A microsatellite-based estimation of clonal diversity and population subdivision in Zostera marina, a marine flowering plant

We examined the genetic population structure in eelgrass (Zostera marina L.), the dominant seagrass species of the northern hemisphere, over spatial scales from 12 km to 10 000 km using the polymorphism of DNA microsatellites. Twelve populations were genotyped for six loci representing a total of 67 alleles. Populations sampled included the North Sea (four), the Baltic Sea (three), the western Atlantic (two), the eastern Atlantic (one), the Mediterranean Sea (one) and the eastern Pacific (one). Microsatellites revealed substantial genetic variation in a plant group with low allozyme diversity. Average expected heterozygosities per population (monoclonal populations excluded) ranged from 0.32 to 0.61 (mean = 0. 48) and allele numbers varied between 3.3 and 6.7 (mean = 4.7). Using the expected frequency of multilocus genotypes within populations, we distinguished ramets from genetic individuals (i.e. equivalent to clones). Differences in clonal diversity among populations varied widely and ranged from maximal diversity (i.e. all ramets with different genotype) to near or total monoclonality (two populations). All multiple sampled ramets were excluded from further analysis of genetic differentiation within and between populations. All but one population were in Hardy-Weinberg equilibrium, indicating that Zostera marina is predominantly outcrossing. From a regression of the pairwise population differentiation with distance, we obtained an effective population size Ne of 2440-5000. The overall genetic differentiation among eelgrass populations, assessed as rho (a standardized estimate of Slatkin's RST) was 0.384 (95% CI 0.34-0.44, P < 0.001). Genetic differentiation was weak among three North Sea populations situated 12-42 km distant from one another, suggesting that tidal currents result in an efficient exchange of propagules. In the Baltic and in Nova Scotia, a small but statistically significant fraction of the genetic variance was distributed between populations (rho = 0.029-0. 053) at scales of 15-35 km. Pairwise genetic differentiation between European populations were correlated with distance between populations up to a distance of 4500 km (linear differentiation-by-distance model, R2 = 0.67). In contrast, both Nova Scotian populations were genetically much closer to North Sea and Baltic populations than expected from their geographical distance (pairwise rho = 0.03-0.08, P < 0.01). A biogeographical cluster of Canadian with Baltic/North Sea populations was also supported using a neighbour-joining tree based on Cavalli-Sforza's chord distance. Relatedness between populations may be very different from predictions based on geographical vicinity.     

Range-edge genetic diversity: locally poor extant southern patches maintain a regionally diverse hotspot in the seagrass Zostera marina

Refugial populations at the rear edge are predicted to contain higher genetic diversity than those resulting from expansion, such as in post-glacial recolonizations. However, peripheral populations are also predicted to have decreased diversity compared to the centre of a species' distribution. We aim to test these predictions by comparing genetic diversity in populations at the limits of distribution of the seagrass Zostera marina, with populations in the species' previously described central diversity 'hotspot'. Zostera marina populations show decreased allelic richness, heterozygosity and genotypic richness in both the 'rear' edge and the 'leading' edge compared to the diversity 'hotspot' in the North Sea/Baltic region. However, when populations are pooled, genetic diversity at the southern range is as high as in the North Sea/Baltic region while the 'leading edge' remains low in genetic diversity. The decreased genetic diversity in these southern Iberian populations compared to more central populations is possibly the effect of drift because of small effective population size, as a result of reduced habitat, low sexual reproduction and low gene flow. However, when considering the whole southern edge of distribution rather than per population, diversity is as high as in the central 'hotspot' in the North Sea/Baltic region. We conclude that diversity patterns assessed per population can mask the real regional richness that is typical of rear edge populations, which have played a key role in the species biogeographical history and as marginal diversity hotspots have very high conservation value.     

Fitness‐consequences of geitonogamous selfing in a clonal marine angiosperm (Zostera marina)

Plant mating systems have received considerable attention because the proportion of selfed vs. outcrossed progeny is an important evolutionary factor. In clonally reproducing plants, geitonogamous selfing between distant ramets belonging to the same genet is expected to be widespread, yet empirical data are sparse. Nothing is known about between‐ramet selfing in aquatic flowering plants with subaqueous pollen transfer, most of which display pronounced clonal reproduction. From two locations in the western Baltic Sea, I present data on the effects of patch isolation and clonal diversity on the outcrossing rate of eelgrass, Zostera marina L., based on the genotypes of maternal plants and recently fertilized ovules scored at eight microsatellite loci. There were no differences in outcrossing rates between vegetation patches and continuous meadow although patches were nearly always composed of single genets. Quantitative effects of clonal diversity were present in the continuous vegetation where a significant positive correlation between genet diversity and the proportion of outcrossed offspring was detected (Kendall’s τ=0.82, P=0.0017). On a population‐scale as well, the genotypic diversity was positively correlated with outcrossing. The relative fitness of selfed offspring was low (ω ± 95% confidence interval=0.56 ± 0.032 and 0.322 ± 0.15) indicating that geitonogamy incurred substantial fitness costs. Selfing rates in Z. marina may not be in evolutionary equilibrium because of spatial and temporal heterogeneity of clonal size and diversity. The high prevalence of dioecy in seagrasses may have evolved to avoid the fitness costs associated with geitonogamy.     

Twentyfive years of changes in the distribution and biomass of eelgrass,Zostera marina,in Grevelingen lagoon,The Netherlands

The wax and wane of the eelgrass (Zostera marina L.) population in Grevelingen lagoon (East Atlantic; The Netherlands) has been documented for over 25 years, together with quantitative and semi-quantitative data on environmental variables. The population expanded after the closure of the Grevelingen estuary in 1971, but declined from 4600 ha surface area in 1978 to less than 100 ha in 1993. There is little causal evidence which factors are responsible for the observed dynamics of the population. The incomplete picture emerging from the data is that of an extremely impoverished eelgrass population, living under constant oligo-mesotrophic marine conditions. Both the sexual and the vegetative modes of reproduction are severely stressed by environmental variables, most likely a combination of low temperatures, high salinity, low dissolved silicate and low ammonium concentrations. Survival of the population asks for the restoration of moderate estuarine conditions.Contribution No. 2180 of the Netherlands Institute of Ecology, Nieuwersluis, The Netherlands.     

The macroecology of population dynamics: taxonomic and biogeographic patterns in population cycles

Regular cycles in population abundance are fascinating phenomena, but are they common in natural populations? How are they distributed among taxa? Are there differences between different regions of the world, or along latitudinal gradients? Using the new Global Population Dynamics Database we analysed nearly 700 long (25 + years) time series of animal field populations, looking for large-scale patterns in cycles. Nearly 30% of the time series were cyclic. Cycle incidence varied among taxonomic classes, being most common in mammal and fish populations, but only in fish did cycle incidence vary among orders. Cycles were equally common in European and North American populations, but were more common in Atlantic fish than Pacific fish. The incidence of cycles increased with latitude in mammals only. There was no latitudinal gradient in cycle period, but cycle amplitude declined with latitude in some groups of fish. Even after considering the biases in the data source and expected type I error, population cycles seem common enough to warrant ecological attention.     

Understanding the population genetic structure of Gleditsia triacanthos L.: seed dispersal and variation in female reproductive success

Fine-scale genetic structuring is influenced by a variety of ecological factors and can directly affect the evolutionary dynamics of plant populations by influencing effective population size and patterns of viability selection. In many plant species, genetic structuring within populations may result from highly localized patterns of seed dispersal around maternal plants or by the correlated dispersal and recruitment of siblings from the same fruit. This fine-scale genetic structuring may be enhanced if female parents vary significantly in their reproductive success. To test these hypotheses, we used genetic data from 17 allozyme loci and a maximum-likelihood, ‘maternity-analysis’ model to estimate individual female fertilities for maternal trees across a large number of naturally established seedlings and saplings in two populations of Gleditsia triacanthos L. (Leguminosae). Maximum-likelihood fertility estimates showed that the three highest fertility females accounted for 58% of the 313 progeny at the first site and 46% of the 651 progeny at the second site, whereas 18 of 35 and 16 of 34 females, respectively, had fertility estimates that did not exceed 1%. Additional analyses of the second site found individual female fertility to vary significantly both within and among juvenile age classes. Female fertility at the first site was weakly correlated with maternal tree size and spatial location relative to the open, old-field portions of the population, where the great majority of seedlings and saplings were growing, but no such correlations were found at the second site. Estimates of realized seed dispersal distances indicated that dispersal was highly localized at the first site, but was nearly random at the second site, possibly reflecting differences between the two sites in the behaviour of animal dispersers. The combined estimates of seed dispersal patterns and fertility variation are sufficient to explain previously described patterns of significant fine-scale spatial genetic structure in these two populations. In general, our results demonstrate that effective seed dispersal distributions may vary significantly from population to population of a species due to the unpredictable behaviour of secondary dispersers. Consequently, the effects of seed dispersal on realized fine-scale genetic structure may also be relatively unpredictable.     

The limits of mtDNA phylogeography: complex patterns of population history in a highly structured Iberian lizard are only revealed by the use of nuclear markers

Phylogeographic analyses based on the sole use of the mitochondrial DNA (mtDNA) molecule reveal only a small part of the evolutionary history of a species or a set of related species. In this study, we have combined the application of slow- and fast-evolving nuclear markers (proteins and microsatellites, respectively) together with the analysis of two-gene genealogies to further understand the history of the Iberian endemic Schreiber's green lizard, Lacerta schreiberi, a species for which a well established phylogeographical scenario is available. In sharp contrast with the observation of four divergent and almost allopatric mtDNA clades, our nuclear data revealed how two groups of populations diverged, persisted and began to admix along the mountains of the Iberian Central System. In addition, the combination of mtDNA and nuclear data showed how the core area of the species distribution responded to ice ages, first by relatively old processes of population expansion to the south followed by episodes of contraction that are at the origin of present-day isolates, and more recently by a postglacial expansion to the Iberian Northwest where new habitats were made available after climatic amelioration. Taken together with recently published results for a variety of other organisms, our results suggest that complex processes of fragmentation, expansion and admixture can only be properly addressed through the use of several and complementary types of molecular markers. Finally, we also suggest that southern European refugia are both hotspots and melting pots of genetic diversity.