcrossing is selected for if gene flow is low; second, intermediate levels of gene flow could promote mixed mating systems, especially when migration occurs through pollen.