From broadscale patterns to fine-scale processes: habitat structure influences genetic differentiation in the pitcher plant midge across multiple spatial scales

The spatial scale at which samples are collected and analysed influences the inferences that can be drawn from landscape genetic studies. We examined genetic structure and its landscape correlates in the pitcher plant midge, Metriocnemus knabi, an inhabitant of the purple pitcher plant, Sarracenia purpurea, across several spatial scales that are naturally delimited by the midge’s habitat (leaf, plant, cluster of plants, bog and system of bogs). We analysed 11 microsatellite loci in 710 M. knabi larvae from two systems of bogs in Algonquin Provincial Park (Canada) and tested the hypotheses that variables related to habitat structure are associated with genetic differentiation in this midge. Up to 54% of variation in individual‐based genetic distances at several scales was explained by broadscale landscape variables of bog size, pitcher plant density within bogs and connectivity of pitcher plant clusters. Our results indicate that oviposition behaviour of females at fine scales, as inferred from the spatial locations of full‐sib larvae, and spatially limited gene flow at broad scales represent the important processes underlying observed genetic patterns in M. knabi. Broadscale landscape features (bog size and plant density) appear to influence oviposition behaviour of midges, which in turn influences the patterns of genetic differentiation observed at both fine and broad scales. Thus, we inferred linkages among genetic patterns, landscape patterns and ecological processes across spatial scales in M. knabi. Our results reinforce the value of exploring such links simultaneously across multiple spatial scales and landscapes when investigating genetic diversity within a species.     

Density of insect‐pollinated grassland plants decreases with increasing surrounding land‐use intensity

Pollinator declines have raised concerns about the persistence of plant species that depend on insect pollination, in particular by bees, for their reproduction. The impact of pollinator declines remains unknown for species‐rich plant communities found in temperate seminatural grasslands. We investigated effects of land‐use intensity in the surrounding landscape on the distribution of plant traits related to insect pollination in 239 European seminatural grasslands. Increasing arable land use in the surrounding landscape consistently reduced the density of plants depending on bee and insect pollination. Similarly, the relative abundance of bee‐pollination‐dependent plants increased with higher proportions of non‐arable agricultural land (e.g. permanent grassland). This was paralleled by an overall increase in bee abundance and diversity. By isolating the impact of the surrounding landscape from effects of local habitat quality, we show for the first time that grassland plants dependent on insect pollination are particularly susceptible to increasing land‐use intensity in the landscape.     

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.     

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.     

A comparison of individual‐based genetic distance metrics for landscape genetics

A major aim of landscape genetics is to understand how landscapes resist gene flow and thereby influence population genetic structure. An empirical understanding of this process provides a wealth of information that can be used to guide conservation and management of species in fragmented landscapes and also to predict how landscape change may affect population viability. Statistical approaches to infer the true model among competing alternatives are based on the strength of the relationship between pairwise genetic distances and landscape distances among sampled individuals in a population. A variety of methods have been devised to quantify individual genetic distances, but no study has yet compared their relative performance when used for model selection in landscape genetics. In this study, we used population genetic simulations to assess the accuracy of 16 individual‐based genetic distance metrics under varying sample sizes and degree of population genetic structure. We found most metrics performed well when sample size and genetic structure was high. However, it was much more challenging to infer the true model when sample size and genetic structure was low. Under these conditions, we found genetic distance metrics based on principal components analysis were the most accurate (although several other metrics performed similarly), but only when they were derived from multiple principal components axes (the optimal number varied depending on the degree of population genetic structure). Our results provide guidance for which genetic distance metrics maximize model selection accuracy and thereby better inform conservation and management decisions based upon landscape genetic analysis.     

Environmental and biotic drivers of soil microbial β‐diversity across spatial and phylogenetic scales

Soil microbial communities play a key role in ecosystem functioning but still little is known about the processes that determine their turnover (β‐diversity) along ecological gradients. Here, we characterize soil microbial β‐diversity at two spatial scales and at multiple phylogenetic grains to ask how archaeal, bacterial and fungal communities are shaped by abiotic processes and biotic interactions with plants. We characterized microbial and plant communities using DNA metabarcoding of soil samples distributed across and within eighteen plots along an elevation gradient in the French Alps. The recovered taxa were placed onto phylogenies to estimate microbial and plant β‐diversity at different phylogenetic grains (i.e. resolution). We then modeled microbial β‐diversities with respect to plant β‐diversities and environmental dissimilarities across plots (landscape scale) and with respect to plant β‐diversities and spatial distances within plots (plot scale). At the landscape scale, fungal and archaeal β‐diversities were mostly related to plant β‐diversity, while bacterial β‐diversities were mostly related to environmental dissimilarities. At the plot scale, we detected a modest covariation of bacterial and fungal β‐diversities with plant β‐diversity; as well as a distance–decay relationship that suggested the influence of ecological drift on microbial communities. In addition, the covariation between fungal and plant β‐diversity at the plot scale was highest at fine or intermediate phylogenetic grains hinting that biotic interactions between those clades depends on early‐evolved traits. Altogether, we show how multiple ecological processes determine soil microbial community assembly at different spatial scales and how the strength of these processes change among microbial clades. In addition, we emphasized the imprint of microbial and plant evolutionary history on today's microbial community structure.     

The relative influence of habitat amount and configuration on genetic structure across multiple spatial scales

Despite strong interest in understanding how habitat spatial structure shapes the genetics of populations, the relative importance of habitat amount and configuration for patterns of genetic differentiation remains largely unexplored in empirical systems. In this study, we evaluate the relative influence of, and interactions among, the amount of habitat and aspects of its spatial configuration on genetic differentiation in the pitcher plant midge, Metriocnemus knabi. Larvae of this species are found exclusively within the water‐filled leaves of pitcher plants (Sarracenia purpurea) in a system that is naturally patchy at multiple spatial scales (i.e., leaf, plant, cluster, peatland). Using generalized linear mixed models and multimodel inference, we estimated effects of the amount of habitat, patch size, interpatch distance, and patch isolation, measured at different spatial scales, on genetic differentiation (F_ST) among larval samples from leaves within plants, plants within clusters, and clusters within peatlands. Among leaves and plants, genetic differentiation appears to be driven by female oviposition behaviors and is influenced by habitat isolation at a broad (peatland) scale. Among clusters, gene flow is spatially restricted and aspects of both the amount of habitat and configuration at the focal scale are important, as is their interaction. Our results suggest that both habitat amount and configuration can be important determinants of genetic structure and that their relative influence is scale dependent.     

Spatial genetic structuring in a widespread wetland plant on a plateau: Effects of elevation-driven geographic isolation and environmental heterogeneity

1. Highlands are ideal research areas for improving our understanding of the influence of ecological factors on the diversity and spatial patterns of natural species. Elevation-driven physical and environmental isolation greatly affect the evolution of plants. The mechanisms and essential drivers underlying these processes may differ among research scales, habitats and landscapes. Wetlands are important elements of the Qinghai–Tibetan Plateau, which is the highest plateau in the world, and these habitats harbour high aquatic organismal diversity. However, how the environments shape the genetic variation and structure of hydrophilous plants is poorly understood.
2. Using microsatellite markers and a chloroplast fragment, we quantified the genetic diversity and spatial genetic pattern of Stuckenia filiformis, one of the most widespread aquatic plants on the plateau. The relative contributions of geography, climate and local conditions to intra- and interpopulation variation were estimated. The results showed that intrapopulation genetic variation of the plant is moderate to high and not constrained by high-altitude environments. Topographical isolation mainly contributes to the genetic structure of S. filiformis, as inferred by simple sequence repeats and chloroplast DNA data. Significant effects of environmental variables on the spatial genetic patterns of this freshwater species were also suggested by landscape genetic analysis.
3. Infrequent long-distance dispersal, sexual recruitment and annual growth are probably important for the maintenance and distribution of this variation. Our findings imply a combined effect of geography and elevation-driven environmental heterogeneity on the evolution of aquatic organisms in highlands.

     

Range‐wide analysis of genetic structure in a widespread,highly mobile species (Odocoileus hemionus) reveals the importance of historical biogeography

Highly mobile species that thrive in a wide range of habitats are expected to show little genetic differentiation across their range. A limited but growing number of studies have revealed that patterns of broad‐scale genetic differentiation can and do emerge in vagile, continuously distributed species. However, these patterns are complex and often shaped by both historical and ecological factors. Comprehensive surveys of genetic variation at a broad scale and at high resolution are useful for detecting cryptic spatial genetic structure and for investigating the relative roles of historical and ecological processes in structuring widespread, highly mobile species. In this study, we analysed 10 microsatellite loci from over 1900 samples collected across the full range of mule deer (Odocoileus hemionus), one of the most widely distributed and abundant of all large mammal species in North America. Through both individual‐ and population‐based analyses, we found evidence for three main genetic lineages, one corresponding to the ‘mule deer’ morphological type and two to the ‘black‐tailed deer’ type. Historical biogeographic events likely are the primary drivers of genetic divergence in this species; boundaries of the three lineages correspond well with predictions based on Pleistocene glacial cycles, and substructure within each lineage demonstrates island vicariance. However, across large geographic areas, including the entire mule deer lineage, we found that genetic variation fit an isolation‐by‐distance pattern rather than discrete clusters. A lack of genetic structure across wide geographic areas of the continental west indicates that ecological processes have not resulted in restrictions to gene flow sufficient for spatial genetic structure to emerge. Our results have important implications for our understanding of evolutionary mechanisms of divergence, as well as for taxonomy, conservation and management.     

Spatial variability in a plant–pollinator community across a continuous habitat: high heterogeneity in the face of apparent uniformity

Large‐scale spatial variability in plant–pollinator communities (e.g. along geographic gradients, across different landscapes) is relatively well understood. However, we know much less about how these communities vary at small scales within a uniform landscape. Plants are sessile and highly sensitive to microhabitat conditions, whereas pollinators are highly mobile and, for the most part, display generalist feeding habits. Therefore, we expect plants to show greater spatial variability than pollinators. We analysed the spatial heterogeneity of a community of flowering plants and their pollinators in 40 plots across a 40‐km² area within an uninterrupted Mediterranean scrubland. We recorded 3577 pollinator visits to 49 plant species. The pollinator community (170 species) was strongly dominated by honey bees (71.8% of the visits recorded). Flower and pollinator communities showed similar beta‐diversity, indicating that spatial variability was similar in the two groups. We used path analysis to establish the direct and indirect effects of flower community distribution and honey bee visitation rate (a measure of the use of floral resources by this species) on the spatial distribution of the pollinator community. Wild pollinator abundance was positively related to flower abundance. Wild pollinator visitation rate was negatively related to flower abundance, suggesting that floral resources were not limiting. Pollinator and flower richness were positively related. Pollinator species composition was weakly related to flower species composition, reflecting the generalist nature of flower–pollinator interactions and the opportunistic nature of pollinator flower choices. Honey bee visitation rate did not affect the distribution of the wild pollinator community. Overall, we show that, in spite of the apparent physiognomic uniformity, both flowers and pollinators display high levels of heterogeneity, resulting in a mosaic of idiosyncratic local communities. Our results provide a measure of the background of intrinsic heterogeneity within a uniform habitat, with potential consequences on low‐scale ecosystem function and microevolutionary patterns.     

Variation at range margins across multiple spatial scales: environmental temperature,population genetics and metabolomic phenotype

Range margins are spatially complex, with environmental, genetic and phenotypic variations occurring across a range of spatial scales. We examine variation in temperature, genes and metabolomic profiles within and between populations of the subalpine perennial plant Arabidopsis lyrata ssp. petraea from across its northwest European range. Our surveys cover a gradient of fragmentation from largely continuous populations in Iceland, through more fragmented Scandinavian populations, to increasingly widely scattered populations at the range margin in Scotland, Wales and Ireland. Temperature regimes vary substantially within some populations, but within-population variation represents a larger fraction of genetic and especially metabolomic variances. Both physical distance and temperature differences between sites are found to be associated with genetic profiles, but not metabolomic profiles, and no relationship was found between genetic and metabolomic population structures in any region. Genetic similarity between plants within populations is the highest in the fragmented populations at the range margin, but differentiation across space is the highest there as well, suggesting that regional patterns of genetic diversity may be scale dependent.     

Do landscape processes predict phylogeographic patterns in the wood frog?

Understanding factors that influence population connectivity and the spatial distribution of genetic variation is a major goal in molecular ecology. Improvements in the availability of high-resolution geographic data have made it increasingly possible to quantify the effects of landscape features on dispersal and genetic structure. However, most studies examining such landscape effects have been conducted at very fine (e.g. landscape genetics) or broad (e.g. phylogeography) spatial scales. Thus, the extent to which processes operating at fine spatial scales are linked to patterns at larger scales remains unclear. Here, we test whether factors impacting wood frog dispersal at fine spatial scales are correlated with genetic structure at regional scales. Using recently developed methods borrowed from electrical circuit theory, we generated landscape resistance matrices among wood frog populations in eastern North America based on slope, a wetness index, land cover and absolute barriers to wood frog dispersal. We then determined whether these matrices are correlated with genetic structure based on six microsatellite markers and whether such correlations outperform a landscape-free model of isolation by resistance. We observed significant genetic structure at regional spatial scales. However, topography and landscape variables associated with the intervening habitat between sites provide little explanation for patterns of genetic structure. Instead, absolute dispersal barriers appear to be the best predictor of regional genetic structure in this species. Our results suggest that landscape variables that influence dispersal, microhabitat selection and population structure at fine spatial scales do not necessarily explain patterns of genetic structure at broader scales.     

Genome‐wide epigenetic isolation by environment in a widespread Anolis lizard

Epigenetic changes can provide a pathway for organisms to respond to local environmental conditions by influencing gene expression. However, we still know little about the spatial distribution of epigenetic variation in natural systems, how it relates to the distribution of genetic variation and the environmental structure of the landscape, and the processes that generate and maintain it. Studies examining spatial patterns of genetic and epigenetic variation can provide valuable insights into how ecological and population processes contribute to epigenetic divergence across heterogeneous landscapes. Here, we perform a comparative analysis of spatial genetic and epigenetic variation based on 8,459 single nucleotide polymorphisms (SNPs) and 8,580 single methylation variants (SMVs) from eight populations of the Puerto Rican crested anole, Anolis cristatellus, an abundant lizard in the adaptive radiations of anoles on the Greater Antilles that occupies a diverse range of habitats. Using generalized dissimilarity modelling and multiple matrix regression, we found that genome‐wide epigenetic differentiation is strongly correlated with environmental divergence, even after controlling for the underlying genetic structure. We also detected significant associations between key environmental variables and 96 SMVs, including 42 located in promoter regions or gene bodies. Our results suggest an environmental basis for population‐level epigenetic differentiation in this system and contribute to better understanding how environmental gradients structure epigenetic variation in nature.     

Genetic differentiation on multiple spatial scales in an ecotype-forming marine snail with limited dispersal: Littorina saxatilis

The population genetic structure of marine species lacking free-swimming larvae is expected to be strongly affected by random genetic drift among populations, resulting in genetic isolation by geographical distance. At the same time, ecological separation over microhabitats followed by direct selection on those parts of the genome that affect adaptation might also be strong. Here, we address the question of how the relative importance of stochastic vs. selective structuring forces varies at different geographical scales. We use microsatellite DNA and allozyme data from samples of the marine rocky shore snail Littorina saxatilis over distance scales ranging from metres to 1000 km, and we show that genetic drift is the most important structuring evolutionary force at distances > 1 km. On smaller geographical scales (< 1 km), divergent selection between contrasting habitats affects population genetic structure by impeding gene flow over microhabitat borders (microsatellite structure), or by directly favouring specific alleles of selected loci (allozyme structure). The results suggest that evolutionary drivers of population genetic structure cannot a priori be assumed to be equally important at different geographical scales. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 31–40.     

Dispersal ability and habitat requirements determine landscape‐level genetic patterns in desert aquatic insects

Species occupying the same geographic range can exhibit remarkably different population structures across the landscape, ranging from highly diversified to panmictic. Given limitations on collecting population‐level data for large numbers of species, ecologists seek to identify proximate organismal traits—such as dispersal ability, habitat preference and life history—that are strong predictors of realized population structure. We examined how dispersal ability and habitat structure affect the regional balance of gene flow and genetic drift within three aquatic insects that represent the range of dispersal abilities and habitat requirements observed in desert stream insect communities. For each species, we tested for linear relationships between genetic distances and geographic distances using Euclidean and landscape‐based metrics of resistance. We found that the moderate‐disperser Mesocapnia arizonensis (Plecoptera: Capniidae) has a strong isolation‐by‐distance pattern, suggesting migration–drift equilibrium. By contrast, population structure in the flightless Abedus herberti (Hemiptera: Belostomatidae) is influenced by genetic drift, while gene flow is the dominant force in the strong‐flying Boreonectes aequinoctialis (Coleoptera: Dytiscidae). The best‐fitting landscape model for M. arizonensis was based on Euclidean distance. Analyses also identified a strong spatial scale‐dependence, where landscape genetic methods only performed well for species that were intermediate in dispersal ability. Our results highlight the fact that when either gene flow or genetic drift dominates in shaping population structure, no detectable relationship between genetic and geographic distances is expected at certain spatial scales. This study provides insight into how gene flow and drift interact at the regional scale for these insects as well as the organisms that share similar habitats and dispersal abilities.     

Genomic footprints of adaptation in a cooperatively breeding tropical bird across a vegetation gradient

Identifying the genetic basis of phenotypic variation and its relationship with the environment is key to understanding how local adaptations evolve. Such patterns are especially interesting among populations distributed across habitat gradients, where genetic structure can be driven by isolation by distance (IBD) and/or isolation by environment (IBE). Here, we used variation in ~1,600 high‐quality SNPs derived from paired‐end sequencing of double‐digest restriction site‐associated DNA (ddRAD‐Seq) to test hypotheses related to IBD and IBE in the Yucatan jay (Cyanocorax yucatanicus), a tropical bird endemic to the Yucatán Peninsula. This peninsula is characterized by a precipitation and vegetation gradient—from dry to evergreen tropical forests—that is associated with morphological variation in this species. We found a moderate level of nucleotide diversity (π = .008) and little evidence for genetic differentiation among vegetation types. Analyses of neutral and putatively adaptive SNPs (identified by complementary genome‐scan approaches) indicate that IBD is the most reliable explanation to account for frequency distribution of the former, while IBE has to be invoked to explain those of the later. These results suggest that selective factors acting along a vegetation gradient can promote local adaptation in the presence of gene flow in a vagile, nonmigratory and geographically restricted species. The putative candidate SNPs identified here are located within or linked to a variety of genes that represent ideal targets for future genomic surveys.     

Drivers of population genetic differentiation in the wild: isolation by dispersal limitation,isolation by adaptation and isolation by colonization

Empirical population genetic studies have been dominated by a neutralist view, according to which gene flow and drift are the main forces driving population genetic structure in nature. The neutralist view in essence describes a process of isolation by dispersal limitation (IBDL) that generally leads to a pattern of isolation by distance (IBD). Recently, however, conceptual frameworks have been put forward that view local genetic adaptation as an important driver of population genetic structure. Isolation by adaptation (IBA) and monopolization (M) posit that gene flow among natural populations is reduced as a consequence of local genetic adaptation. IBA stresses that effective gene flow is reduced among habitats that show dissimilar ecological characteristics, leading to a pattern of isolation by environment. In monopolization, local genetic adaptation of initial colonizing genotypes results in a reduction in gene flow that fosters the persistence of founder effects. Here, we relate these different processes driving landscape genetic structure to patterns of IBD and isolation by environment (IBE). We propose a method to detect whether IBDL, IBA and M shape genetic differentiation in natural landscapes by studying patterns of variation at neutral and non‐neutral markers as well as at ecologically relevant traits. Finally, we reinterpret a representative number of studies from the recent literature by associating patterns to processes and identify patterns associated with local genetic adaptation to be as common as IBDL in structuring regional genetic variation of populations in the wild. Our results point to the importance of quantifying environmental gradients and incorporating ecology in the analysis of population genetics.