Landscape Genetic Studies Research Articles

Where do you come from, where do you go? Directional migration rates in landscape genetics

Identifying landscape elements that influence gene flow and migration in wild species is the current main topic of landscape genetics. Most landscape genetic studies infer gene flow and migration from genetic distances among populations or individuals and statistically relate these measurements to landscape composition and configuration. This approach assumes symmetrical gene flow between pairs of populations. Such an assumption, however, will often be violated, especially in source–sink systems. Source populations provide more emigrants than they receive immigrants, and sink populations get many immigrants, but release few emigrants. Source–sink dynamics cannot be explored using common landscape genetic approaches relying on genetic distances. In this issue of Molecular Ecology, Andreasen et al. (2012) apply an alternative approach allowing them to infer asymmetrical migration. They use a Bayesian assignment test among objectively defined populations of mountain lions (Puma concolor) in western USA to estimate recent and directional migration rates. The study shows that an area with a high amount of wildlife refuges and low hunting pressure harbours a source population for mountain lion dispersal, while areas with high hunting pressures form sink populations; a result helpful in making informed decisions in conservation management.

Differential effects of landscape‐level environmental features on genetic structure in three codistributed tree species in Central America

Landscape genetic studies use spatially explicit population genetic information to determine the physical and environmental causes of population genetic structure on regional scales. Comparative studies that identify common barriers to gene flow across multiple species within a community are important to both understand the evolutionary trajectories of populations and prioritize habitat conservation. Here, we use a comparative landscape genetic approach to ask whether gradients in temperature or precipitation seasonality structure genetic variation across three codistributed tree species in Central America, or whether a simpler (geographic distance) or more complex, species-specific environmental niche model is necessary to individually explain population genetic structure. Using descriptive statistics and causal modelling, we find that different factors best explain genetic distance in each of the three species: environmental niche distance in Bursera simaruba, geographic distance in Ficus insipida and historical barriers to gene flow or cryptic reproductive barriers for Brosimum alicastrum. This study confirms suggestions from previous studies of Central American tree species that imply that population genetic structure of trees in this region is determined by complex interactions of both historical and current barriers to gene flow.

A decade of amphibian population genetic studies: synthesis and recommendations

Amphibians are declining globally, and a comprehensive understanding of the spatial distribution of genetic diversity will inform conservation efforts. However, studies that estimate amphibian population genetic structure and gene flow have not yet been synthesized. Our search of literature from 2001 to 2010 yielded 552 amphibian population and landscape genetic studies, of which 139 explicitly estimated gene flow or genetic structure. We examined these works for general trends and conducted a meta-analysis of reported FST values. The majority of studies took place in temperate forests in North America and Europe, with no studies of caecilians and few studies of direct-developing species. Among landscape genetic studies, rivers, roads, and mountain ridges were the predominant barriers identified. Conservation status was the only factor that showed a significant relationship with FST, with the least concern IUCN status differing significantly from the near threatened (NT) status as well as from any combination of IUCN statuses that included NT. Recent technological advances will help researchers fill taxonomic and geographic research gaps, thereby facilitating management plans that address a greater diversity of amphibian species.

Genetic discontinuities in roe deer (Capreolus capreolus) coincide with fenced transportation infrastructure

Linear landscape elements may act as barriers to the movement of wildlife, inducing genetic sub-structure because barriers impair gene flow. This effect often occurs in response to transportation infrastructure such as freeways, requiring expensive measures, such as overpasses, to re-establish connectivity among separated populations. Here, we present a landscape genetic study using a spatial overlay of landscape elements and genetic clustering based on nuclear microsatellites in roe deer. Our results show that fenced freeways appeared as the main obstacles to gene flow in roe deer within a nationally important wildlife corridor in Switzerland. On the other hand, a wide river only showed a weak barrier effect, whereas a highly frequented but unfenced railway track had no detectable effect on gene flow. Landscape genetic overlays proved helpful in the communication with practical environmental management, as they are intuitively appealing. Furthermore, the chosen approach pointed to the need for setting priorities for building wildlife passages as a connectivity measure in the study landscape and sets the reference line for testing the effectiveness of the measures taken.

Comparative biogeography reveals differences in population genetic structure of five species of stream fishes

The distribution of genetic variation in Texas stream fishes has been shaped by a complex mix of historical and anthropogenic factors. Although Texas was not glaciated during the Pleistocene, the rise in sea level following this epoch isolated formerly connected drainages. More recently, the construction of dams, modifications of stream systems, and the release of commercially raised fish have influenced the patterns of genetic diversity. To examine how these different factors have impacted Texas stream fishes, we compared the genetic structure of five species of fish spanning two families and inhabiting two adjacent drainages: Lepomis megalotis, Lepomis cyanellus, Cyprinella lutrensis, Cyprinella venusta, and Campostoma anomalum. Our analyses of the mitochondrial D-Loop show that genetic patterns differ strongly across species. A phylogeographical split between the Brazos and Trinity drainages was seen in conspecific populations of Lepomis species and is probably the result of the historical separation of these river systems. In contrast, contemporary ecological and anthropogenic factors, such as the desiccation of streams during summer, and the translocation of bait fish, appear to have a stronger influence on the genetic patterns in the remaining species. The contrasting results demonstrate the importance of using a multi-species, comparative approach for landscape genetic studies as single species patterns may not be representative of others and thus may obscure differential effects of historical versus recent events as well as natural versus anthropogenic forces. By comparing closely related species that differ in their life history and economic importance it may be possible to disentangle the relative roles of historical, intrinsic, and anthropogenic influences on different organisms within a region. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, ••, ••–••.

Scale-Dependent Effects of a Heterogeneous Landscape on Genetic Differentiation in the Central American Squirrel Monkey (Saimiri oerstedii)

Landscape genetic studies offer a fine-scale understanding of how habitat heterogeneity influences population genetic structure. We examined population genetic structure and conducted a landscape genetic analysis for the endangered Central American Squirrel Monkey (Saimiri oerstedii) that lives in the fragmented, human-modified habitats of the Central Pacific region of Costa Rica. We analyzed non-invasively collected fecal samples from 244 individuals from 14 groups for 16 microsatellite markers. We found two geographically separate genetic clusters in the Central Pacific region with evidence of recent gene flow among them. We also found significant differentiation among groups of S. o. citrinellus using pairwise FST comparisons. These groups are in fragments of secondary forest separated by unsuitable “matrix” habitats such as cattle pasture, commercial African oil palm plantations, and human residential areas. We used an individual-based landscape genetic approach to measure spatial patterns of genetic variance while taking into account landscape heterogeneity. We found that large, commercial oil palm plantations represent moderate barriers to gene flow between populations, but cattle pastures, rivers, and residential areas do not. However, the influence of oil palm plantations on genetic variance was diminished when we restricted analyses to within population pairs, suggesting that their effect is scale-dependent and manifests during longer dispersal events among populations. We show that when landscape genetic methods are applied rigorously and at the right scale, they are sensitive enough to track population processes even in species with long, overlapping generations such as primates. Thus landscape genetic approaches are extremely valuable for the conservation management of a diverse array of endangered species in heterogeneous, human-modified habitats. Our results also stress the importance of explicitly considering the heterogeneity of matrix habitats in landscape genetic studies, instead of assuming that all matrix habitats have a uniform effect on population genetic processes.

Individual variation in dispersal associated with phenotype influences fine-scale genetic structure in weasels

In general, landscape genetic studies have ignored the potential role that the phenotype of individuals plays in determining fine-scale genetic structure in species. This potential over-simplification ignores an important component that dispersal is both condition- and phenotype-dependent. In order to investigate the relationship between potential dispersal, habitat selection and phenotype, we examined the spatial ecology, body mass and fine-scale genetic structure of weasels (Mustela nivalis) in Bialowieza Forest in Poland. Our study population is characterized by an almost three-fold phenotypic variation in adult body mass and weasels were segregated in certain habitats according to size. We detected significant genetic structuring associated with habitat within the studied area and analyses of radio-tracking and re-capture data showed that the maximum extent of movement was achieved by weasels of medium body size, whereas the smallest and largest individuals exhibited higher site fidelity. With the unrestricted movement of the medium-sized individuals across optimal habitat, genetic admixture does occur. However, the presence of a barrier leads to unidirectional gene flow, with larger individuals outcompeting smaller individuals and therefore maintaining the genetic break in the study area. This highlights the importance of considering both intrinsic (phenotype) and extrinsic (environmental) factors in understanding dispersal patterns and ultimately, gene flow in complex landscapes.

Population structure and gene flow in a heavily disturbed habitat: implications for the management of the imperilled Red Hills salamander (Phaeognathus hubrichti)

Estimating levels of gene flow and assessing levels of population connectivity are of critical importance to the field of conservation genetics, especially for imperiled species. Many factors can influence dispersal and therefore gene-flow patterns across a natural landscape. These patterns can be substantially altered by the impacts of habitat modification by humans or natural phenomena. Landscape-genetic studies that address both historical and contemporary influences on gene flow can be critical to demonstrating whether isolated populations with low levels of genetic variation are typical of the species or a result of strong negative effects of such modification. We used 10 microsatellite markers to investigate the spatial genetic patterns of the Red Hills salamander (Phaeognathus hubrichti), a federally listed species. Bayesian clustering revealed five well-supported demes within the range of P. hubrichti. Gene-flow analysis suggested that overall migration levels for P. hubrichti are low, but coalescent methods indicate that migration levels were significantly higher before habitat modification by humans. By accounting for history and species characteristics, our results suggest that loss and fragmentation of habitat have strongly negatively affected P. hubrichti by reducing migration, increasing bottlenecks, and promoting high levels of inbreeding.

Environmental and topographic variables shape genetic structure and effective population sizes in the endangered Yosemite toad

AbstractAim Describing the landscape variables that accurately reflect how environmental and topographic variations affect population connectivity and demography is a major goal of landscape genetics and conservation biology. However, few landscape genetics studies have quantified the relationships between landscape variables and effective population size (Ne), although Ne is a key conservation and population genetics parameter. In this study, I estimated genetic structure and effective population sizes in the Yosemite toad (Bufo canorus) and tested for associations with environmental and geographic variables.Location Yosemite National Park, California, USA.Methods I estimated FST, Dps and Ne using 10 microsatellite loci amplified from 781 individuals from 24 populations. I used three landscape variables (environmental variation, topography and slope) to generate geographic distance models and a series of regression analyses to identify the variables that contributed to genetic structure in this species. I also tested for correlations between Ne and a suite of variables, including geographic and genetic isolation, habitat suitability, elevation, temperature and precipitation.Results I found substantial variation in genetic distances between populations (FST = 0.004–0.396, Dps = 0.045–0.839) and in effective population sizes (Ne = 9–52). Environmental variation and slope played important roles in explaining variation in genetic distances, and precipitation variables were significantly correlated with Ne.Main conclusions These results show that environmental and topographic variables are both important for understanding population connectivity in B. canorus and provide some of the first evidence, in any species, for a link between environmental variables and effective population size.

The effect of cost surface parameterization on landscape resistance estimates

A cost or resistance surface is a representation of a landscape's permeability to animal movement or gene flow and is a tool for measuring functional connectivity in landscape ecology and genetics studies. Parameterizing cost surfaces by assigning weights to different landscape elements has been challenging however, because true costs are rarely known; thus, expert opinion is often used to derive relative weights. Assigning weights would be made easier if the sensitivity of different landscape resistance estimates to relative costs was known. We carried out a sensitivity analysis of three methods to parameterize a cost surface and two models of landscape permeability: least cost path and effective resistance. We found two qualitatively different responses to varying cost weights: linear and asymptotic changes. The most sensitive models (i.e. those leading to linear change) were accumulated least cost and effective resistance estimates on a surface coded as resistance (i.e. where high-quality elements were held constant at a low-value, and low-quality elements were varied at higher values). All other cost surface scenarios led to asymptotic change. Developing a cost surface that produces a linear response of landscape resistance estimates to cost weight variation will improve the accuracy of functional connectivity estimates, especially when cost weights are selected through statistical model fitting procedures. On the other hand, for studies where cost weights are unknown and model selection is not being used, methods where resistance estimates vary asymptotically with cost weights may be more appropriate, because of their relative insensitivity to parameterization.

Fine-Scale Analysis Reveals Cryptic Landscape Genetic Structure in Desert Tortoises

Characterizing the effects of landscape features on genetic variation is essential for understanding how landscapes shape patterns of gene flow and spatial genetic structure of populations. Most landscape genetics studies have focused on patterns of gene flow at a regional scale. However, the genetic structure of populations at a local scale may be influenced by a unique suite of landscape variables that have little bearing on connectivity patterns observed at broader spatial scales. We investigated fine-scale spatial patterns of genetic variation and gene flow in relation to features of the landscape in desert tortoise (Gopherus agassizii), using 859 tortoises genotyped at 16 microsatellite loci with associated data on geographic location, sex, elevation, slope, and soil type, and spatial relationship to putative barriers (power lines, roads). We used spatially explicit and non-explicit Bayesian clustering algorithms to partition the sample into discrete clusters, and characterize the relationships between genetic distance and ecological variables to identify factors with the greatest influence on gene flow at a local scale. Desert tortoises exhibit weak genetic structure at a local scale, and we identified two subpopulations across the study area. Although genetic differentiation between the subpopulations was low, our landscape genetic analysis identified both natural (slope) and anthropogenic (roads) landscape variables that have significantly influenced gene flow within this local population. We show that desert tortoise movements at a local scale are influenced by features of the landscape, and that these features are different than those that influence gene flow at larger scales. Our findings are important for desert tortoise conservation and management, particularly in light of recent translocation efforts in the region. More generally, our results indicate that recent landscape changes can affect gene flow at a local scale and that their effects can be detected almost immediately.

Effects of the landscape on boreal toad gene flow: does the pattern-process relationship hold true across distinct landscapes at the northern range margin?

Understanding the impact of natural and anthropogenic landscape features on population connectivity is a major goal in evolutionary ecology and conservation. Discovery of dispersal barriers is important for predicting population responses to landscape and environmental changes, particularly for populations at geographic range margins. We used a landscape genetics approach to quantify the effects of landscape features on gene flow and connectivity of boreal toad (Bufo boreas) populations from two distinct landscapes in south-east Alaska (Admiralty Island, ANM, and the Chilkat River Valley, CRV). We used two common methodologies for calculating resistance distances in landscape genetics studies (resistance based on least-cost paths and circuit theory). We found a strong effect of saltwater on genetic distance of CRV populations, but no landscape effects were found for the ANM populations. Our discordant results show the importance of examining multiple landscapes that differ in the variability of their features, to maximize detectability of underlying processes and allow results to be broadly applicable across regions. Saltwater serves as a physiological barrier to boreal toad gene flow and affects populations on a small geographic scale, yet there appear to be few other barriers to toad dispersal in this intact northern region.

Novel tetra- and pentanucleotide microsatellite markers allow for multiplexed genotyping of Sulawesi tarsiers (Tarsius spp.)

Based on 454 sequencing, we characterized 10 polymorphic tetra- and pentanucleotide microsatellites for population studies of Sulawesi tarsiers. We identified 2516 repeat regions and designed PCR primer pairs for 60 tetra-, penta- and hexanucleotide repeat loci. Of 16 markers tested with dye-labelled primers, 11 proved to be polymorphic and 10 were readily amplified in multiplex PCR reactions. We tested 54 individuals of three species (T. lariang, T. dentatus, T. wallacei) and 10 putative hybrids for allelic diversity. All loci are genetically unlinked, one locus was found to deviate from Hardy–Weinberg equilibrium in one species. The novel marker system will aid studies of tarsier landscape genetics in the biodiversity hotspot Sulawesi.

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.

Using a genetic network to parameterize a landscape resistance surface for fishers, Martes pennanti

Knowledge of dispersal-related gene flow is important for addressing many basic and applied questions in ecology and evolution. We used landscape genetics to understand the recovery of a recently expanded population of fishers (Martes pennanti) in Ontario, Canada. An important focus of landscape genetics is modelling the effects of landscape features on gene flow. Most often resistance surfaces in landscape genetic studies are built a priori based upon nongenetic field data or expert opinion. The resistance surface that best fits genetic data is then selected and interpreted. Given inherent biases in using expert opinion or movement data to model gene flow, we sought an alternative approach. We used estimates of conditional genetic distance derived from a network of genetic connectivity to parameterize landscape resistance and build a final resistance surface based upon information-theoretic model selection and multi-model averaging. We sampled 657 fishers from 31 landscapes, genotyped them at 16 microsatellite loci, and modelled the effects of snow depth, road density, river density, and coniferous forest on gene flow. Our final model suggested that road density, river density, and snow depth impeded gene flow during the fisher population expansion demonstrating that both human impacts and seasonal habitat variation affect gene flow for fishers. Our approach to building landscape genetic resistance surfaces mitigates many of the problems and caveats associated with using either nongenetic field data or expert opinion to derive resistance surfaces.

Effect of Anthropogenic Landscape Features on Population Genetic Differentiation of Przewalski's Gazelle: Main Role of Human Settlement

Anthropogenic landscapes influence evolutionary processes such as population genetic differentiation, however, not every type of landscape features exert the same effect on a species, hence it is necessary to estimate their relative effect for species management and conservation. Przewalski's gazelle (Procapra przewalskii), which inhabits a human-altered area on Qinghai-Tibet Plateau, is one of the most endangered antelope species in the world. Here, we report a landscape genetic study on Przewalski's gazelle. We used skin and fecal samples of 169 wild gazelles collected from nine populations and thirteen microsatellite markers to assess the genetic effect of anthropogenic landscape features on this species. For comparison, the genetic effect of geographical distance and topography were also evaluated. We found significant genetic differentiation, six genetic groups and restricted dispersal pattern in Przewalski's gazelle. Topography, human settlement and road appear to be responsible for observed genetic differentiation as they were significantly correlated with both genetic distance measures [FST/(1−FST) and F′ST/(1−F′ST)] in Mantel tests. IBD (isolation by distance) was also inferred as a significant factor in Mantel tests when genetic distance was measured as FST/(1−FST). However, using partial Mantel tests, AICc calculations, causal modeling and AMOVA analysis, we found that human settlement was the main factor shaping current genetic differentiation among those tested. Altogether, our results reveal the relative influence of geographical distance, topography and three anthropogenic landscape-type on population genetic differentiation of Przewalski's gazelle and provide useful information for conservation measures on this endangered species.

Development of 21 microsatellite markers for the threatened Yarra pygmy perch (Nannoperca obscura) through 454 shot-gun pyrosequencing

Using a next generation sequencing approach, a set of 21 new microsatellites loci was developed from the threatened freshwater fish Yarra pygmy perch (YPP) Nannoperca obscura (Percichthyidae). All markers were successfully genotyped using 28 YPP kept in captivity. These animals represent an entire population rescued from the lower Murray-Darling Basin in Australia before its habitat dried out. As expected due to the critical conservation status of the population, we observed low genetic variation across most loci (mean number of alleles per locus = 2.76; mean heterozygosity = 0.28). No deviations from Hardy–Weinberg equilibrium or linkage disequilibrium were detected and only one locus (Nob30) showed evidence for null alleles. These molecular markers represent important resources for the ongoing YPP captive breeding program, and for upcoming restoration and landscape genetic studies of this species.

Where movement happens: scale-dependent landscape effects on genetic differentiation in the European tree frog

Functional connectivity among fragmented populations depends on the landscape matrix between occupied habitat patches and its effect on the frequency of animal movement and gene flow. The quantification of landscape effects on gene flow should therefore be scale-dependent. Here, we explored the impact of different spatial scales in a landscape genetic analysis of the European tree frog Hyla arborea in a fragmented landscape in Switzerland. We examined the effects of landscape elements and geographic distance on genetic differentiation at three distance classes reflecting varying frequencies of tree frog movement. We calculated pairwise FST-values and assembled 16 landscape elements within 1 km wide corridors between all pairs of tree frog breeding sites. Per distance class, we computed a multiple regression model with stepwise backward elimination and permutation testing. At distances of 2 km, geographic distance had a negative effect on gene flow as had landscape elements such as forests and roads. In general, hedgerows and various structure-rich landscape elements positively affected gene flow. As we found distinct scale-dependent landscape effects on gene flow, future landscape genetic studies should analyse the effects of landscape variables at different spatial dimensions relevant for the movement and dispersal of the study organisms. Corresponding studies should also carefully consider relevant correlations among the landscape elements tested and should preferentially replicate their analysis at the landscape-level in order to avoid idiosyncratic results owing to the particular scale and landscape studied.

Simulation modelling in landscape genetics: on the need to go further

With the emergence of landscape genetics, the basic assumptions and predictions of classical population genetic theories are being re-evaluated to account for more complex spatial and temporal dynamics. Within the last decade, there has been an exponential increase in such landscape genetic studies (Holderegger & Wagner 2006; Storfer et al. 2010), and both methodology and underlying concepts of the field are under rapid and constant development. A number of major innovations and a high level of originality are required to fully merge existing population genetic theory with landscape ecology and to develop novel statistical approaches for measuring and predicting genetic patterns. The importance of simulation studies for this specific research has been emphasized in a number of recent articles (e.g., Balkenhol et al. 2009a; Epperson et al. 2010). Indeed, many of the major questions in landscape genetics require the development and application of sophisticated simulation tools to explore gene flow, genetic drift, mutation and natural selection in landscapes with a wide range of spatial and temporal complexities. In this issue, Jaquiery et al. (2011) provide an excellent example of such a simulation study for landscape genetics. Using a metapopulation simulation design and a novel ‘scale of phenomena’ approach, Jaquiery et al. (2011) demonstrate the utility and limitations of genetic distances for inferring landscape effects on effective dispersal.

Python based GIS tools for landscape genetics: visualising genetic relatedness and measuring landscape connectivity

Summary1. Landscape genetics is an area of research that can help to understand many spatial ecological processes, but requires significant interdisciplinary collaboration. Use of geographic information system (GIS) software is essential, but requires a degree of customisation that is often beyond the non‐specialist.2. To help address this, a series of Python script based GIS tools have been developed for use in landscape genetics studies.3. The scripts convert files, visualise genetic relatedness, and measure landscape connectivity using least‐cost path analysis. The scripts are housed in an ArcToolbox that is freely available along with the underlying Python code.4. The Python scripts allow researchers to use more current software, provide the option of further development by the user community, and reduce the amount of time that would be spent developing common solutions.