Small-scale Spatial Genetic Structure Research Articles

Wind pollination over 70 years reduces the negative genetic effects of severe forest fragmentation in the tropical oak Quercus bambusifolia.

Whether wind pollination in trees can offset the negative genetic consequences of anthropogenic forest fragmentation is not clearly established. To answer this question, we examined the demographic genetics of Quercus bambusifolia over a 70-year recovery period in highly fragmented forests in Hong Kong. We sampled 1138 individuals from 37 locations, and genetically analysed the chronosequence through the classification of tree diameters from the same populations using 13 microsatellite markers. Our study reveals that severe fragmentation caused a significant genetic bottleneck with very few remaining but genetically diverse individuals. We observed an enhanced genetic diversity during demographic recovery. We found full-sibs within populations and half-sibs across the study range. This reflects a limited seed dispersal and extensive pollen flow. Despite reduced genetic structure both among and within populations, overall a strong persisting genetic differentiation (F'ST = 0.240, P < 0.01) and significant small-scale spatial genetic structure (F(1) = 0.13, Sp = 0.024, P < 0.01) were observed. Existing bottlenecks and low effective population sizes within the temporal chronosequence suggest that the long-term effect of severe fragmentation cannot be entirely eliminated by wind pollination with demographic recovery in the absence of effective seed dispersal. Our results lead to recommendations for forest management.

Differential role of a persistent seed bank for genetic variation in early vs. late successional stages.

Persistent seed banks are predicted to have an important impact on population genetic processes by increasing effective population size and storing past genetic diversity. Accordingly, persistent seed banks may buffer genetic effects of disturbance, fragmentation and/or selection. However, empirical studies surveying the relationship between aboveground and seed bank genetics under changing environments are scarce. Here, we compared genetic variation of aboveground and seed bank cohorts in 15 populations of the partially cleistogamous Viola elatior in two contrasting early and late successional habitats characterized by strong differences in light-availability and declining population size. Using AFLP markers, we found significantly higher aboveground than seed bank genetic diversity in early successional meadow but not in late successional woodland habitats. Moreover, individually, three of eight woodland populations even showed higher seed bank than aboveground diversity. Genetic differentiation among populations was very strong (фST = 0.8), but overall no significant differentiation could be detected between above ground and seed bank cohorts. Small scale spatial genetic structure was generally pronounced but was much stronger in meadow (Sp-statistic: aboveground: 0.60, seed bank: 0.32) than in woodland habitats (aboveground: 0.11; seed bank: 0.03). Our findings indicate that relative seed bank diversity (i.e. compared to aboveground diversity) increases with ongoing succession and despite decreasing population size. As corroborated by markedly lower small-scale genetic structure in late successional habitats, we suggest that the observed changes in relative seed bank diversity are driven by an increase of outcrossing rates. Persistent seed banks in Viola elatior hence will counteract effects of drift and selection, and assure a higher chance for the species’ long term persistence, particularly maintaining genetic variation in declining populations of late successional habitats and thus enhancing success rates of population recovery after disturbance events.

Breeding system, gene dispersal and small-scale spatial genetic structure of a threatened food tree species, Pentadesma butyracea (Clusiaceae) in Benin

Pentadesma butyracea Sabine, a rain forest food tree species, plays a vital role in the socio-economic livelihood of some West African rural communities due to its various products. However, its scattered populations are threatened in Benin. Defining appropriate conservation strategies requires a good knowledge of mating patterns and their consequences for population genetics. The outcrossing rate, levels of correlated paternity and fine-scale spatial genetic structure of adults and maternal sibships were estimated for one small population and three large populations in Benin using microsatellite markers. Similar outcrossing rates (88–95%) were found in all populations, showing that P. butyracea is mainly an outbreeding species. We found no evidence of inbreeding depression from a decay of inbreeding with age. The spatial genetic structure within the large populations (Sp statistic = 0.003–0.038) was consistent with isolation-by-distance expectations, showing that gene dispersal is spatially limited. Limited pollen dispersal is highlighted by the decay of the degree of correlated paternity between sibships with spatial distance. The mean pollen dispersal distance was estimated between 50 m and 450 m, but up to 21% pollen may migrate from external sources. The smallest population displayed slightly higher correlated paternity than the large populations (r p = 0.37 vs. r p = 0.17–0.30). In conclusion, our results suggest that small populations may show a reduction in sire numbers in seed, while the fragmented populations, large and small, are connected through gene flow. There is little inbreeding and no evidence of inbreeding depression.

Euglossine bees mediate only limited long-distance gene flow in a tropical vine.

Euglossine bees (Apidae: Euglossini) have long been hypothesized to act as long-distance pollinators of many low-density tropical plants. We tested this hypothesis by the analysis of gene flow and genetic structure within and among populations of the euglossine bee-pollinated vine Dalechampia scandens. Using microsatellite markers, we assessed historical gene flow by the quantification of regional-scale genetic structure and isolation by distance among 18 populations, and contemporary gene flow by the estimation of recent migration rates among populations. To assess bee-mediated pollen dispersal on a smaller scale, we conducted paternity analyses within a focal population, and quantified within-population spatial genetic structure in four populations. Gene flow was limited to certain nearby populations within continuous forest blocks, whereas drift appeared to dominate on larger scales. Limited long-distance gene flow was supported by within-population patterns; gene flow was biased towards nearby plants, and significant small-scale spatial genetic structure was detected within populations. These findings suggest that, although female euglossine bees might be effective at moving pollen within populations, and perhaps within forest blocks, their contribution to gene flow on the regional scale seems too limited to counteract genetic drift in patchily distributed tropical plants. Among-population gene flow might have been reduced following habitat fragmentation.

Clonality increases with snow depth in the arctic dwarf shrub Empetrum hermaphroditum.

Vegetative reproduction and spread through clonal growth plays an important role in arctic-alpine ecosystems with short cool growing seasons. Local variation in winter snow accumulation leads to discrete habitat types that may provide divergent conditions for sexual and vegetative reproduction. Therefore, we studied variation in clonal structure of a dominant, evergreen, dwarf shrub (Empetrum nigrum s.l. with the two taxa E. nigrum L. s.s. and E. hermaphroditum Hagerup) along a snow cover gradient and compared clonal diversity and spatial genetic structure between habitats. We studied 374 individual shoots using 105 polymorphic AFLP markers and analyses based on hierarchical clustering, clonal diversity indices, and small-scale spatial genetic structure with pairwise kinship coefficient. We used two approaches to define a threshold of genotypic distance between two samples that are considered the same clone. Clonality was examined among three habitats (exposed ridges, sheltered depressions, birch forest) differing in snow conditions replicated in four study regions in Norway and Sweden. Clonality of E. hermaphroditum differed between habitats with an increase in clonal diversity with decreasing snow depth. Small-scale spatial genetic structure increased with decreasing clonal diversity and increasing clone size. In three study regions, E. hermaphroditum was the only species, whereas in one region E. nigrum also occurred, largely confined to exposed ridges. Our results demonstrated that snow cover in conjunction with associated habitat conditions plays an important role for the mode of propagation of the dwarf shrub E. hermaphroditum.

Hidden founder effects: small-scale spatial genetic structure in recently established populations of the grassland specialist plant Anthyllisvulneraria.

The long-term establishment success of founder plant populations has been commonly assessed based on the measures of population genetic diversity and among population genetic differentiation, with founder populations expected to carry sufficient genetic diversity when population establishment is the result of many colonists from multiple source populations (the 'migrant pool' colonization model). Theory, however, predicts that, after initial colonization, rapid population expansion may result in a fast increase in the extent of spatial genetic structure (SGS), independent of extant genetic diversity. This SGS can reduce long-term population viability by increasing inbreeding. Using 12 microsatellite markers, we inferred colonization patterns in four recent populations of the grassland specialist plant Anthyllisvulneraria and compared the extent of SGS between recently established and old populations. Assignment analyses of the individuals of recent population based on the genetic composition of nine adjacent putative source populations suggested the occurrence of the 'migrant pool' colonization model, further confirmed by high genetic diversity within and low genetic differentiation among recent populations. Population establishment, however, resulted in the build-up of strong SGS, most likely as a result of spatially restricted recruitment of the progeny of initial colonists. Although reduced, significant SGS was nonetheless observed to persist in old populations. The presence of SGS was in all populations associated with elevated inbreeding coefficients, potentially affecting the long-term viability of these populations. In conclusion, this study illustrates the importance of studying SGS next to population genetic diversity and differentiation to adequately infer colonization patterns and long-term establishment success of plant species.

Transmission of genetic variation from the adult generation to naturally established seedling cohorts in small forest stands of pedunculate oak (Quercus robur L.)

Natural regeneration is being increasingly encouraged as the preferred regeneration method for sustainable forestry. However, the benefits of natural regeneration may be jeopardized in small and low-density forest stands, as genetic drift and inbreeding may reduce genetic diversity of the standing population. Particularly in light-demanding tree species, which are characterized by a narrow recruitment window, conservation of genetic diversity during natural regeneration can be challenging in small forest stands. In this study, we investigated intergenerational transmission of genetic diversity in stands of the light-demanding tree species pedunculate oak (Quercus robur L.) by comparing genetic diversity between adults and recently established seedling cohorts (1–3years old) in four small stands of Q. robur (<4.5ha) that varied in tree density. We also quantified mating patterns and gene flow to investigate their role in shaping the genetic diversity and spatial genetic structure of the studied populations. Because of the closed canopy cover of these stands, only recently established seedlings could be studied. When all stands were pooled, the adult cohort showed a slightly but significantly higher allelic richness (Ar) than the established seedling cohort (Ar=11.5 and 10.7, respectively). However, at the stand level, no significant negative effects on the genetic diversity of the offspring generation were found in the small and low-density forest stands. As expected, acorn dispersal resulting in seedling recruitment was restricted to a few meters from mother trees, resulting in significant small-scale spatial genetic structure in the offspring. Pollen inflow from outside the study plots varied strongly among stands, but all plots showed a significant correlated paternity (rp), with higher estimates of rp found in forest stands with lower effective population sizes (Ne) and lower tree densities. Given that high rp-levels may increase the probability of biparental inbreeding and may incur fitness costs in subsequent offspring generations, we recommend that in small scale forestry of Q. robur, Ne and tree densities should be sufficiently large to maintain genetic diversity over the long term. Allowing gene flow between tree populations through reducing the spatial isolation among forest stands, can help to increase Ne in small-scale silvicultural systems of pedunculate oak, but also in other species characterized by narrow recruitment windows.

Habitat fragmentation and the genetic structure of the Amazonian palm Mauritia flexuosa L.f. (Arecaceae) on the island of Trinidad

Studies of small-scale spatial genetic structure are crucial to the implementation of successful conservation and management plans as they enhance our capacity to predict a population’s ability to respond to changing environments. This is especially true in the tropics, where high rates of fragmentation and land-use change create potential barriers to genetic exchanges. We examined the genetic diversity of wild populations of the economically important palm, Mauritia flexuosa (Arecaceae) in and around the Aripo Savannas Scientific Reserve on the island of Trinidad. In a small collection area of roughly 10 km2 we found both spatial and inter-generational, or temporal, genetic differentiation and high levels of nearest-neighbor mating. We suggest that these spatial and temporal genetic patterns reflect recent and drastic anthropogenic changes to the landscape of the study sites, which we hypothesize have created barriers to gene flow through animal-mediated seed dispersal and pollination.

Species diversity and population density affect genetic structure and gene dispersal in a subtropical understory shrub

Aims The dispersal of pollen and seeds is spatially restricted and may vary among plant populations because of varying biotic interactions, population histories or abiotic conditions. Because gene dispersal is spatially restricted, it will eventually result in the development of spatial genetic structure (SGS), which in turn can allow insights into gene dispersal processes. Here, we assessed the effect of habitat characteristics like population density and community structure on small-scale SGS and estimate historical gene dispersal at different spatial scales. Methods In a set of 12 populations of the subtropical understory shrub Ardisia crenata, we assessed genetic variation at 7 microsatellite loci within and among populations. We investigated small-scale genetic structure with spatial genetic autocorrelation statistics and heterogeneity tests and estimated gene dispersal distances based on population differentiation and on within-population SGS. SGS was related to habitat characteristics by multiple regression.

Floodplain willows in fragmented river landscapes: Understanding spatio-temporal genetic patterns as a basis for restoration plantings

In Central Europe, floodplain fragmentation by dykes and river regulation by dams has led to a fundamental loss of riparian softwood forests and dramatically restricted natural regeneration of the Salicaceae species involved. As a consequence, reforestation is one of the widely-used measures to maintain this valuable vegetation type. Knowledge about the genetic population structure of existing stands of willows and poplars is necessary to preserve their genetic potential in the long term. In this study, we investigated clonal and genetic diversity patterns of Salix viminalis for 23 stands, taking into account young and old age classes and locations in front of the dykes in the active floodplain and behind the dykes in the inactive floodplain along the Elbe River, Germany. Microsatellites were used to assess effects of stand and floodplain fragmentation and to evaluate the extent of clonal structures. We detected considerable numbers of multi-ramet-clones almost exclusively in the active floodplain with old stands exhibiting the largest number of these clones. Individual clones mostly covered distances of less than 10m, but single long distance dispersal events of vegetative propagules were also detected. Genetic diversity patterns revealed one continuous population although a certain small-scale spatial genetic structure was identified. Our study suggests that riparian softwood forest species have efficient dispersal strategies which allow the population to survive altered floodplain conditions from a genetic point of view. Management advice is given for selecting genetically suitable planting material for restoration purposes.

Spatial autocorrelation: an overlooked concept in behavioral ecology

Spatial autocorrelation (SAC) is the dependence of a given variable’s values on the values of the same variable recorded at neighboring locations (Cliff and Ord 1973; Fortin and Dale 2005). When high values are associated with relatively high values at neighboring locations, SAC is said to be positive and, conversely, where high values correspond to relatively low values at neighboring locations, SAC is negative. SAC can be a property of the variable itself (inherent or intrinsic SAC) or it can arise due to the dependence of the variable of interest on another spatially autocorrelated variable (induced SAC) (Legendre et al. 2002; Fortin and Dale 2005). Because it lies at the core of most spatial models, SAC is a fundamental concept of spatial analysis (Getis 2008). During the last 2 decades, mostly after Pierre Legendre published his seminal paper ‘‘Spatial autocorrelation: trouble or new paradigm’’ (Legendre 1993), SAC received considerable attention from ecologists—in particular biogeographers investigating macroecological patterns of species distributions (Kissling and Carl 2008)—and from population geneticists investigating small-scale spatial genetic structure of populations (Guillot et al. 2009). These circumstances prompted Arthur Getis, in a review on the evolution of the SAC concept, to conclude that ‘‘Nearly all the major journals that concern themselves with the ecological aspects of their subjects print articles having a spatial autocorrelation foundation’’ (Getis 2008). In stark contrast, the issue of SAC has hitherto been largely ignored in behavioral ecology, despite the fact that many studies in this field deal with a spatial component. Thus, despite its recognized importance in adjacent fields of ecological research, even very basic topics in behavioral ecology remain unexplored with respect to SAC, and we could only find a handful of studies (van der Jeugd and McCleery 2002; Laiolo and Tella 2006; Duraes et al. 2007; Aarts et al. 2008; Giesselmann et al. 2008; Holdo et al. 2009), which included SAC in their research paradigm. The general aim of this paper is to draw the attention of behavioral ecologists to the phenomenon of SAC. Specifically, we aim 1) to provide examples of spatially autocorrelated variables, indicating that SAC is widespread in variables commonly used in behavioral ecology studies, 2) to show why it is important to take SAC into account, and 3) to point to some tools to explore and model it.

Small-scale spatial genetic structure in Scopalina lophyropoda, an encrusting sponge with philopatric larval dispersal and frequent fission and fusion events

Insight from the spatial genetic structure (SGS) of a species is fundamental to under- standing the patterns of effective dispersal and gene flow among its populations. Despite the ecolog- ical importance of sponges and the variety of reproduction and dispersal strategies they present, which can strongly influence SGS, there is only 1 study assessing small-scale SGS in sponges. That species had a continuous distribution and relatively wide-scale larval dispersal. Here we study the contribution of sexual and asexual reproduction, and the breeding and mating system to the SGS of a sponge species, Scopalina lophyropoda, with a patchy distribution and more limited larval disper- sal. All individuals from 3 populations were mapped and genetically characterised for 7 microsatel- lite loci. The extent of clonality was minor (ca. 7%), possibly caused by a balance between fissions and fusions. The scarce clonality did not contribute to the SGS, which was analysed by autocorrela- tion statistics at both the ramet (including clones) and the genet (excluding clones) levels. The spatial autocorrelation analyses elicited a pattern of strong SGS at the small scale, confirming the predic- tions of philopatric larval dispersal, which fosters isolation by distance. All these patterns, however, contrast with the conspicuous lack of inbreeding detected in the populations, which is in agreement with recent data on other marine modular invertebrates and confirms that strong SGS does not necessarily imply inbreeding.

Small-scale spatial genetic structure in an ant species with sex-biased dispersal

In a population of the monogynous, polyandrous ant Cataglyphis cursor, we analysed the spatial genetic structure of queens, colony fathers and workers at a microgeographical scale to infer the extent of sex-biased dispersal and to assess the impact of limited dispersal on the patterns of relatedness within the colony. To this end, four microsatellite markers were scored for the queen and an average of 26 workers from each of 35 mapped colonies. We used pair-wise kinship coefficients between all pairs of genotypes, including the reconstructed colony father genotypes (1) to test and quantify isolation by distance patterns within each sex or caste through the analysis of kinship–distance curves, and (2) to compute the average relatedness between categories of colony members. The kinship–distance curve was much steeper for colony queens than colony fathers, indicating male-biased dispersal. However, colony fathers also displayed a non-random spatial genetic structure, so that even males show some dispersal limitation at the scale of the population, which extends over less than 250 m. The degree of relatedness between the different sexes and castes of colonies was well predicted from the number of mates per queen and the inbreeding of queens, and the impact of limited dispersal was very weak at this scale of observation. We discuss the interest of kinship–distance curves to assess sex-biased dispersal on a local scale and we compare our results with large-scale analyses of genetic structure in Cataglyphis cursor and other monogynous ant species.

Genetic structure of the subtidal red alga Delisea pulchra

We used random amplified polymorphic DNA (RAPDs) to examine small-scale spatial genetic structure in the red alga Delisea pulchra (Greville) Montagne at two locations near Sydney, Australia. We examined genetic structure among plants at four spatial scales ranging from 2 km apart down to <50 cm apart between locations, among sites within locations, among quadrats within sites, and among plants within quadrats. Haploid stages of D. pulchra were absent from the populations studied, suggesting that they are maintained through asexual reproduction of diploid plants. Consistent with this, we found that 19 RAPD phenotypes scored in this study had multiple individuals, indicating the presence of clones in these populations. However, there were no RAPD phenotypes common to two locations separated by only 2 km. Analysis of molecular variance revealed that strong genetic differences occurred between plants from these two locations, with 46.3% of the total genetic variation occurring at this scale, most probably reflecting limited gene flow. Within each location, <25% of the genetic variation was attributable to differences among sites or quadrats, indicating gene flow at those smaller scales. Most of the variation within each location occurred at the smallest spatial scale, among plants within 0.25 m2 quadrats. Nonetheless, some pairwise genetic distances (φST) between sites or quadrats within locations were large, indicating some genetic divergence on smaller scales. Genetic distance was independent of spatial distance within both locations, suggesting that fine-scale differences within locations were most probably caused by variation in fine-scale patterns of water movement or fine-scale natural selection. We assessed the impact of one potential selective agent, grazing sea urchins, on the fine-scale genetic structure of D. pulchra. There was no evidence that grazing by sea urchins affected the genetic structure of D. pulchra. In combination with demographic data, our results indicated that local populations of D. pulchra within locations were relatively open and that fine-scale genetic structure was probably constrained by gene flow. At the larger scale however, strong genetic differentiation indicated little gene flow between locations and restricted dispersal of spores.