Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change

Landscape genetics seeks to determine the effect of landscape features on gene flow and genetic structure. Often, such analyses are intended to inform conservation and management. However, depending on the many factors that influence the time to reach equilibrium, genetic structure may more strongly represent past rather than contemporary landscapes. This well‐known lag between current demographic processes and population genetic structure often makes it challenging to interpret how contemporary landscapes and anthropogenic activity shape gene flow. Here, we review the theoretical framework for factors that influence time lags, summarize approaches to address this temporal disconnect in landscape genetic studies, and evaluate ways to make inferences about landscape change and its effects on species using genetic data alone or in combination with other data. Those approaches include comparing correlation of genetic structure with historical versus contemporary landscapes, using molecular markers with different rates of evolution, contrasting metrics of genetic structure and gene flow that reflect population genetic processes operating at different temporal scales, comparing historical and contemporary samples, combining genetic data with contemporary estimates of species distribution or movement, and controlling for phylogeographic history. We recommend using simulated data sets to explore time lags in genetic structure, and argue that time lags should be explicitly considered both when designing and interpreting landscape genetic studies. We conclude that the time lag problem can be exploited to strengthen inferences about recent landscape changes and to establish conservation baselines, particularly when genetic data are combined with other data.     

Choosing appropriate genetic markers and analytical methods for testing landscape genetic hypotheses

Landscape genetics and phylogeography both examine population‐level microevolutionary processes, such as population structure and gene flow, in the context of environmental and geographic variation. They differ in terms of the spatial and temporal scales they typically investigate, meaning that different genetic markers and analytical methods are better suited for testing the different hypotheses typically posed by each discipline. In a recent comment, Bohonak & Vandergast (2011) argue that I overlooked the value of mtDNA for landscape genetics in an article I published last year in Molecular Ecology (Wang 2010) and that a gap between landscape genetics and phylogeography, which I outlined, does not exist. Here, I clarify several points in my original article and summarize the commonly held viewpoint that different genetic markers are appropriate for drawing inferences at different temporal scales.     

Using neutral cline decay to estimate contemporary dispersal: a generic tool and its application to a major crop pathogen

Dispersal is a key parameter of adaptation, invasion and persistence. Yet standard population genetics inference methods hardly distinguish it from drift and many species cannot be studied by direct mark‐recapture methods. Here, we introduce a method using rates of change in cline shapes for neutral markers to estimate contemporary dispersal. We apply it to the devastating banana pest Mycosphaerella fijiensis, a wind‐dispersed fungus for which a secondary contact zone had previously been detected using landscape genetics tools. By tracking the spatio‐temporal frequency change of 15 microsatellite markers, we find that σ, the standard deviation of parent–offspring dispersal distances, is 1.2 km/generation^1/2. The analysis is further shown robust to a large range of dispersal kernels. We conclude that combining landscape genetics approaches to detect breaks in allelic frequencies with analyses of changes in neutral genetic clines offers a powerful way to obtain ecologically relevant estimates of dispersal in many species.     

Spatiotemporally explicit demographic modelling supports a joint effect of historical barriers to dispersal and contemporary landscape composition on structuring genomic variation in a red‐listed grasshopper

Inferring the processes underlying spatial patterns of genomic variation is fundamental to understand how organisms interact with landscape heterogeneity and to identify the factors determining species distributional shifts. Here, we use genomic data (restriction site‐associated DNA sequencing) to test biologically informed models representing historical and contemporary demographic scenarios of population connectivity for the Iberian cross‐backed grasshopper Dociostaurus hispanicus, a species with a narrow distribution that currently forms highly fragmented populations. All models incorporated biological aspects of the focal taxon that could hypothetically impact its geographical patterns of genomic variation, including (a) spatial configuration of impassable barriers to dispersal defined by topographic landscapes not occupied by the species; (b) distributional shifts resulting from the interaction between the species bioclimatic envelope and Pleistocene glacial cycles; and (c) contemporary distribution of suitable habitats after extensive land clearing for agriculture. Spatiotemporally explicit simulations under different scenarios considering these aspects and statistical evaluation of competing models within an Approximate Bayesian Computation framework supported spatial configuration of topographic barriers to dispersal and human‐driven habitat fragmentation as the main factors explaining the geographical distribution of genomic variation in the species, with no apparent impact of hypothetical distributional shifts linked to Pleistocene climatic oscillations. Collectively, this study supports that both historical (i.e., topographic barriers) and contemporary (i.e., anthropogenic habitat fragmentation) aspects of landscape composition have shaped major axes of genomic variation in the studied species and emphasizes the potential of model‐based approaches to gain insights into the temporal scale at which different processes impact the demography of natural populations.     

A landscape genetics approach for quantifying the relative influence of historic and contemporary habitat heterogeneity on the genetic connectivity of a rainforest bird

Landscape genetics is an important framework for investigating the influence of spatial pattern on ecological process. Nevertheless, the standard analytic frameworks in landscape genetics have difficulty evaluating hypotheses about spatial processes in dynamic landscapes. We use a predictive hypothesis-driven approach to quantify the relative contribution of historic and contemporary processes to genetic connectivity. By confronting genetic data with models of historic and contemporary landscapes, we identify dispersal processes operating in naturally heterogeneous and human-altered systems. We demonstrate the approach using a case study of microsatellite polymorphism and indirect estimates of gene flow for a rainforest bird, the logrunner ( Orthonyx temminckii ). Of particular interest was how much information in the genetic data was attributable to processes occurring in the reconstructed historic landscape and contemporary human-modified landscape. A linear mixed model was used to estimate appropriate sampling variance from nonindependent data and information-theoretic model selection provided strength of evidence for alternative hypotheses. The contemporary landscape explained slightly more information in the genetic differentiation data than the historic landscape, and there was considerable evidence for a temporal shift in dispersal pattern. In contrast, migration rates estimated from genealogical information were primarily influenced by contemporary landscape change. We discovered that landscape heterogeneity facilitated gene flow before European settlement, but contemporary deforestation is rapidly becoming the most important barrier to logrunner dispersal.     

Tracking climate change in a dispersal-limited species: reduced spatial and genetic connectivity in a montane salamander

Tropical montane taxa are often locally adapted to very specific climatic conditions, contributing to their lower dispersal potential across complex landscapes. Climate and landscape features in montane regions affect population genetic structure in predictable ways, yet few empirical studies quantify the effects of both factors in shaping genetic structure of montane-adapted taxa. Here, we considered temporal and spatial variability in climate to explain contemporary genetic differentiation between populations of the montane salamander, Pseudoeurycea leprosa. Specifically, we used ecological niche modelling (ENM) and measured spatial connectivity and gene flow (using both mtDNA and microsatellite markers) across extant populations of P. leprosa in the Trans-Mexican Volcanic Belt (TVB). Our results indicate significant spatial and genetic isolation among populations, but we cannot distinguish between isolation by distance over time or current landscape barriers as mechanisms shaping population genetic divergences. Combining ecological niche modelling, spatial connectivity analyses, and historical and contemporary genetic signatures from different classes of genetic markers allows for inference of historical evolutionary processes and predictions of the impacts future climate change will have on the genetic diversity of montane taxa with low dispersal rates. Pseudoeurycea leprosa is one montane species among many endemic to this region and thus is a case study for the continued persistence of spatially and genetically isolated populations in the highly biodiverse TVB of central Mexico.     

GENE TREES AND ORGANISMAL HISTORIES: A PHYLOGENETIC APPROACH TO POPULATION BIOLOGY

A “gene tree” is the phylogeny of alleles or haplotypes for any specified stretch of DNA. Gene trees are components of population trees or species trees; their analysis entails a shift in perspective from many of the familiar models and concepts of population genetics, which typically deal with frequencies of phylogenetically unordered alleles. Molecular surveys of haplotype diversity in mitochondrial DNA (mtDNA) have provided the first extensive empirical data suitable for estimation of gene trees on a microevolutionary (intraspecific) scale. The relationship between phylogeny and geographic distribution constitutes the phylogeographic pattern for any species. Observed phylogeographic trees can be interpreted in terms of historical demography by comparison to predictions derived from models of gene lineage sorting, such as inbreeding theory and branching-process theory. Results of such analyses for more than 20 vertebrate species strongly suggest that the demographies of populations have been remarkably dynamic and unsettled over space and recent evolutionary time. This conclusion is consistent with ecological observations documenting dramatic population-size fluctuations and range shifts in many contemporary species. By adding an historical perspective to population biology, the gene-lineage approach can help forge links between the disciplines of phylogenetic systematics (and macroevolutionary study) and population genetics (microevolution). Preliminary extensions of the “gene tree” methodology to haplotypes of nuclear genes (such as Adh in Drosophila melanogaster) demonstrate that the phylogenetic perspective can also help to illuminate molecular-genetic processes (such as recombination or gene conversion), as well as contribute to knowledge of the origin, age, and molecular basis of particular adaptations.     

THE EVOLUTION OF LANDSCAPE GENETICS

The main objective of this special section is not to review the broad field of landscape genetics, but to provide a glimpse of how the developing landscape genetics perspective has the potential to change the way we study evolution. Evolutionary landscape genetics is the study of how migration and population structure affects evolutionary processes. As a field it dates back to Sewall Wright and the origin of theoretical population genetics, but empirical tests of adaptive processes of evolution in natural landscapes have been rare. Now, with recent developments in technology, methodology, and modeling tools, we are poised to trace adaptive genetic variation across space and through time. Not only will we see more empirical tests of classical theory, we can expect to see new phenomena emerging, as we reveal complex interactions among evolutionary processes as they unfold in natural landscapes.     

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, Jaquiéry 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, Jaquiéry et al. (2011) demonstrate the utility and limitations of genetic distances for inferring landscape effects on effective dispersal.     

Patterns of weed invasion: evidence from the spatial genetic structure of Raphanus raphanistrum

Knowledge of the pathways of colonization is critical for risk assessment and management of weeds. In this study we adopted a landscape genetics approach to assess the impact of human disturbances and large-scale environmental features on the colonization of a global agricultural weed, Raphanus raphanistrum. We used nuclear microsatellite and chloroplast DNA sequence data to quantify the pattern of genetic diversity in 336 plants collected from 13 sites throughout the Cape Floristic Region, South Africa, one of the world’s recognized global biodiversity hotspots. The lack of strong spatial genetic structure suggests that R. raphanistrum colonized throughout the Cape Floristic Region via both local diffusive spread and long-distance jump dispersal. Furthermore, 47 % of analyzed plants contained Raphanus sativus (cultivated radish) chloroplast genomes, indicating historical and/or contemporary gene flow between wild and cultivated radish populations. The prevalence of high genetic diversity and long-distance gene flow are discussed in the context of ecological risk assessment.     

Quantifying past and present connectivity illuminates a rapidly changing landscape for the African elephant

There is widespread concern about impacts of land‐use change on connectivity among animal and plant populations, but those impacts are difficult to quantify. Moreover, lack of knowledge regarding ecosystems before fragmentation may obscure appropriate conservation targets. We use occurrence and population genetic data to contrast connectivity for a long‐lived mega‐herbivore over historical and contemporary time frames. We test whether (i) historical gene flow is predicted by persistent landscape features rather than human settlement, (ii) contemporary connectivity is most affected by human settlement and (iii) recent gene flow estimates show the effects of both factors. We used 16 microsatellite loci to estimate historical and recent gene flow among African elephant (Loxodonta africana) populations in seven protected areas in Tanzania, East Africa. We used historical gene flow (F_ST and G'_ST) to test and optimize models of historical landscape resistance to movement. We inferred contemporary landscape resistance from elephant resource selection, assessed via walking surveys across ~15 400 km² of protected and unprotected lands. We used assignment‐based recent gene flow estimates to optimize and test the contemporary resistance model, and to test a combined historical and contemporary model. We detected striking changes in connectivity. Historical connectivity among elephant populations was strongly influenced by slope but not human settlement, whereas contemporary connectivity was influenced most by human settlement. Recent gene flow was strongly influenced by slope but was also correlated with contemporary resistance. Inferences across multiple timescales can better inform conservation efforts on large and complex landscapes, while mitigating the fundamental problem of shifting baselines in conservation.     

Genomic signatures of population bottleneck and recovery in Northwest Atlantic pinnipeds

Population increases over the past several decades provide natural settings in which to study the evolutionary processes that occur during bottleneck, growth, and spatial expansion. We used parallel natural experiments of historical decline and subsequent recovery in two sympatric pinniped species in the Northwest Atlantic, the gray seal (Halichoerus grypus atlantica) and harbor seal (Phoca vitulina vitulina), to study the impact of recent demographic change in genomic diversity. Using restriction site‐associated DNA sequencing, we assessed genomic diversity at over 8,700 polymorphic gray seal loci and 3,700 polymorphic harbor seal loci in samples from multiple cohorts collected throughout recovery over the past half‐century. Despite significant differences in the degree of genetic diversity assessed in the two species, we found signatures of historical bottlenecks in the contemporary genomes of both gray and harbor seals. We evaluated temporal trends in diversity across cohorts, as well as compared samples from sites at both the center and edge of a recent gray seal range expansion, but found no significant change in genomewide diversity following recovery. We did, however, find that the variance and degree of allele frequency change measured over the past several decades were significantly different from neutral expectations of drift under population growth. These two cases of well‐described demographic history provide opportunities for critical evaluation of current approaches to simulating and understanding the genetic effects of historical demographic change in natural populations.     

Evaluating methods to visualize patterns of genetic differentiation on a landscape

With advances in sequencing technology, research in the field of landscape genetics can now be conducted at unprecedented spatial and genomic scales. This has been especially evident when using sequence data to visualize patterns of genetic differentiation across a landscape due to demographic history, including changes in migration. Two recent model‐based visualization methods that can highlight unusual patterns of genetic differentiation across a landscape, SpaceMix and EEMS, are increasingly used. While SpaceMix's model can infer long‐distance migration, EEMS’ model is more sensitive to short‐distance changes in genetic differentiation, and it is unclear how these differences may affect their results in various situations. Here, we compare SpaceMix and EEMS side by side using landscape genetics simulations representing different migration scenarios. While both methods excel when patterns of simulated migration closely match their underlying models, they can produce either un‐intuitive or misleading results when the simulated migration patterns match their models less well, and this may be difficult to assess in empirical data sets. We also introduce unbundled principal components (un‐PC), a fast, model‐free method to visualize patterns of genetic differentiation by combining principal components analysis (PCA), which is already used in many landscape genetics studies, with the locations of sampled individuals. Un‐PC has characteristics of both SpaceMix and EEMS and works well with simulated and empirical data. Finally, we introduce msLandscape, a collection of tools that streamline the creation of customizable landscape‐scale simulations using the popular coalescent simulator ms and conversion of the simulated data for use with un‐PC, SpaceMix and EEMS.     

Echoes of a distant time: effects of historical processes on contemporary genetic patterns in Galaxias platei in Patagonia

Interpreting the genetic structure of a metapopulation as the outcome of gene flow over a variety of timescales is essential for the proper understanding of how changes in landscape affect biological connectivity. Here we contrast historical and contemporary connectivity in two metapopulations of the freshwater fish Galaxias platei in northern and southernmost Patagonia where paleolakes existed during the Holocene and Pleistocene, respectively. Contemporary gene flow was mostly high and asymmetrical in the northern system while extremely reduced in the southernmost system. Historical migration patterns were high and symmetric in the northern system and high and largely asymmetric in the southern system. Both systems showed a moderate structure with a clear pattern of isolation by distance (IBD). Effective population sizes were smaller in populations with low contemporary gene flow. An approximate Bayesian computation (ABC) approach suggests a late Holocene colonization of the lakes in the northern system and recent divergence of the populations from refugial populations from east and west of the Andes. For the southern system, the ABC approach reveals that some of the extant G. platei populations most likely derive from an ancestral population inhabiting a large Pleistocene paleolake while the rest derive from a higher‐altitude lake. Our results suggest that neither historical nor contemporary processes individually fully explain the observed structure and geneflow patterns and both are necessary for a proper understanding of the factors that affect diversity and its distribution. Our study highlights the importance of a temporal perspective on connectivity to analyse the diversity of spatially complex metapopulations.     

景观遗传学：概念与方法

全球变化下的物种栖息地丧失和破碎化给生物多样性保护带来了新的问题和挑战,生物多样性保护必须由单纯的物种保护上升到栖息地景观的保护。景观遗传学是定量确定栖息地景观特征对种群遗传结构影响的一门交叉学科,在生物保护及自然保护区管理方面有巨大的潜力。从生物多样性保护的角度评述了景观结构与遗传多样性的关系,介绍了景观遗传学的基本概念,研究尺度和方法,并对景观遗传学当前的研究焦点及面临的挑战做了总结。     

Higher genetic diversity on mountain tops: the role of historical and contemporary processes in shaping genetic variation in the bank vole

Glacial phases during the Pleistocene caused remarkable changes in species range distributions, with inevitable genetic consequences. Specifically, during interglacial phases, when the ice melted and new habitats became suitable again, species could recolonize regions that were previously covered by ice, such as high latitudes and elevations. Based on theoretical models and empirical data, a decrease in genetic variation is predicted along recolonization routes as a result of the consecutive founder effects that characterize the recolonization process. In the present study, we assessed the relative importance of historical and contemporary processes in shaping genetic diversity and differentiation of bank vole (Myodes glareolus) populations at different elevations in the Swiss Alps. By contrast to expectations, we found that genetic variation increased with elevation. Estimates of recent migration rates and a contrasting pattern of genetic differentiation observed at the mitochondrial cytochrome b gene and nuclear microsatellites support the hypothesis that higher genetic diversity at high elevation results from contemporary gene flow. Although historical recolonization processes can have marked effects on the genetic structure of populations, the present study provides an example where contemporary processes along an environmental gradient can reverse predicted patterns of genetic variation.     

Spatiotemporal analysis of gene flow in Chesapeake Bay Diamondback Terrapins (Malaclemys terrapin)

There is widespread concern regarding the impacts of anthropogenic activities on connectivity among populations of plants and animals, and understanding how contemporary and historical processes shape metapopulation dynamics is crucial for setting appropriate conservation targets. We used genetic data to identify population clusters and quantify gene flow over historical and contemporary time frames in the Diamondback Terrapin (Malaclemys terrapin). This species has a long and complicated history with humans, including commercial overharvesting and subsequent translocation events during the early twentieth century. Today, terrapins face threats from habitat loss and mortality in fisheries bycatch. To evaluate population structure and gene flow among Diamondback Terrapin populations in the Chesapeake Bay region, we sampled 617 individuals from 15 localities and screened individuals at 12 polymorphic microsatellite loci. Our goals were to demarcate metapopulation structure, quantify genetic diversity, estimate effective population sizes, and document temporal changes in gene flow. We found that terrapins in the Chesapeake Bay region harbour high levels of genetic diversity and form four populations. Effective population sizes were variable. Among most population comparisons, estimates of historical and contemporary terrapin gene flow were generally low (m ≈ 0.01). However, we detected a substantial increase in contemporary gene flow into Chesapeake Bay from populations outside the bay, as well as between two populations within Chesapeake Bay, possibly as a consequence of translocations during the early twentieth century. Our study shows that inferences across multiple time scales are needed to evaluate population connectivity, especially as recent changes may identify threats to population persistence.     

Molecular evidence for the coexistence of two sibling species in Pylaiella littoralis (Ectocarpales,Phaeophyceae) along the Brittany coast

The great phenotypic variability and the lack of diagnostic characters in the genus Pylaiella render the systematic study of this genus problematic. In this study, we investigated the diversity of Pylaiella littoralis along the Brittany (France) coast using a DNA barcoding multilocus approach with mitochondrial (cox1, nad1, and atp9) and chloroplastic (rbcL and atpB) markers associated with a population genetics approach using 10 microsatellite markers. In addition, spatio‐temporal sampling was conducted along the Brittany coast. We sampled 140 individuals from four sites located between Saint‐Malo and Concarneau (380 km) from April to October. Mitochondrial sequence data revealed the occurrence of two sibling species, with a minimum of 2.4% divergence between them. Microsatellite genotypic data congruently revealed two well‐supported clusters matching the two mitochondrial clades of Pylaiella. Although gene flow is limited between species, occurrence of genetic admixtures in some populations suggested that reproductive isolation is not complete. Our study highlighted the complementarity of barcoding and population genetics approaches to shed light on the evolutionary processes that lead to speciation.     

Landscape genetics of California mule deer (Odocoileus hemionus): the roles of ecological and historical factors in generating differentiation

Landscape genetics is an emerging discipline that utilizes environmental and historical data to understand geographic patterns of genetic diversity. Niche modelling has added a new dimension to such efforts by allowing species–environmental associations to be projected into the past so that hypotheses about historical vicariance can be generated and tested independently with genetic data. However, previous approaches have primarily utilized DNA sequence data to test inferences about historical isolation and may have missed very recent episodes of environmentally mediated divergence. We type 15 microsatellite loci in California mule deer and identify five genetic groupings through a Structure analysis that are also well predicted by environmental data. We project the niches of these five deer ecotypes to the last glacial maximum (LGM) and show they overlap to a much greater extent than today, suggesting that vicariance associated with the LGM cannot explain the present-day genetic patterns. Further, we analyse mitochondrial DNA (mtDNA) sequence trees to search for evidence of historical vicariance and find only two well-supported clades. A coalescence-based analysis of mtDNA data shows that the genetic divergence of the mule deer genetic clusters in California is recent and appears to be mediated by ecological factors. The importance of environmental factors in explaining the genetic diversity of California mule deer is unexpected given that they are highly mobile species and have a broad habitat distribution. Geographic differences in the timing of reproduction and peak vegetation as well as habitat choice reflecting natal origin may explain the persistence of genetic subdivision.     

Contrasting effects of landscape features on genetic structure in different geographic regions in the ornate dragon lizard,Ctenophorus ornatus

Habitat fragmentation can have profound effects on the distribution of genetic variation within and between populations. Previously, we showed that in the ornate dragon lizard, Ctenophorus ornatus, lizards residing on outcrops that are separated by cleared agricultural land are significantly more isolated and hold less genetic variation than lizards residing on neighbouring outcrops connected by undisturbed native vegetation. Here, we extend the fine‐scale study to examine the pattern of genetic variation and population structure across the species' range. Using a landscape genetics approach, we test whether land clearing for agricultural purposes has affected the population structure of the ornate dragon lizard. We found significant genetic differentiation between outcrop populations (F_ST = 0.12), as well as isolation by distance within each geographic region. In support of our previous study, land clearing was associated with higher genetic divergences between outcrops and lower genetic variation within outcrops, but only in the region that had been exposed to intense agriculture for the longest period of time. No other landscape features influenced population structure in any geographic region. These results show that the effects of landscape features can vary across species' ranges and suggest there may be a temporal lag in response to contemporary changes in land use. These findings therefore highlight the need for caution when assessing the impact of contemporary land use practices on genetic variation and population structure.