Isolation By Resistance Research Articles

Walking in a heterogeneous landscape: Dispersal, gene flow and conservation implications for the giant panda in the Qinling Mountains

Understanding the interaction between life history, demography and population genetics in threatened species is critical for the conservations of viable populations. In the context of habitat loss and fragmentation, identifying the factors that underpin the structuring of genetic variation within populations can allow conservationists to evaluate habitat quality and connectivity and help to design dispersal corridors effectively. In this study, we carried out a detailed, fine‐scale landscape genetic investigation of a giant panda population from the Qinling Mountains for the first time. With a large microsatellite data set and complementary analysis methods, we examined the role of isolation‐by‐barriers (IBB), isolation‐by‐distance (IBD) and isolation‐by‐resistance (IBR) in shaping the pattern of genetic variation in this giant panda population. We found that the Qinling population comprises one continuous genetic cluster, and among the landscape hypotheses tested, gene flow was found to be correlated with resistance gradients for two topographic factors, slope aspect and topographic complexity, rather than geographical distance or barriers. Gene flow was inferred to be facilitated by easterly slope aspect and to be constrained by topographically complex landscapes. These factors are related to benign microclimatic conditions for both the pandas and the food resources they rely on and more accessible topographic conditions for movement, respectively. We identified optimal corridors based on these results, aiming to promote gene flow between human‐induced habitat fragments. These findings provide insight into the permeability and affinities of giant panda habitats and offer important reference for the conservation of the giant panda and its habitat.

Landscape heterogeneity and ecological niche isolation shape the distribution of spatial genetic variation in Iranian brown bears, Ursus arctos (Carnivora: Ursidae)

The formerly large continuous range of brown bears in Iran has become confined to fragmented patches due to habitat conversion. Little is known about population genetic diversity, spatial genetic structure, and the consequences of geographic and ecological isolation on spatial genetic variations in Iranian bears. Literature is generally sparse on the effects of isolation by distance (IBD), isolation by resistance (IBR), isolation by environment (IBE), and ecological niche isolation on genetic differentiations of large-bodied carnivores. In this study, we investigated population structure, landscape connectivity, and genetic variations of Iranian brown bear populations using microsatellites. We tested the effects of IBD, IBR, and IBE on the genetic structure using multiple matrix randomized regression (MMRR) in an individual-based approach. A population level method based on an ecological niche modelling (ENM) framework was then used to evaluate the effect of niche divergence on genetic patterns. Bear populations displayed high genetic diversity, among the highest reported for wild brown bears. We also found a relatively significant division of brown bear populations, as well as higher effect of IBR than IBD and IBE, demonstrating the influence of landscape resistance in shaping spatial genetic variations. The results of niche comparisons among brown bear groups showed low niche overlap, and a probable phylogenetic conservatism event. We concluded that a combination of landscape resistance, ecological niche divergence, and probably mate-based dispersal behavior are affecting the gene flow of bear populations. Conservation planning of this vulnerable species should include landscape linkages to maintain gene flow among the isolated populations.

Quaternary climate instability is correlated with patterns of population genetic variability in Bombus huntii.

Climate oscillations have left a significant impact on the patterns of genetic diversity observed in numerous taxa. In this study, we examine the effect of Quaternary climate instability on population genetic variability of a bumble bee pollinator species, Bombus huntii in western North America. Pleistocene and contemporary B. huntii habitat suitability (HS) was estimated with an environmental niche model (ENM) by associating 1,035 locality records with 10 bioclimatic variables. To estimate genetic variability, we genotyped 380 individuals from 33 localities at 13 microsatellite loci. Bayesian inference was used to examine population structure with and without a priori specification of geographic locality. We compared isolation by distance (IBD) and isolation by resistance (IBR) models to examine population differentiation within and among the Bayesian inferred genetic clusters. Furthermore, we tested for the effect of environmental niche stability (ENS) on population genetic diversity with linear regression. As predicted, high‐latitude B. huntii habitats exhibit low ENS when compared to low‐latitude habitats. Two major genetic clusters of B. huntii inhabit western North America: (a) a north genetic cluster predominantly distributed north of 28°N and (b) a south genetic cluster distributed south of 28°N. In the south genetic cluser, both IBD and IBR models are significant. However, in the north genetic cluster, IBD is significant but not IBR. Furthermore, the IBR models suggest that low‐latitude montane populations are surrounded by habitat with low HS, possibly limiting dispersal, and ultimately gene flow between populations. Finally, we detected high genetic diversity across populations in regions that have been climatically unstable since the last glacial maximum (LGM), and low genetic diversity across populations in regions that have been climatically stable since the LGM. Understanding how species have responded to climate change has the potential to inform management and conservation decisions of both ecological and economic concerns.

Does silvoagropecuary landscape fragmentation affect the genetic diversity of the sigmodontine rodent Oligoryzomys longicaudatus?

BackgroundFragmentation of native forests is a highly visible result of human land-use throughout the world. In this study, we evaluated the effects of landscape fragmentation and matrix features on the genetic diversity and structure of Oligoryzomys longicaudatus, the natural reservoir of Hantavirus in southern South America. We focused our work in the Valdivian Rainforest where human activities have produced strong change of natural habitats, with an important number of human cases of Hantavirus.MethodsWe sampled specimens of O. longicaudatus from five native forest patches surrounded by silvoagropecuary matrix from Panguipulli, Los Rios Region, Chile. Using the hypervariable domain I (mtDNA), we characterized the genetic diversity and evaluated the effect of fragmentation and landscape matrix on the genetic structure of O. longicaudatus. For the latter, we used three approaches: (i) Isolation by Distance (IBD) as null model, (ii) Least-cost Path (LCP) where genetic distances between patch pairs increase with cost-weighted distances, and (iii) Isolation by Resistance (IBR) where the resistance distance is the average number of steps that is needed to commute between the patches during a random walk.ResultsWe found low values of nucleotide diversity (π) for the five patches surveyed, ranging from 0.012 to 0.015, revealing that the 73 sampled specimens of this study belong to two populations but with low values of genetic distance (γST) ranging from 0.022 to 0.099. Likewise, we found that there are no significant associations between genetic distance and geographic distance for IBD and IBR. However, we found for the LCP approach, a significant positive relationship (r = 0.737, p = 0.05), with shortest least-cost paths traced through native forest and arborescent shrublands.DiscussionIn this work we found that, at this reduced geographical scale, Oligoryzomys longicaudatus shows genetic signs of fragmentation. In addition, we found that connectivity between full growth native forest remnants is mediated by the presence of dense shrublands and native forest corridors. In this sense, our results are important because they show how native forest patches and associated routes act as source of vector species in silvoagropecuary landscape, increasing the infection risk on human population. This study is the first approach to understand the epidemiological spatial context of silvoagropecuary risk of Hantavirus emergence. Further studies are needed to elucidate the effects of landscape fragmentation in order to generate new predictive models based on vector intrinsic attributes and landscape features.

Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution

Genetic differentiation among populations may arise from the disruption of gene flow due to local adaptation to distinct environments and/or neutral accumulation of mutations and genetic drift resulted from geographical isolation. Quantifying the role of these processes in determining the genetic structure of natural populations remains challenging. Here, we analyze the relative contribution of isolation‐by‐resistance (IBR), isolation‐by‐environment (IBE), genetic drift and historical isolation in allopatry during Pleistocene glacial cycles on shaping patterns of genetic differentiation in caribou/reindeer populations Rangifer tarandus across the entire distribution range of the species. Our study integrates analyses at range‐wide and regional scales to partial out the effects of historical and contemporary isolation mechanisms. At the circumpolar scale, our results indicate that genetic differentiation is predominantly explained by IBR and historical isolation. At a regional scale, we found that IBR, IBE and population size significantly explained the spatial distribution of genetic variation among populations belonging to the Euro‐Beringian lineage within North America. In contrast, genetic differentiation among populations within the North American lineage was predominantly explained by IBR and population size, but not IBE. We also found discrepancies between genetic and ecotype designation across the Holarctic species distribution range. Overall, these results indicate that multiple isolating mechanisms have played roles in shaping the spatial distribution of genetic variation across the distribution range of a large mammal with high potential for gene flow. Considering multiple spatial scales and simultaneously testing a comprehensive suite of potential isolating mechanisms, our study contributes to understand the ecological and evolutionary processes underlying organism–landscape interactions.

Effect of landscape features on genetic structure of the goitered gazelle (Gazella subgutturosa) in Central Iran

The populations of goitered gazelle suffered significant decline due to natural and anthropogenic factors over the last century. Investigating the effects of barriers on gene flow among the remaining populations is vital for conservation planning. Here we adopted a landscape genetics approach to evaluate the genetic structure of the goitered gazelle in Central Iran and the effects of landscape features on gene flow using 15 polymorphic microsatellite loci. Spatial autocorrelation, isolation by distance (IBD) and isolation by resistance (IBR) models were used to elucidate the effects of landscape features on the genetic structure. Ecological modeling was used to construct landscape permeability and resistance map using 12 ecogeographical variables. Bayesian algorithms revealed three genetically homogeneous groups and restricted dispersal pattern in the six populations. The IBD and spatial autocorrelation revealed a pattern of decreasing relatedness with increasing distance. The distribution of potential habitats was strongly correlated with bioclimatic factors, vegetation type, and elevation. Resistance distances and graph theory were significantly related with variation in genetic structure, suggesting that gazelles are affected by landscape composition. The IBD showed greater impact on genetic structure than IBR. The Mantel and partial Mantel tests indicated low but non-significant effects of anthropogenic barriers on observed genetic structure. We concluded that a combination of geographic distance, landscape resistance, and anthropogenic factors are affecting the genetic structure and gene flow of populations. Future road construction might impede connectivity and gene exchange of populations. Conservation measures on this vulnerable species should consider some isolated population as separate management units.

Landscape determinants of genetic differentiation, inbreeding and genetic drift in the hazel dormouse (Muscardinus avellanarius)

The dispersal process is crucial in determining the fate of populations over time, but habitat fragmentation limits or prevents it. Landscape genetic is an effective tool to assess the degree to which dispersal still occurs in fragmented landscapes. The purpose of this study was to investigate the landscape determinants of genetic differentiation in the hazel dormouse (Muscardinus avellanarius), a forest-dependent species of conservation concern. By comparing subpopulations in a continuous (SLR) and a fragmented (VTH) population, we (i) searched for the presence of Isolation-by-Resistance (IBR); (ii) estimated migration rates; (iii) evaluated the degree of inbreeding and genetic drift, and searched for their landscape determinants. We found an IBR effect in VTH, which heavily hindered the dispersal process. The overall number of migrants among VTH subpopulations was very low (1 per generation, compared to 15 in SLR), although a between-patch displacement of about 4 km along a well-structured hedgerow probably occurred. The inbreeding (F > 0.2 in most subpopulations) and the genetic drift (four out five subpopulations showed private alleles on several loci, with relatively high frequencies) are of particular concern in VTH. However, they were found to be limited in large patches or in patches connected by hedgerows with a high number of neighbouring patches. As a conservation strategy in the VTH landscape, characterized by small patches, we suggest that the dispersal process among subpopulations is enhanced to sustain a functional metapopulation. For this purpose, an effective ecological network should be created by enhancing the continuity and the internal features of hedgerows.

Fine-scale genetic structure of the ringtail (Bassariscus astutus) in a Sky Island mountain range

Landscape complexity provides opportunities for local adaptation and creates population genetic structure at limited geographic scales. We determined if fine-scale genetic structure was evident in a population of ringtails (Bassariscus astutus) inhabiting the Guadalupe Mountains, a small, isolated, and ecologically diverse mountain range in the southwest United States. We hypothesized that ringtails would exhibit either a genetic pattern of isolation by distance (IBD), because their small body size would most likely limit dispersal distances, or a pattern of isolation by resistance (IBR), because the topographical complexity of the mountain range would result in complex dispersal patterns. To investigate for the presence of fine-scale genetic structure in this population, we genotyped 153 ringtails at 15 microsatellite loci and described genetic structure using 2 Bayesian clustering techniques. Six genetic clusters were identified revealing complex spatial genetic structure within a localized geographic a...

Dispersal constraints and fine-scale spatial genetic structure in two earthworm species

The limited dispersal ability of earthworms is expected to result in marked genetic isolation by distance and remarkable spatial patterns of genetic variation. To test this hypothesis, we investigated, using microsatellite loci, the spatial genetic structure of two earthworm species, Allolobophora chlorotica and Aporrectodea icterica, in two plots of less than 1 ha where a total of 282 individuals were collected. We used spatial autocorrelation statistics, partial Mantel tests of isolation-by-distance (IBD) and isolation-by-resistance (IBR), and Bayesian test of clustering to explore recent patterns involved in the observed genetic structure. For A. icterica, a low signal of genetic structure was detected, which may be explained by an important dispersal capacity and/or by the low polymorphism of the microsatellite loci. For A. chlorotica, a weak, but significant, pattern of IBD associated with positive autocorrelation was observed in one of the plots. In the other plot, which had been recently ploughed, two genetically differentiated clusters were identified. These results suggest a spatial neighbourhood structure in A. chlorotica, with neighbour individuals that tend to be more genetically similar to one another, and also highlight that habitat perturbation as a result of human activities may deeply alter the genetic structure of earthworm species, even at a very small scale. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114, 335–347.

Climatically stable landscapes predict patterns of genetic structure and admixture in the Californian canyon live oak

AbstractAimWe studied which factors shape contemporary patterns of genetic structure, diversity and admixture in the canyon live oak (Quercus chrysolepis). Specifically, we tested two alternative hypotheses: (1) that areas with high habitat suitability and stability since the Last Glacial Maximum (LGM) sustain higher effective population sizes, resulting in increased levels of genetic diversity; and (2) that populations from areas with lower habitat stability show higher levels of genetic admixture due to their recurrent colonization by individuals originating from genetically differentiated populations. Furthermore, we analysed the relative importance of past and current habitat suitability and their additive effects on contemporary patterns of genetic structure.LocationCalifornia, USA.MethodsWe sampled 160 individuals from 33 localities across the distribution range of the canyon live oak in California and then combined information from 13 nuclear microsatellite DNA markers and climate niche modelling to study patterns of genetic variation in this species. We used Bayesian clustering analyses to analyse geographical patterns of genetic structure and admixture, and circuit theory to generate isolation‐by‐resistance (IBR) distance matrices.ResultsWe found that the degree of genetic admixture was higher in localities with lower inferred population stability, but that genetic diversity was not associated with habitat suitability or stability. Landscape genetic analyses identified habitat stability as the primary driver of population genetic differentiation.Main conclusionsThis study shows that habitat stability can be a major factor shaping genetic variation in wind‐pollinated trees and supports the idea that stable regions contribute to genetic connectivity across different climatic periods. To our knowledge, this study is the first to report an association between patterns of genetic admixture and stability of local habitat.

Landscape influences on dispersal behaviour: a theoretical model and empirical test using the fire salamander, Salamandra infraimmaculata

When populations reside within a heterogeneous landscape, isolation by distance may not be a good predictor of genetic divergence if dispersal behaviour and therefore gene flow depend on landscape features. Commonly used approaches linking landscape features to gene flow include the least cost path (LCP), random walk (RW), and isolation by resistance (IBR) models. However, none of these models is likely to be the most appropriate for all species and in all environments. We compared the performance of LCP, RW and IBR models of dispersal with the aid of simulations conducted on artificially generated landscapes. We also applied each model to empirical data on the landscape genetics of the endangered fire salamander, Salamandra infraimmaculata, in northern Israel, where conservation planning requires an understanding of the dispersal corridors. Our simulations demonstrate that wide dispersal corridors of the low-cost environment facilitate dispersal in the IBR model, but inhibit dispersal in the RW model. In our empirical study, IBR explained the genetic divergence better than the LCP and RW models (partial Mantel correlation 0.413 for IBR, compared to 0.212 for LCP, and 0.340 for RW). Overall dispersal cost in salamanders was also well predicted by landscape feature slope steepness (76%), and elevation (24%). We conclude that fire salamander dispersal is well characterised by IBR predictions. Together with our simulation findings, these results indicate that wide dispersal corridors facilitate, rather than hinder, salamander dispersal. Comparison of genetic data to dispersal model outputs can be a useful technique in inferring dispersal behaviour from population genetic data.

Using multilevel models to identify drivers of landscape‐genetic structure among management areas

Landscape genetics offers a powerful approach to understanding species' dispersal patterns. However, a central obstacle is to account for ecological processes operating at multiple spatial scales, while keeping research outcomes applicable to conservation management. We address this challenge by applying a novel multilevel regression approach to model landscape drivers of genetic structure at both the resolution of individuals and at a spatial resolution relevant to management (i.e. local government management areas: LGAs) for the koala (Phascolartos cinereus) in Australia. Our approach allows for the simultaneous incorporation of drivers of landscape-genetic relationships operating at multiple spatial resolutions. Using microsatellite data for 1106 koalas, we show that, at the individual resolution, foliage projective cover (FPC) facilitates high gene flow (i.e. low resistance) until it falls below approximately 30%. Out of six additional land-cover variables, only highways and freeways further explained genetic distance after accounting for the effect of FPC. At the LGA resolution, there was significant variation in isolation-by-resistance (IBR) relationships in terms of their slopes and intercepts. This was predominantly explained by the average resistance distance among LGAs, with a weaker effect of historical forest cover. Rates of recent landscape change did not further explain variation in IBR relationships among LGAs. By using a novel multilevel model, we disentangle the effect of landscape resistance on gene flow at the fine resolution (i.e. among individuals) from effects occurring at coarser resolutions (i.e. among LGAs). This has important implications for our ability to identify appropriate scale-dependent management actions.

Urban landscape genetics: canopy cover predicts gene flow between white‐footed mouse (Peromyscus leucopus) populations in New York City

In this study, I examine the influence of urban canopy cover on gene flow between 15 white-footed mouse (Peromyscus leucopus) populations in New York City parklands. Parks in the urban core are often highly fragmented, leading to rapid genetic differentiation of relatively nonvagile species. However, a diverse array of 'green' spaces may provide dispersal corridors through 'grey' urban infrastructure. I identify urban landscape features that promote genetic connectivity in an urban environment and compare the success of two different landscape connectivity approaches at explaining gene flow. Gene flow was associated with 'effective distances' between populations that were calculated based on per cent tree canopy cover using two different approaches: (i) isolation by effective distance (IED) that calculates the single best pathway to minimize passage through high-resistance (i.e. low canopy cover) areas, and (ii) isolation by resistance (IBR), an implementation of circuit theory that identifies all low-resistance paths through the landscape. IBR, but not IED, models were significantly associated with three measures of gene flow (Nm from F(ST) , BayesAss+ and Migrate-n) after factoring out the influence of isolation by distance using partial Mantel tests. Predicted corridors for gene flow between city parks were largely narrow, linear parklands or vegetated spaces that are not managed for wildlife, such as cemeteries and roadway medians. These results have implications for understanding the impacts of urbanization trends on native wildlife, as well as for urban reforestation efforts that aim to improve urban ecosystem processes.

ISOLATION BY RESISTANCE

Despite growing interest in the effects of landscape heterogeneity on genetic structuring, few tools are available to incorporate data on landscape composition into population genetic studies. Analyses of isolation by distance have typically either assumed spatial homogeneity for convenience or applied theoretically unjustified distance metrics to compensate for heterogeneity. Here I propose the isolation-by-resistance (IBR) model as an alternative for predicting equilibrium genetic structuring in complex landscapes. The model predicts a positive relationship between genetic differentiation and the resistance distance, a distance metric that exploits precise relationships between random walk times and effective resistances in electronic networks. As a predictor of genetic differentiation, the resistance distance is both more theoretically justified and more robust to spatial heterogeneity than Euclidean or least cost path-based distance measures. Moreover, the metric can be applied with a wide range of data inputs, including coarse-scale range maps, simple maps of habitat and nonhabitat within a species' range, or complex spatial datasets with habitats and barriers of differing qualities. The IBR model thus provides a flexible and efficient tool to account for habitat heterogeneity in studies of isolation by distance, improve understanding of how landscape characteristics affect genetic structuring, and predict genetic and evolutionary consequences of landscape change.

ISOLATION BY RESISTANCE

Despite growing interest in the effects of landscape heterogeneity on genetic structuring, few tools are available to incorporate data on landscape composition into population genetic studies. Analyses of isolation by distance have typically either assumed spatial homogeneity for convenience or applied theoretically unjustified distance metrics to compensate for heterogeneity. Here I propose the isolation-by-resistance (IBR) model as an alternative for predicting equilibrium genetic structuring in complex landscapes. The model predicts a positive relationship between genetic differentiation and the resistance distance, a distance metric that exploits precise relationships between random walk times and effective resistances in electronic networks. As a predictor of genetic differentiation, the resistance distance is both more theoretically justified and more robust to spatial heterogeneity than Euclidean or least cost path-based distance measures. Moreover, the metric can be applied with a wide range of data inputs, including coarse-scale range maps, simple maps of habitat and nonhabitat within a species' range, or complex spatial datasets with habitats and barriers of differing qualities. The IBR model thus provides a flexible and efficient tool to account for habitat heterogeneity in studies of isolation by distance, improve understanding of how landscape characteristics affect genetic structuring, and predict genetic and evolutionary consequences of landscape change.