DISENTANGLING THE EFFECTS OF GEOGRAPHIC AND ECOLOGICAL ISOLATION ON GENETIC DIFFERENTIATION

Populations can be genetically isolated both by geographic distance and by differences in their ecology or environment that decrease the rate of successful migration. Empirical studies often seek to investigate the relationship between genetic differentiation and some ecological variable(s) while accounting for geographic distance, but common approaches to this problem (such as the partial Mantel test) have a number of drawbacks. In this article, we present a Bayesian method that enables users to quantify the relative contributions of geographic distance and ecological distance to genetic differentiation between sampled populations or individuals. We model the allele frequencies in a set of populations at a set of unlinked loci as spatially correlated Gaussian processes, in which the covariance structure is a decreasing function of both geographic and ecological distance. Parameters of the model are estimated using a Markov chain Monte Carlo algorithm. We call this method Bayesian Estimation of Differentiation in Alleles by Spatial Structure and Local Ecology (BEDASSLE), and have implemented it in a user‐friendly format in the statistical platform R. We demonstrate its utility with a simulation study and empirical applications to human and teosinte data sets.

[1]  B. Weir,et al.  Estimation of inbreeding parameters in stratified populations , 1986, Annals of human genetics.

[2]  B S Weir,et al.  Estimating F-statistics. , 2002, Annual review of genetics.

[3]  W. K. Hastings,et al.  Monte Carlo Sampling Methods Using Markov Chains and Their Applications , 1970 .

[4]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[5]  J. Doebley,et al.  Genetic Diversity and Population Structure of Teosinte , 2005, Genetics.

[6]  P. Morrell,et al.  Megabase-Scale Inversion Polymorphism in the Wild Ancestor of Maize , 2012, Genetics.

[7]  N. Metropolis,et al.  Equation of State Calculations by Fast Computing Machines , 1953, Resonance.

[8]  J. Doebley,et al.  Genetic signals of origin, spread, and introgression in a large sample of maize landraces , 2010, Proceedings of the National Academy of Sciences.

[9]  L. Wasserman,et al.  Computing Bayes Factors Using a Generalization of the Savage-Dickey Density Ratio , 1995 .

[10]  Sarah C. Goslee,et al.  The ecodist Package for Dissimilarity-based Analysis of Ecological Data , 2007 .

[11]  J. Hey,et al.  A multi-dimensional coalescent process applied to multi-allelic selection models and migration models. , 1991, Theoretical population biology.

[12]  Matthew Stephens,et al.  Assigning African elephant DNA to geographic region of origin: applications to the ivory trade. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Stephen M. Krone,et al.  Separation of time scales and convergence to the coalescent in structured populations ∗ , 2001 .

[14]  M. Feldman,et al.  Genetic Structure of Human Populations , 2002, Science.

[15]  R. Waagepetersen,et al.  Bayesian Prediction of Spatial Count Data Using Generalized Linear Mixed Models , 2002, Biometrics.

[16]  P. Meirmans,et al.  The trouble with isolation by distance , 2012, Molecular ecology.

[17]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[18]  F. Rousset Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. , 1997, Genetics.

[19]  G Malécot,et al.  Heterozygosity and relationship in regularly subdivided populations. , 1975, Theoretical population biology.

[20]  Nicholas H. Barton,et al.  The Effects of Genetic and Geographic Structure on Neutral Variation , 2003 .

[21]  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.

[22]  J. Losos,et al.  Quantifying the roles of ecology and geography in spatial genetic divergence. , 2013, Ecology letters.

[23]  G. Coop,et al.  Robust Identification of Local Adaptation from Allele Frequencies , 2012, Genetics.

[24]  D. Conrad,et al.  A worldwide survey of haplotype variation and linkage disequilibrium in the human genome , 2006, Nature Genetics.

[25]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[26]  M. Feldman,et al.  Clines, Clusters, and the Effect of Study Design on the Inference of Human Population Structure , 2005, PLoS genetics.

[27]  D. Neale,et al.  The geographical and environmental determinants of genetic diversity for four alpine conifers of the European Alps , 2012, Molecular ecology.

[28]  J. Mallet,et al.  Host races in plant-feeding insects and their importance in sympatric speciation. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[29]  Gilles Guillot,et al.  Dismantling the Mantel tests , 2011, 1112.0651.

[30]  P. Diggle,et al.  Model‐based geostatistics , 2007 .

[31]  J. Møller,et al.  Log Gaussian Cox Processes , 1998 .

[32]  D. A. Williams,et al.  The analysis of binary responses from toxicological experiments involving reproduction and teratogenicity. , 1975, Biometrics.

[33]  Williams Da,et al.  The analysis of binary responses from toxicological experiments involving reproduction and teratogenicity. , 1975 .

[34]  R. Sokal,et al.  Multiple regression and correlation extensions of the mantel test of matrix correspondence , 1986 .

[35]  M. Feldman,et al.  Worldwide Human Relationships Inferred from Genome-Wide Patterns of Variation , 2008 .

[36]  David B. Witonsky,et al.  Using Environmental Correlations to Identify Loci Underlying Local Adaptation , 2010, Genetics.

[37]  H. Eagles,et al.  Highland Maize from Central Mexico—Its Origin, Characteristics, and Use in Breeding Programs , 1994 .

[38]  O. Hardy,et al.  New insights from fine‐scale spatial genetic structure analyses in plant populations , 2004, Molecular ecology.

[39]  J. Dickey The Weighted Likelihood Ratio, Linear Hypotheses on Normal Location Parameters , 1971 .

[40]  M. Slatkin,et al.  The Influence of Gene Flow on Genetic Distance , 1975, The American Naturalist.

[41]  D. Balding Likelihood-based inference for genetic correlation coefficients. , 2003, Theoretical population biology.

[42]  L. Rieseberg,et al.  Adaptation with gene flow across the landscape in a dune sunflower , 2012, Molecular ecology.

[43]  K. McCoy,et al.  Cryptic vector divergence masks vector-specific patterns of infection: an example from the marine cycle of Lyme borreliosis , 2010, Evolutionary applications.

[44]  Paul Beier,et al.  Circuit theory predicts gene flow in plant and animal populations , 2007, Proceedings of the National Academy of Sciences.

[45]  D. Bolnick,et al.  Non-random gene flow: an underappreciated force in evolution and ecology. , 2012, Trends in ecology & evolution.

[46]  D. Balding,et al.  A method for quantifying differentiation between populations at multi-allelic loci and its implications for investigating identity and paternity , 2005, Genetica.

[47]  N. Rosenberg A Population-Genetic Perspective on the Similarities and Differences among Worldwide Human Populations , 2011, Human biology.

[48]  Montgomery Slatkin,et al.  ISOLATION BY DISTANCE IN EQUILIBRIUM AND NON‐EQUILIBRIUM POPULATIONS , 1993, Evolution; international journal of organic evolution.

[49]  A. Hendry Selection against migrants contributes to the rapid evolution of ecologically dependent reproductive isolation , 2004 .

[50]  L. Harmon,et al.  “SAME SAME BUT DIFFERENT”: REPLICATED ECOLOGICAL SPECIATION AT WHITE SANDS , 2011, Evolution; international journal of organic evolution.

[51]  Xiao-Li Meng,et al.  POSTERIOR PREDICTIVE ASSESSMENT OF MODEL FITNESS VIA REALIZED DISCREPANCIES , 1996 .

[52]  Richard R. Hudson,et al.  Generating samples under a Wright-Fisher neutral model of genetic variation , 2002, Bioinform..

[53]  D. Balding,et al.  Significant genetic correlations among Caucasians at forensic DNA loci , 1997, Heredity.