Effects of habitat fragmentation on the genetic structure of the monophagous butterfly Polyommatus coridon along its northern range margin

Population genetic patterns of species at their range margin have important implications for species conservation. We performed allozyme electrophoresis of 19 loci to investigate patterns of the genetic structure of 17 populations (538 individuals) of the butterfly Polyommatus coridon, a monophagous habitat specialist with a patchy distribution. The butterfly and its larval food plant Hippocrepis comosa reach their northern distribution margin in the study region (southern Lower Saxony, Germany). Butterfly population size increased with host plant population size. The genetic differentiation between populations was low but significant (FST = 0.013). No isolation-by-distance was found. Hierarchical F-statistics revealed significant differentiation between a western and an eastern subregion, separated by a river valley. The combination of genetic and ecological data sets revealed that the expected heterozygosity (mean: 18.5%) decreased with increasing distance to the nearest P. coridon population. The population size of P. coridon and the size of larval food plant population had no effect on the genetic diversity. The genetic diversity of edge populations of P. coridon was reduced compared to populations from the centre of its distribution. This might be explained by (i). an increasing habitat fragmentation towards the edge of the distribution range and/or (ii). a general reduction of genetic variability towards the northern edge of its distribution.     

Habitat differentiation vs. isolation-by-distance: the genetic population structure of Elymus athericus in European salt marshes

We investigated genetic differentiation among populations of the clonal grass Elymus athericus, a common salt-marsh species occurring along the Wadden Sea coast of Europe. While E. athericus traditionally occurs in the high salt marsh, it recently also invaded lower parts of the marsh. In one of the first analyses of the genetic population structure in salt-marsh species, we were interested in population differentiation through isolation-by-distance, and among strongly divergent habitats (low and high marsh) in this wind- and water-dispersed species. High and low marsh habitats were sampled at six sites throughout the Wadden Sea. Based on reciprocal transplantation experiments conducted earlier revealing lower survival of foreign genotypes we predicted reduced gene flow among habitats. Accordingly, an analysis with polymorphic cross-species microsatellite primers revealed significant genetic differentiation between high and low marsh habitats already on a very small scale (< 100 m), while isolation-by-distance was present only on larger scales (60-443 km). In an analysis of molecular variance we found that 14% of the genetic variance could be explained by the differentiation between habitats, as compared to only 8.9% to geographical (isolation-by-distance) effects among six sites 2.5-443 km distant from each other. This suggests that markedly different selection regimes between these habitats, in particular intraspecific competition and herbivory, result in habitat adaptation and restricted gene flow over distances as small as 80 m. Hence, the genetic population structure of plant species can only be understood when considering geographical and selection-mediated restrictions to gene flow simultaneously.     

Cryptic population structure in a large,mobile mammalian predator: the Scandinavian lynx

The Eurasian lynx (Lynx lynx) is an example of a species that has gone through a severe bottleneck, leading to near extinction in Scandinavia around 1930-- a pattern shared with several other large carnivorous mammals. Here we extend previous genetic analyses of northern European lynx, confirming that lynx from the Scandinavian Peninsula represent a distinct clade differing clearly from European conspecifics. Furthermore, and despite a recent bottleneck and subsequent range expansion, we detect marked genetic differentiation within Scandinavia. This differentiation is largely manifested as a north-south gradient, with a linear increase in the quantity FST/(1 - FST). Aided by computer simulations we find that this pattern is unlikely to have arisen by random genetic drift in the short time since lynx started to expand in the 1950s, suggesting that the spatial structure may predate the bottleneck. Individual-based analyses indicate that, instead of a continuous gradient, Scandinavian lynx may be structured into three more or less distinct groups, possibly corresponding to northern, central and southern subpopulations. The presence of such structuring was unknown previously and was unexpected from general considerations on the mobility of the species, historical data and the absence of geographical barriers. Our study demonstrates how molecular markers may be used to detect cryptic population structure, invisible using traditional methods.     

Phylogeography of the intertidal copepod Tigriopus californicus reveals substantially reduced population differentiation at northern latitudes

Previous studies of the intertidal copepod Tigriopus californicus revealed one of the highest levels of mitochondrial DNA differentiation ever reported among conspecific populations. The present study extends the geographical sampling northward, adding populations from northern California to south-east Alaska. The mitochondrial phylogeny for the entire species range, based on cytochrome oxidase I sequences for a total of 49 individuals from 27 populations, again shows extreme differentiation among populations (up to 23%). However, populations from Oregon northwards appear to be derived and have interpopulation divergences five times lower than those between southern populations. Furthermore, although few individuals were sequenced from each locality, populations from Puget Sound northward had significantly reduced levels of within-population variation. These patterns are hypothesized to result from the contraction and expansion of populations driven by recent ice ages.     

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.     

EFFECTS OF POSTGLACIAL RANGE EXPANSION ON ALLOZYME AND QUANTITATIVE GENETIC VARIATION OF THE PITCHER-PLANT MOSQUITO,WYEOMYIA SMITHII

We determined allozyme variability of 34 populations of the pitcher-plant mosquito, Wyeomyia smithii, from Florida (30°N) to northern Manitoba (54°N) and compared allozyme variability with the additive genetic variance for preadult development time and photoperiodic response determined previously for six populations over a similar range (30–50°N). Phylogenetic analysis of allozymes shows a well-defined split between Gulf Coast and lowland North Carolina populations, similar to previously observed phylogeographic patterns in a wide variety of taxa. A deeper split in the phylogeny of W. smithii coincides with the location of the maximum extent of the Laurentide Ice Sheet. Furthermore, both average heterozygosity and patterns of isolation-by-distance decline in populations north of the former glacial border. It is likely that northern populations are the result of a range expansion that occurred subsequent to the late-Wisconsin retreat of the Laurentide Ice Sheet and that these populations have not yet reached a drift-migration equilibrium. The northern decline in allozyme heterozygosity contrasts sharply with the northern increase in additive genetic variance of development time and photoperiodic response found in previous studies. These previous studies also showed that the genetic divergence of populations has involved stochastic variation in the contribution of dominance and epistasis to the genetic architecture underlying demographic traits, including preadult development time, and photoperiodic response. When taken together, the present and prior studies identify the genetic processes underlying the lack of concordance between geographic patterns of allozyme and quantitative genetic variation in natural populations of W. smithii. In the presence of nonadditive genetic variation, isolation and drift can result in opposite patterns of genetic variation for structural genes and quantitative traits.     

Geographical distance and physical barriers shape the genetic structure of Eurasian red squirrels (Sciurus vulgaris) in the Italian Alps

Red squirrels (Sciurus vulgaris) are widely distributed throughout Eurasia, occurring in many types of coniferous and mixed-deciduous forests. In fragmented landscapes, small and partly isolated populations with low immigration rates show reduced genetic diversity, but reforestation can increase gene flow and restore levels of genetic variation in a few decades. No studies have so far investigated the genetic structure of red squirrel in large, continuous forests. The Italian Alps are presently characterized by almost continuous, recently reconnected forest habitats, that were affected by deep landscape changes during last glaciations but remained mostly unchanged between 10 000 and 200 years bp, when forest cover was heavily reduced. In this study we analyse patterns of genetic variability of red squirrels in and between seven sites distributed over 250 km of Alpine habitat, using mitochondrial DNA (mtDNA) and microsatellites. We use isolation-by-distance (IBD) models to investigate the relative importance that past (Pleistocene glaciations) and recent (fragmentation, bottlenecks) events had on the present genetic situation. Both nuclear and mtDNA data indicate a significant differentiation among study sites and a significant correlation between genetic and geographical distance only over a large scale. No recent bottlenecks are recorded through microsatellites and demographic models strongly support equilibrium between gene flow and drift; however, mtDNA suggests that there may have been local demographic crashes, probably in correspondence with the 19th-century forest fragmentation. These findings indicate that local landscape factors other than geographical distance per se, such as barriers of unsuitable habitat, affect gene flow and determine differentiation.     

Population subdivision in marine environments: the contributions of biogeography, geographical distance and discontinuous habitat to genetic differentiation in a blennioid fish, Axoclinus nigricaudus

The relative importance of factors that may promote genetic differentiation in marine organisms is largely unknown. Here, contributions to population structure from a biogeographic boundary, geographical distance and the distribution of suitable habitat were investigated in Axoclinus nigricaudus, a small subtidal rock-reef fish, throughout its range in the Gulf of California. A 408-bp fragment of the mitochondrial control region was sequenced from 105 individuals. Variation was significantly partitioned between 28 of 36 possible combinations of population pairs. Phylogenetic analyses, hierarchical analyses of variance and a modified Mantel test substantiated a major break between two putative biogeographic regions. This genetic discontinuity coincides with an abrupt change in ecological characteristics, including temperature and salinity, but does not coincide with known oceanographic circulation patterns or any known historic barriers. There was an overall relationship of increasing genetic distance with increasing geographical distance between population pairs, in a manner consistent with isolation-by-distance. A significant habitat-by-geographical-distance interaction term indicated that, for a given geographical distance, populations separated by discontinuous habitat (sand) are more distinct genetically than are populations separated by continuous habitat (rock). In addition, populations separated by deep open waters were more genetically distinct than populations separated by continuous habitat (rock). These results indicate that levels of genetic differentiation among populations of A. nigricaudus cannot be explained by a single factor, but are due to the combined influences of biogeography, geographical distance and availability of suitable habitat.     

Fine-scale genetic structure, co-founding and multiple mating in the Australian allodapine bee (Exoneura robusta)

Despite the role of Australian native bees in important ecological processes, surprisingly little is known of their population structuring. In this study five microsatellite loci were used to investigate genetic structuring of the allodapine bee Exoneura robusta sampled from four locations (maximum pairwise distance c . 35 km) in the Mountain Ash forests of Victoria. Although E. robusta would seem to have high dispersal ability, several analyses show significant population subdivision and a strong pattern of isolation-by-distance from which limited gene flow was inferred. Limited gene flow was not associated with inbreeding at the within-colony level, and within-colony genetic structure implied co-founding, multiple breeding pairs and some degree of reproductive skew. Strong population structure at such fine scales suggests that substantially divergent populations are likely within the extensive distribution currently ascribed to E. robusta .     

LIKELIHOOD-BASED INFERENCE IN ISOLATION-BY-DISTANCE MODELS USING THE SPATIAL DISTRIBUTION OF LOW-FREQUENCY ALLELES

Estimating dispersal distances from population genetic data provides an important alternative to logistically taxing methods for directly observing dispersal. Although methods for estimating dispersal rates between a modest number of discrete demes are well developed, methods of inference applicable to "isolation-by-distance" models are much less established. Here, we present a method for estimating ρσ², the product of population density (ρ) and the variance of the dispersal displacement distribution (σ²). The method is based on the assumption that low-frequency alleles are identical by descent. Hence, the extent of geographic clustering of such alleles, relative to their frequency in the population, provides information about ρσ². We show that a novel likelihood-based method can infer this composite parameter with a modest bias in a lattice model of isolation-by-distance. For calculating the likelihood, we use an importance sampling approach to average over the unobserved intraallelic genealogies, where the intraallelic genealogies are modeled as a pure birth process. The approach also leads to a likelihood-ratio test of isotropy of dispersal, that is, whether dispersal distances on two axes are different. We test the performance of our methods using simulations of new mutations in a lattice model and illustrate its use with a dataset from Arabidopsis thaliana .