Fine-scale spatial genetic structure and gene dispersal in Silene latifolia

Plants are sessile organisms, often characterized by limited dispersal. Seeds and pollen are the critical stages for gene flow. Here we investigate spatial genetic structure, gene dispersal and the relative contribution of pollen vs seed in the movement of genes in a stable metapopulation of the white campion Silene latifolia within its native range. This short-lived perennial plant is dioecious, has gravity-dispersed seeds and moth-mediated pollination. Direct measures of pollen dispersal suggested that large populations receive more pollen than small isolated populations and that most gene flow occurs within tens of meters. However, these studies were performed in the newly colonized range (North America) where the specialist pollinator is absent. In the native range (Europe), gene dispersal could fall on a different spatial scale. We genotyped 258 individuals from large and small (15) subpopulations along a 60 km, elongated metapopulation in Europe using six highly variable microsatellite markers, two X-linked and four autosomal. We found substantial genetic differentiation among subpopulations (global F_ST=0.11) and a general pattern of isolation by distance over the whole sampled area. Spatial autocorrelation revealed high relatedness among neighboring individuals over hundreds of meters. Estimates of gene dispersal revealed gene flow at the scale of tens of meters (5–30 m), similar to the newly colonized range. Contrary to expectations, estimates of dispersal based on X and autosomal markers showed very similar ranges, suggesting similar levels of pollen and seed dispersal. This may be explained by stochastic events of extensive seed dispersal in this area and limited pollen dispersal.     

New interpretations of fine-scale spatial genetic structure

Recent methodological advances permit refined inferences of evolutionary processes from the fine-scale spatial genetic structure of plant populations. In this issue of Molecular Ecology, Born et al. (2008) exploit the full power of these methods by examining effects of ancient and recent landscape histories in an African rainforest tree species. The authors first detected admixture of distinct gene pools that may have formed in Pleistocene forest refuges. Then, comparing across six study populations in Gabon, the authors found similar patterns of fine-scale spatial genetic structure despite natural and anthropogenic variation in population density. The latter results suggest that enhanced gene dispersal may compensate for low population densities in fragmented landscapes.     

Effects of zoochory on the spatial genetic structure of plant populations

Spatial genetic structure (SGS) of plants results from the nonrandom distribution of related individuals. SGS provides information on gene flow and spatial patterns of genetic diversity within populations. Seed dispersal creates the spatial template for plant distribution. Thus, in zoochorous plants, dispersal mode and disperser behaviour might have a strong impact on SGS. However, many studies only report the taxonomic group of seed dispersers, without further details. The recent increase in studies on SGS provides the opportunity to review findings and test for the influence of dispersal mode, taxonomic affiliation of dispersers and their behaviour. We compared the proportions of studies with SGS among groups and tested for differences in strength of SGS using Sp statistics. The presence of SGS differed among taxonomic groups, with reduced presence in plants dispersed by birds. Strength of SGS was instead significantly influenced by the behaviour of seed dispersal vectors, with higher SGS in plant species dispersed by animals with behavioural traits that result in short seed dispersal distances. We observed high variance in the strength of SGS in plants dispersed by animals that actively or passively accumulate seeds. Additionally, we found SGS was also affected by pollination and marker type used. Our study highlights the importance of vector behaviour on SGS even in the presence of variance created by other factors. Thus, more detailed information on the behaviour of seed dispersers would contribute to better understand which factors shape the spatial scale of gene flow in animal‐dispersed plant species.     

Inferring recruitment history from spatial genetic structure within populations of the colonizing tree Albizia julibrissin (Fabaceae)

Comparative analyses of spatial genetic structure (SGS) among species, populations, or cohorts give insight into the genetic consequences of seed dispersal in plants. We analysed SGS of a weedy tree in populations with known and unknown recruitment histories to first establish patterns in populations with single vs. multiple founders, and then to infer possible recruitment scenarios in populations with unknown histories. We analysed SGS in six populations of the colonizing tree Albizia julibrissin Durazz. (Fabaceae) in Athens, Georgia. Study sites included two large populations with multiple, known founders, two small populations with a single, known founder, and two large populations with unknown recruitment histories. Eleven allozyme loci were used to genotype 1385 individuals. Insights about the effects of colonization history from the SGS analyses were obtained from correlograms and Sp statistics. Distinct differences in patterns of SGS were identified between populations with multiple founders vs. a single founder. We observed significant, positive SGS, which decayed with increasing distance in the populations with multiple colonists, but little to no SGS in populations founded by one colonist. Because relatedness among individuals is estimated relative to a local reference population, which usually consists of those individuals sampled in the study population, SGS in populations with high background relatedness, such as those with a single founder, may be obscured. We performed additional analyses using a regional reference population and, in populations with a single founder, detected significant, positive SGS at all distances, indicating that these populations consist of highly related descendants and receive little seed immigration. Subsequent analyses of SGS in size cohorts in the four large study populations showed significant SGS in both juveniles and adults, probably because of a relative lack of intraspecific demographic thinning. SGS in populations of this colonizing tree is pronounced and persistent and is determined by the number and relatedness of founding individuals and adjacent seed sources. Patterns of SGS in populations with known histories may be used to indirectly infer possible colonization scenarios for populations where it is unknown.     

A heterogeneity test for fine-scale genetic structure

For organisms with limited vagility and/or occupying patchy habitats, we often encounter nonrandom patterns of genetic affinity over relatively small spatial scales, labelled fine-scale genetic structure. Both the extent and decay rate of that pattern can be expected to depend on numerous interesting demographic, ecological, historical, and mating system factors, and it would be useful to be able to compare different situations. There is, however, no heterogeneity test currently available for fine-scale genetic structure that would provide us with any guidance on whether the differences we encounter are statistically credible. Here, we develop a general nonparametric heterogeneity test, elaborating on standard autocorrelation methods for pairs of individuals. We first develop a 'pooled within-population' correlogram, where the distance classes (lags) can be defined as functions of distance. Using that pooled correlogram as our null-hypothesis reference frame, we then develop a heterogeneity test of the autocorrelations among different populations, lag-by-lag. From these single-lag tests, we construct an analogous test of heterogeneity for multilag correlograms. We illustrate with a pair of biological examples, one involving the Australian bush rat, the other involving toadshade trillium. The Australian bush rat has limited vagility, and sometimes occupies patchy habitat. We show that the autocorrelation pattern diverges somewhat between continuous and patchy habitat types. For toadshade trillium, clonal replication in Piedmont populations substantially increases autocorrelation for short lags, but clonal replication is less pronounced in mountain populations. Removal of clonal replicates reduces the autocorrelation for short lags and reverses the sign of the difference between mountain and Piedmont correlograms.     

Spatial correlations at different spatial scales are themselves highly correlated in isolation by distance processes

Although many properties of spatial autocorrelation statistics are well characterized, virtually nothing is known about possible correlations among values at different spatial scales, which ultimately would influence how inferences about spatial genetics are made at multiple spatial scales. This article reports the results of stochastic space-time simulations of isolation by distance processes, having a very wide range of amounts of dispersal for plants or animals, and analyses of the correlations among Moran's I-statistics for different mutually exclusive distance classes. In general, the stochastic correlations are extremely large (>0.90); however, the correlations bear a complex relationship with level of dispersal, spatial scale and spatial lag between distance classes. The correlations are so large that any existing or conceived statistical method that employs more than one distance class (or spatial scale) should not ignore them. This result also suggests that gains in statistical power via increasing sample size are limited, and that increasing numbers of assayed loci generally should be preferred. To the extent that sampling error for real data sets can be treated as white noise, it should be possible to account for stochastic correlations in formulating more precise statistical methods. Further, while the current results are for isolation by distance processes, they provide some guidance for some more complex stochastic space-time processes of landscape genetics. Moreover, the results hold for several popular measures other than Moran's I. In addition, in the results, the signal to noise ratios strongly decreased with distance, which also has several implications for optimal statistical methods using correlations at multiple spatial scales.     

Effect of sampling strategy on estimation of fine-scale spatial genetic structure in Androsace tapete (Primulaceae), an alpine plant endemic to Qinghai-Tibetan Plateau

The fine-scale spatial genetic structure (SGS) of alpine plants is receiving increasing attention, from which seed and pollen dispersal can be inferred. However, estimation of SGS may depend strongly on the sampling strategy,including the sample size and spatial sampling scheme. Here, we examined the effects of sample size and three spatial schemes, simple-random, line-transect, and random-cluster sampling, on the estimation of SGS in Androsace tapete, an alpine cushion plant endemic to Qinghai-Tibetan Plateau. Using both real data and simulated data of dominant molecular markers, we show that: (i) SGS is highly sensitive to sample strategy especially when the sample size is small (e.g., below 100); (ii) the commonly used SGS parameter (the intercept of the autocorrelogram) is more susceptible to sample error than a newly developed Sp statistic; and (iii) the random-cluster scheme is susceptible to obvious bias in parameter estimation even when the sample size is relatively large (e.g., above 200). Overall,the line-transect scheme is recommendable, in that it performs slightly better than the simple-random scheme in parameter estimation and is more efficient to encompass broad spatial scales. The consistency between simulated data and real data implies that these findings might hold true in other alpine plants and more species should be examined in future work.     

Comparative analysis of the within-population genetic structure in wild cherry (Prunus avium L.) at the self-incompatibility locus and nuclear microsatellites

Gametophytic self-incompatibility (SI) systems in plants exhibit high polymorphism at the SI controlling S-locus because individuals with rare alleles have a higher probability to successfully pollinate other plants than individuals with more frequent alleles. This process, referred to as frequency-dependent selection, is expected to shape number, frequency distribution, and spatial distribution of self-incompatibility alleles in natural populations. We investigated the genetic diversity and the spatial genetic structure within a Prunus avium population at two contrasting gene loci: nuclear microsatellites and the S-locus. The S-locus revealed a higher diversity (15 alleles) than the eight microsatellites (4-12 alleles). Although the frequency distribution of S-alleles differed significantly from the expected equal distribution, the S-locus showed a higher evenness than the microsatellites (Shannon's evenness index for the S-locus: E = 0.91; for the microsatellites: E = 0.48-0.83). Also, highly significant deviations from neutrality were found for the S-locus whereas only minor deviations were found for two of eight microsatellites. A comparison of the frequency distribution of S-alleles in three age-cohorts revealed no significant differences, suggesting that different levels of selection acting on the S-locus or on S-linked sites might also affect the distribution and dynamics of S-alleles. Autocorrelation analysis revealed a weak but significant spatial genetic structure for the multilocus average of the microsatellites and for the S-locus, but could not ascertain differences in the extent of spatial genetic structure between these locus types. An indirect estimate of gene dispersal, which was obtained to explain this spatial genetic pattern, indicated high levels of gene dispersal within our population (sigma(g) = 106 m). This high gene dispersal, which may be partly due to the self-incompatibility system itself, aids the effective gene flow of the microsatellites, thereby decreasing the contrast between the neutral microsatellites and the S-locus.     

Inverted patterns of genetic diversity in continental and island populations of the heather Erica scoparia s.l.

Aim Using the heather Erica scoparia s.l. as a model, this paper aims to test theoretical predictions that island populations are genetically less diverse than continental ones and to determine the extent to which island and continental populations are connected by pollen‐ and seed‐mediated gene flow. Location Macaronesia, Mediterranean, Atlantic fringe of Europe. Methods Patterns of genetic diversity are described based on variation at two chloroplast DNA (cpDNA) loci and one nuclear DNA (nDNA) locus for 109 accessions across the entire distribution range of the species. Global patterns of genetic differentiation were investigated using principal coordinates analysis. Genetic differentiation between island and continental areas, estimations of pollen‐ and seed‐mediated gene flow, and the presence of phylogeographical signal were assessed by means of F_st /N_ST (continental scale) and F_ij/N_ij (local scale). Extant and past distribution ranges of the species were inferred from niche modelling using layers describing present and Last Glacial Maximum (LGM) macroclimatic conditions. Results The Azores exhibited a significantly higher genetic diversity than the continent. The lowest levels of genetic differentiation were observed between the Azores and the western Mediterranean, and the diversity observed in the Azores resulted from at least two colonization waves. Within the Azores, kinship coefficients showed a significant and much steeper decrease with geographical distance in the cpDNA than in the nDNA. The distribution predicted by LGM models was markedly different from the current potential distribution, particularly in western Europe, where no suitable areas were predicted by LGM models, and along the Atlantic coast of the African continent, where LGM models predicted highly suitable climatic conditions. Main conclusions The higher diversity observed in Azorean than in continental populations is inconsistent with MacArthur and Wilson’s equilibrium model and derived theoretical population genetic expectations. This inverted pattern may be the result of extinction on the continent coupled with multiple island colonization events and subsequent allopatric diversification and lineage hybridization in the Azores. The results highlight the role of allopatric diversification in explaining diversification on islands and suggest that this process has played a much more significant role in shaping Azorean biodiversity than previously thought.