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Contributions of Landscape Genetics – Approaches, Insights, and Future

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Contributions of Landscape Genetics – Approaches, Insights, and Future Molecular Ecology (2010) 19, 3489–3495 INTRODUCTION Contributions of landscape genetics – populations within an increasingly human-impacted approaches, insights, and future world (Agee & Johnson 1987; Leita˜o et al. 2006; Trombu- lak & Baldwin 2010). This paradigm shift is linked to the potential important development of metapopulation theory (Hanski & Gilpin 1991; Harrison & Hastings 1996; Hanski & VICTORIA L. SORK* and LISETTE WAITS† Simberloff 1997) and the emergence of the discipline *Department of Ecology and Evolutionary Biology and Institute of landscape ecology (Urban et al. 1987; Turner 1989; of the Environment, University of California Los Angeles, Los Hansson et al. 1995; Pickett & Cadenasso 1995). Second, Angeles, CA 90095-1606, USA, †Department of Fish and technological improvements in molecular methods and Wildlife Resources, University of Idaho, Moscow, ID 83844- corresponding decreases in cost per sample have made it 1136, USA physically and financially feasible to collect large amounts of genetic data from hundreds of individuals at a land- scape scale (Storz 2005). Third, improvements in geo- Keywords: adaptation, conservation biology, gene flow, graphic information systems and remote sensing tools landscape ecology, landscape genetics, population genetics have greatly increased our ability to quantify landscape Received 17 June 2010; revision received 11 July 2010; accepted and environmental variables at biologically meaningful 14 July 2010 scales (McGarigal & Marks 1995; Wulder et al. 2004; Thomassen et al. 2010). The field of landscape genetics draws from all three of these conceptual and technical advances to explicitly evaluate hypotheses that examine Introduction how landscape and environmental features shape gene Landscape genetics is an emerging field that seeks to flow among populations, the spatial patterning of genetic understand how specific landscape features and microevo- variation, and local adaptation. lutionary processes such as gene flow, genetic drift, and The overwhelming majority of landscape genetic studies selection interact to shape the amount and spatial distri- have addressed the question of how landscape features bution of genetic variation (Manel et al. 2010). Its concep- affect connectivity or create barriers to gene movement. Ani- tual basis is founded in landscape ecology, population mal studies, in particular, are likely to focus on how natural genetics, and spatial statistics, which are integrated to and anthropogenic landscape features affect animal-medi- address landscape-scale research questions and hypothe- ated gene movement. In fact, 62% of landscape genetic stud- ses (Manel et al. 2003; Storfer et al. 2007; Storfer et al. ies examine vertebrates (Storfer et al. 2010). These studies 2010). When the term ‘landscape genetics’ was first pro- have effectively documented patterns of connectivity on posed (Manel et al. 2003), it was not clear how it differed landscapes and identified barriers to movement. Plant stud- from established disciplines such as population and geo- ies have been less likely to utilize a landscape genetic graphical genetics. However, the focus of landscape genet- approach, comprising only 14.5% of the current studies ics was refined to include spatially explicit research that (Storfer et al. 2010). However, this discrepancy is not specifically ‘quantifies the effects of landscape composi- because plant researchers are not concerned with the genetic tion, configuration and matrix quality on gene flow and consequences of landscapes. Indeed, numerous plant studies spatial genetic variation’ (Storfer et al. 2007). Early have documented the impact of landscape factors such as research models in this discipline focused on the terres- fragmentation and isolation on genetic processes such as trial landscape, but the field has expanded to include inbreeding and inbreeding depression, loss of genetic diver- ‘riverscape’ and ‘seascape’ systems (Fausch et al. 2002; sity, and gene flow (Holsinger 1993; Young et al. 1996; Sork Galindo et al. 2006, 2010; Selkoe et al. 2008, 2010). Across et al. 1999; Sork & Smouse 2006; Aguilar et al. 2008). As all ecosystems, a common emphasis is unravelling the plant biologists increase their attention on connectivity, we influence of landscape and environmental features on the should also see an increase in spatially explicit analyses that distribution of genetic variation. utilize the spatially explicit tools of landscape genetics (for Three main forces have driven the current rapid growth an example see Dyer et al. 2010). of landscape genetics. First, managers and conservation Understanding the spatial pattern of genetic variation is biologists have shifted to landscape and ecosystem level an important contribution of landscape genetics. Landscape planning to address the challenge of maintaining viable effects on the distribution of neutral genetic variation can help identify corridors and barriers to gene flow, but the association between environmental and genetic gradients Correspondence: Victoria Sork, Fax: 310 206 0484; can provide initial evidence of the impact of natural selec- E-mail: [email protected] Ó 2010 Blackwell Publishing Ltd 3490 INTRODUCTION tion (Endler 1986; Holderegger et al. 2006; Manel et al. illustrate the connection with phylogeography including 2010a). Environmental correlations with neutral genetic studies that uncover historical and current landscape pro- markers can help identify opportunities for natural selection cesses in landscape genetics (Dyer et al. 2010; Knowles & (e.g. Sork et al. 2010), but the mapping of adaptive genetic Alvarado-Serrano 2010). Fifth, we explore adaptive land- variation that underlies the phenotypes under selection pro- scape genetics by including studies examining the impact vides even stronger evidence (Storz 2005; Balding 2006; Han- of landscape environmental factors on adaptive genetic cock & Di Rienzo 2008; Stinchcombe & Hoekstra 2008). variation (Eckert et al. 2010; Freedman et al. 2010; Manel Recently, researchers have begun to contrast neutral and et al. 2010a,b; Sork et al. 2010). adaptive variation using AFLP’s (Bonin et al. 2006; Joost et al. 2007; Freedman et al. 2010) in order to identify adap- tive genetic variation. However, as next-generation genomic Methodological reviews and commentaries tools become more accessible (Beaumont & Balding 2004; The interdisciplinary nature of landscape genetics creates a Storz 2005), we will see the surfacing of landscape genomic number of unique methodological challenges centred on studies that examine genetic variation associated with func- integrating and analysing spatially explicit environmental tional genes (Hancock et al. 2008; Eckert et al. 2010). It variables and genetic data at a landscape scale. A recent appears that the study of spatial patterns of adaptive varia- review of research needs in landscape genetics highlighted tion will become a strong tool for incorporating the process analytical limitations as one of four major challenges in the of selection into landscape genetics. field (Balkenhol et al. 2009). Empirical analysis articles in Through the development of new approaches and new this special issue address these challenges using a diversity questions arising out of research that explicitly links of novel and creative approaches, and this section of meth- genetic data with landscape and environmental variables, odological reviews and commentaries highlights some of the field of landscape genetics can provide valuable the key methodological approaches, considerations, and insights into how the evolutionary processes of gene flow, challenges in landscape genetics. Thomassen et al. (2010) genetic drift, and natural selection have been influenced by review current methods and data sources for making landscape-scale processes to shape current patterns of continuous spatial predictions from biological variation genetic variation. Understanding these processes will allow using spatial and environmental predictor variables. This us to predict the response of current populations to anthro- review article overviews a diversity of regression methods, pogenic forces, such as climate change, human population decision tree approaches, and generalized dissimilarity growth, habitat destruction, and fragmentation. modelling techniques summarizing the advantages and limitations of each method and ending with a section on key challenges and opportunities for future research. Ep- Contributions and overview of the special issue on person et al. (2010) examine the current and future role of landscape genetics computer simulation approaches in the development of landscape genetic theory and methods. This article reviews This special issue was designed to highlight the diversity the development of stochastic space–time simulation of questions that can be investigated through an interdis- approaches and the roles of simulations in testing model ciplinary landscape genetics framework and furthermore assumptions, characterizing the properties of statistical esti- introduce new analytical approaches and update the cur- mators, and testing alternative hypotheses in empirical rent status of the field and its future potential. The issue data sets. One major methodological challenge in landscape includes 22 contributions that span a diversity of terres- genetics is interpreting spatial genetic patterns that are the trial, marine, and freshwater landscapes and range from outcome of multiple biotic and abiotic processes operating topical reviews to new methods
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