Landscape structure affects dispersal in the greater white-toothed shrew : Inference between genetic and simulated ecological distances

Dispersal is often viewed as a process on which the landscape has little effect. This is particularly apparent in populations’ genetic and ecological studies, where isolation by distance is generally tested using a Euclidean distance between populations. However, landscapes can be richly textured mosaics of patches, associated with different qualities (e.g. different costs crossing patches) and different structures (shape, size and arrangement). An important challenge, therefore, is to determine if accounting for this additional complexity enriches our understanding of the dispersal processes. In this study, we quantify the effect of landscape structure on dispersal distances between 15 populations of the greater white-toothed shrew (Crocidura russula) in a highly fragmented landscape in Switzerland. We use a spatially explicit individual-based model to simulate C. russula dispersal. This model is designed to account for movement behavior in heterogeneous landscapes. We explore the relationship between simulation results and genetic differentiation between actual subpopulations. Finally, we test if simulated dispersal distances are better predictors of genetic differentiation than traditional Euclidean distances. The ecological distances measured by the model show a clear relationship with genetic differentiation between C. russula subpopulations. This relationship is stronger than the one obtained by the usual Euclidean distance.

[1]  Hugh P Possingham,et al.  Does colonization asymmetry matter in metapopulations? , 2006, Proceedings of the Royal Society B: Biological Sciences.

[2]  R. Griffiths,et al.  Inference from gene trees in a subdivided population. , 2000, Theoretical population biology.

[3]  Paul G. Blackwell,et al.  Random diffusion models for animal movement , 1997 .

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

[5]  F. Rousset,et al.  AN EXACT TEST FOR POPULATION DIFFERENTIATION , 1995, Evolution; international journal of organic evolution.

[6]  Séverine Vuilleumier,et al.  Animal dispersal modelling: handling landscape features and related animal choices , 2006 .

[7]  G. Barrett,et al.  Influence of Landscape Structure on Movement Patterns of Small Mammals , 1999 .

[8]  K H Pollock,et al.  Tests for mortality and recruitment in a K-sample tag-recapture experiment. , 1974, Biometrics.

[9]  Cinda Davis,et al.  MOVEMENT RESPONSES TO PATCH STRUCTURE IN EXPERIMENTAL FRACTAL LANDSCAPES , 1999 .

[10]  Roger Pradel,et al.  Methods for estimating dispersal probabilities and related parameters using marked animals , 2001 .

[11]  L. Fahrig,et al.  Mosaic Landscapes and Ecological Processes , 1995, Springer Netherlands.

[12]  Jon A Yamato,et al.  Estimating effective population size and mutation rate from sequence data using Metropolis-Hastings sampling. , 1995, Genetics.

[13]  Denis Couvet,et al.  Deleterious Effects of Restricted Gene Flow in Fragmented Populations , 2002 .

[14]  J. Gamarra,et al.  Metapopulation Ecology , 2007 .

[15]  J. Wolff,et al.  Population regulation in mammals : an evolutionary perspective , 1997 .

[16]  François-Joseph Lapointe,et al.  ASSESSING CONGRUENCEAMONG DISTANCE MATRICES: SINGLE‐MALT SCOTCH WHISKIES REVISITED , 2004 .

[17]  P. C. Dias,et al.  Sources and sinks in population biology. , 1996, Trends in ecology & evolution.

[18]  D. Skibinski,et al.  A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes , 1994 .

[19]  David B. Lindenmayer,et al.  Modelling dispersal behaviour on a fractal landscape , 1998, Environ. Model. Softw..

[20]  Charles C. Miller,et al.  Microsatellite DNA and recent statistical methods in wildlife conservation management: applications in Alpine ibex [Capra ibex (ibex)] , 2002, Molecular ecology.

[21]  Ian P. Woiwod,et al.  Insect Movement: Mechanisms and Consequences , 2001 .

[22]  A. Cockburn.  Habitat heterogeneity and dispersal: environmental and genetic patchiness , 1992 .

[23]  Kenneth H. Pollock,et al.  CAPTURE-RECAPTURE STUDIES FOR MULTIPLE STRATA INCLUDING NON-MARKOVIAN TRANSITIONS , 1993 .

[24]  C. Cockerham,et al.  ESTIMATION OF GENE FLOW FROM F‐STATISTICS , 1993, Evolution; international journal of organic evolution.

[25]  L. Waits,et al.  An empirical evaluation of genetic distance statistics using microsatellite data from bear (Ursidae) populations. , 1997, Genetics.

[26]  J. Cornuet,et al.  GENECLASS2: a software for genetic assignment and first-generation migrant detection. , 2004, The Journal of heredity.

[27]  Mark Reed,et al.  Object-oriented migration modelling for biological impact assessment , 1996 .

[28]  K D Farnsworth,et al.  How Do Grazers Achieve Their Distribution? A Continuum of Models from Random Diffusion to the Ideal Free Distribution Using Biased Random Walks , 1999, The American Naturalist.

[29]  D. H. Vuren,et al.  Detectability, philopatry, and the distribution of dispersal distances in vertebrates. , 1996, Trends in ecology & evolution.

[30]  S. Wright.  THE INTERPRETATION OF POPULATION STRUCTURE BY F‐STATISTICS WITH SPECIAL REGARD TO SYSTEMS OF MATING , 1965 .

[31]  G. Barrett,et al.  Landscape Ecology of Small Mammals , 1999, Springer New York.

[32]  Lutz Tischendorf,et al.  Modelling individual movements in heterogeneous landscapes: potentials of a new approach , 1997 .

[33]  Monica G. Turner,et al.  Landscape connectivity and population distributions in heterogeneous environments , 1997 .

[34]  R. Lande,et al.  Finite metapopulation models with density–dependent migration and stochastic local dynamics , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[35]  A. Hastings,et al.  Metapopulation Dynamics and Genetics , 1994 .

[36]  M. Eldridge,et al.  Source population of dispersing rock‐wallabies (Petrogale lateralis) idengified by assignment tests on multilocus genotypic data , 2001, Molecular ecology.

[37]  Keith D. Farnsworth,et al.  Animal foraging from an individual perspective: an object orientated model , 1998 .

[38]  Jacoby Carter,et al.  MOAB : a spatially explicit, individual-based expert system for creating animal foraging models , 1999 .

[39]  Yoshio Tateno,et al.  Accuracy of estimated phylogenetic trees from molecular data , 2005, Journal of Molecular Evolution.

[40]  J. Felsenstein,et al.  Maximum-likelihood estimation of migration rates and effective population numbers in two populations using a coalescent approach. , 1999, Genetics.

[41]  J. Gentle,et al.  Randomization and Monte Carlo Methods in Biology. , 1990 .

[42]  F. Balloux,et al.  Female-biased dispersal in the monogamous mammal Crocidura russula: evidence from field data and microsatellite patterns. , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[43]  J. Hestbeck.  Population Regulation of Cyclic Mammals: The Social Fence Hypothesis , 1982 .

[44]  R. Holt,et al.  Evolutionary Consequences of Asymmetric Dispersal Rates , 2002, The American Naturalist.

[45]  Eric J. Gustafson,et al.  Simulating dispersal of reintroduced species within heterogeneous landscapes , 2004 .

[46]  Nicolas Perrin,et al.  Effects of cognitive abilities on metapopulation connectivity , 2006 .

[47]  O. Berry,et al.  Can assignment tests measure dispersal? , 2004, Molecular ecology.

[48]  Peter Beerli,et al.  Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Florian Jeltsch,et al.  From pattern to practice: a scaling-down strategy for spatially explicit modelling illustrated by the spread and control of rabies , 1999 .

[50]  P. Fontanillas,et al.  Mitochondrial DNA variation along an altitudinal gradient in the greater white‐toothed shrew, Crocidura russula , 2002, Molecular ecology.

[51]  Stefan Halle,et al.  Modelling activity synchronisation in free-ranging microtine rodents , 1999 .

[52]  F. Bonhomme,et al.  GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. , 1996 .

[53]  G Luikart,et al.  New methods employing multilocus genotypes to select or exclude populations as origins of individuals. , 1999, Genetics.

[54]  A. Pusey,et al.  Inbreeding avoidance in animals. , 1996, Trends in ecology & evolution.

[55]  L. C. Rutledge,et al.  Genetic Data Analysis , 1991 .

[56]  J. Goudet.  FSTAT (Version 1.2): A Computer Program to Calculate F-Statistics , 1995 .

[57]  J. O. Wolff.  More on Juvenile Dispersal in Mammals , 1994 .

[58]  Nils Chr. Stenseth,et al.  To disperse or not to disperse: who does it and why? , 1992 .

[59]  M Slatkin,et al.  A measure of population subdivision based on microsatellite allele frequencies. , 1995, Genetics.

[60]  Roger Pradel,et al.  Utilization of capture-mark-recapture for the study of recruitment and population growth rate. , 1996 .

[61]  Thorsten Wiegand,et al.  Finding the Missing Link between Landscape Structure and Population Dynamics: A Spatially Explicit Perspective , 1999, The American Naturalist.

[62]  Stephen R. Baillie,et al.  Modeling large-scale dispersal distances , 2002 .

[63]  N Takezaki,et al.  Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. , 1996, Genetics.

[64]  Uta Berger,et al.  Virtual biologists observe virtual grasshoppers: an assessment of different mobility parameters for the analysis of movement patterns , 1999 .

[65]  F. Balloux,et al.  Statistical properties of population differentiation estimators under stepwise mutation in a finite island model , 2002, Molecular ecology.

[66]  A. Carlson,et al.  The effect of landscape composition on colonization success, growth rate and dispersal in introduced bush‐crickets Metrioptera roeseli , 2001 .

[67]  L. Hansson,et al.  Dispersal and connectivity in metapopulations , 1991 .

[68]  N. Barton.  The genetic consequences of dispersal , 1992 .

[69]  Volker Grimm,et al.  Individual-based modelling and ecological theory: synthesis of a workshop , 1999 .

[70]  S. L. Lima,et al.  Towards a behavioral ecology of ecological landscapes. , 1996, Trends in ecology & evolution.

[71]  J. Wolff,et al.  Behavioral Model Systems , 1999 .

[72]  M. Taper,et al.  Interspecific Competition, Environmental Gradients, Gene Flow, and the Coevolution of Species' Borders , 2000, The American Naturalist.

[73]  Eric J. Gustafson,et al.  The Effect of Landscape Heterogeneity on the Probability of Patch Colonization , 1996 .

[74]  John A. Wiens,et al.  Landscape mosaics and ecological theory , 1995 .

[75]  L. Fahrig,et al.  Habitat Patch Connectivity and Population Survival , 1985 .

[76]  Nils Chr. Stenseth,et al.  The study of dispersal: a conceptual guide , 1992 .

[77]  Andrew T. Smith,et al.  Conspecific Attraction and the Determination of Metapopulation Colonization Rates , 1990 .

[78]  Michael Sonnenschein,et al.  Modelling and simulation software to support individual-based ecological modelling , 1999 .

[79]  L. Fahrig,et al.  How should we measure landscape connectivity? , 2000, Landscape Ecology.

[80]  M. Turner,et al.  LANDSCAPE ECOLOGY : The Effect of Pattern on Process 1 , 2002 .

[81]  A. I.,et al.  Neural Field Continuum Limits and the Structure–Function Partitioning of Cognitive–Emotional Brain Networks , 2023, Biology.

[82]  Nils Chr. Stenseth,et al.  Animal dispersal : small mammals as a model , 1992 .

[83]  Paul R. Moorcroft,et al.  Home range analysis using a mechanistic home range model , 1999 .

[84]  P. Fontanillas,et al.  ESTIMATING SEX‐SPECIFIC DISPERSAL RATES WITH AUTOSOMAL MARKERS IN HIERARCHICALLY STRUCTURED POPULATIONS , 2004, Evolution; international journal of organic evolution.

[85]  Otso Ovaskainen,et al.  The metapopulation capacity of a fragmented landscape , 2000, Nature.

[86]  K J Dawson,et al.  A Bayesian approach to the identification of panmictic populations and the assignment of individuals. , 2001, Genetical research.

[87]  J. Endler.  Geographic variation, speciation, and clines. , 1977, Monographs in population biology.

[88]  D. Morris.  On the Evolutionary Stability of Dispersal to Sink Habitats , 1991, The American Naturalist.

[89]  F. Record.  On Gene Flow , 2020, Geographic Variation, Speciation and Clines. (MPB-10), Volume 10.

[90]  F. Balloux,et al.  The estimation of population differentiation with microsatellite markers , 2002, Molecular ecology.

[91]  M. Whitlock,et al.  Indirect measures of gene flow and migration: FST≠1/(4Nm+1) , 1999, Heredity.