A simulation‐based evaluation of methods for inferring linear barriers to gene flow

Different analytical techniques used on the same data set may lead to different conclusions about the existence and strength of genetic structure. Therefore, reliable interpretation of the results from different methods depends on the efficacy and reliability of different statistical methods. In this paper, we evaluated the performance of multiple analytical methods to detect the presence of a linear barrier dividing populations. We were specifically interested in determining if simulation conditions, such as dispersal ability and genetic equilibrium, affect the power of different analytical methods for detecting barriers. We evaluated two boundary detection methods (Monmonier’s algorithm and WOMBLING), two spatial Bayesian clustering methods (TESS and GENELAND), an aspatial clustering approach (STRUCTURE), and two recently developed, non‐Bayesian clustering methods [PSMIX and discriminant analysis of principal components (DAPC)]. We found that clustering methods had higher success rates than boundary detection methods and also detected the barrier more quickly. All methods detected the barrier more quickly when dispersal was long distance in comparison to short‐distance dispersal scenarios. Bayesian clustering methods performed best overall, both in terms of highest success rates and lowest time to barrier detection, with GENELAND showing the highest power. None of the methods suggested a continuous linear barrier when the data were generated under an isolation‐by‐distance (IBD) model. However, the clustering methods had higher potential for leading to incorrect barrier inferences under IBD unless strict criteria for successful barrier detection were implemented. Based on our findings and those of previous simulation studies, we discuss the utility of different methods for detecting linear barriers to gene flow.

[1]  Ellen I. Damschen,et al.  Corridors Increase Plant Species Richness at Large Scales , 2006, Science.

[2]  S. Cushman,et al.  cdpop: A spatially explicit cost distance population genetics program , 2010, Molecular ecology resources.

[3]  Rob Roy Ramey,et al.  Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep , 2005 .

[4]  Jukka Corander,et al.  Bayesian spatial modeling of genetic population structure , 2008, Comput. Stat..

[5]  Marie-Josée Fortin,et al.  Utility of computer simulations in landscape genetics , 2010, Molecular ecology.

[6]  S. Kalinowski,et al.  Founding population size of an aquatic invasive species , 2010, Conservation Genetics.

[7]  A Coulon,et al.  Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub‐jay (Aphelocoma cœrulescens) , 2008, Molecular ecology.

[8]  Rob Harrop,et al.  Installation and Administration , 2004 .

[9]  K. McGarigal,et al.  The gradient concept of landscape structure [Chapter 12] , 2005 .

[10]  M. Fortin,et al.  Comparison of Bayesian Clustering and Edge Detection Methods for Inferring Boundaries in Landscape Genetics , 2011, International journal of molecular sciences.

[11]  AURÉLIE COULON,et al.  Statistical methods in spatial genetics , 2009, Molecular ecology.

[12]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. , 2003, Genetics.

[13]  Samuel A. Cushman,et al.  Representing genetic variation as continuous surfaces: An approach for identifying spatial dependency in landscape genetic studies , 2008 .

[14]  T. Ricketts The Matrix Matters: Effective Isolation in Fragmented Landscapes , 2001, The American Naturalist.

[15]  S. Cushman,et al.  Use of Empirically Derived Source‐Destination Models to Map Regional Conservation Corridors , 2009, Conservation biology : the journal of the Society for Conservation Biology.

[16]  L. Waits,et al.  Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife , 2009, Molecular ecology.

[17]  David O. Wallin,et al.  Spatial scaling and multi-model inference in landscape genetics: Martes americana in northern Idaho , 2010, Landscape Ecology.

[18]  Sophie Ancelet,et al.  Bayesian Clustering Using Hidden Markov Random Fields in Spatial Population Genetics , 2006, Genetics.

[19]  M. Stephens,et al.  Inferring weak population structure with the assistance of sample group information , 2009, Molecular ecology resources.

[20]  F. Balloux,et al.  Discriminant analysis of principal components: a new method for the analysis of genetically structured populations , 2010, BMC Genetics.

[21]  Justin S. Brashares,et al.  Optimizing dispersal and corridor models using landscape genetics , 2007 .

[22]  M. Antrop Changing patterns in the urbanized countryside of Western Europe , 2000, Landscape Ecology.

[23]  R. Leemans Changes in Land use and land cover: A global perspective , 1995 .

[24]  David Herlihy,et al.  The Great Transformation ? , 2007 .

[25]  S. Manel,et al.  WOMBSOFT: an R package that implements the Wombling method to identify genetic boundary , 2007 .

[26]  D. H. Reed Extinction risk in fragmented habitats , 2004 .

[27]  L. Waits,et al.  Putting the ‘landscape’ in landscape genetics , 2007, Heredity.

[28]  Mark Monmonier,et al.  Maximum‐Difference Barriers: An Alternative Numerical Regionalization Method* , 2010 .

[29]  G. Evanno,et al.  Detecting the number of clusters of individuals using the software structure: a simulation study , 2005, Molecular ecology.

[30]  L. Fahrig,et al.  Effects of Road Fencing on Population Persistence , 2004 .

[31]  R. Holderegger,et al.  The genetic effects of roads: A review of empirical evidence , 2010 .

[32]  Gilles Guillot,et al.  On the inference of spatial structure from population genetics data , 2009, Bioinform..

[33]  Terry Burke,et al.  Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? , 2009 .

[34]  N. Balkenhol,et al.  Simulation modelling in landscape genetics: on the need to go further , 2011, Molecular ecology.

[35]  F. Rousset,et al.  ARE PARTIAL MANTEL TESTS ADEQUATE? , 2001, Evolution; international journal of organic evolution.

[36]  Flora Jay,et al.  Spatial inference of admixture proportions and secondary contact zones. , 2009, Molecular biology and evolution.

[37]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[38]  Nianjun Liu,et al.  PSMIX: an R package for population structure inference via maximum likelihood method , 2006, BMC Bioinformatics.

[39]  Olivier François,et al.  Spatially explicit Bayesian clustering models in population genetics , 2010, Molecular ecology resources.

[40]  I. Bičík,et al.  Land-use changes and their social driving forces in Czechia in the 19th and 20th centuries , 2001 .

[41]  K. Polanyi The Great Transformation , 1944 .

[42]  Gilles Guillot,et al.  Response to comment on 'On the inference of spatial structure from population genetics data' , 2009, Bioinform..

[43]  S. Cushman,et al.  Inferring landscape effects on gene flow: a new model selection framework , 2010, Molecular ecology.

[44]  M. Pärtel,et al.  Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels , 2010, Ecology letters.

[45]  Samuel A. Cushman,et al.  Gene Flow in Complex Landscapes: Testing Multiple Hypotheses with Causal Modeling , 2006, The American Naturalist.

[46]  S. Cushman,et al.  Spurious correlations and inference in landscape genetics , 2010, Molecular ecology.

[47]  M. Fortin,et al.  Comparison of the Mantel test and alternative approaches for detecting complex multivariate relationships in the spatial analysis of genetic data , 2010, Molecular ecology resources.

[48]  R. Wayne,et al.  FAST‐TRACK: A southern California freeway is a physical and social barrier to gene flow in carnivores , 2006, Molecular ecology.

[49]  K. McGarigal,et al.  Issues and Perspectives in Landscape Ecology: The gradient concept of landscape structure , 2005 .

[50]  A. Estoup,et al.  Spatial genetic structure of a small rodent in a heterogeneous landscape , 2008, Molecular ecology.

[51]  L. Fahrig Effects of Habitat Fragmentation on Biodiversity , 2003 .

[52]  A. Bennett Linkages in the Landscape: The Role Of Corridors And Connectivity In Wildlife Conservation , 1999 .

[53]  David Lodge,et al.  Habitat loss, trophic collapse, and the decline of ecosystem services. , 2006, Ecology.

[54]  M. Fortin,et al.  Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis , 2010, Molecular ecology.

[55]  Paul B Eier,et al.  South Coast Missing Linkages: restoring connectivity to wildlands in the largest metropolitan area in the USA , 2006 .

[56]  W. H. Womble,et al.  Differential systematics. , 1951, Science.

[57]  L. Waits,et al.  Landscape genetics: where are we now? , 2010, Molecular ecology.

[58]  Raymond J. Dezzani,et al.  Statistical approaches in landscape genetics: an evaluation of methods for linking landscape and genetic data , 2009 .

[59]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[60]  Håkan Sand,et al.  Rescue of a severely bottlenecked wolf (Canis lupus) population by a single immigrant , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[61]  G. Luikart,et al.  Quantifying the lag time to detect barriers in landscape genetics , 2010, Molecular ecology.

[62]  Olivier François,et al.  Bayesian clustering algorithms ascertaining spatial population structure: a new computer program and a comparison study , 2007 .

[63]  C. Norwood Linkages in the Landscape: The Role of Corridors and Connectivity in wildlife Conservation , 1999 .

[64]  Arnaud Estoup,et al.  Geneland: a computer package for landscape genetics , 2005 .

[65]  Anthony W. King,et al.  The Implications of Metalandscape Connectivity for Population Viabilityin Migratory Songbirds , 2006, Landscape Ecology.

[66]  M. Stephens,et al.  Inference of population structure using multilocus genotype data: dominant markers and null alleles , 2007, Molecular ecology notes.

[67]  J. Tewksbury,et al.  Connectivity Conservation: Impacts of corridors on populations and communities , 2006 .

[68]  Kevin S. McKelvey,et al.  Why sampling scheme matters: the effect of sampling scheme on landscape genetic results , 2009, Conservation Genetics.

[69]  Eric Durand,et al.  Comment on 'On the inference of spatial structure from population genetics data' , 2009, Bioinform..