Genetic structure is influenced by landscape features: empirical evidence from a roe deer population

The delimitation of population units is of primary importance in population management and conservation biology. Moreover, when coupled with landscape data, the description of population genetic structure can provide valuable knowledge about the permeability of landscape features, which is often difficult to assess by direct methods (e.g. telemetry). In this study, we investigated the genetic structuring of a roe deer population which recently recolonized a fragmented landscape. We sampled 1148 individuals from a 40 × 55‐km area containing several putative barriers to deer movements, and hence to gene flow, namely a highway, rivers and several canals. In order to assess the effect of these landscape features on genetic structure, we implemented a spatial statistical model known as geneland which analyses genetic structure, explicitly taking into account the spatial nature of the problem. Two genetic units were inferred, exhibiting a very low level of differentiation (FST = 0.008). The location of their boundaries suggested that there are no absolute barriers in this study area, but that the combination of several landscape features with low permeability can lead to population differentiation. Our analysis hence suggests that the landscape has a significant influence on the structuring of the population under study. It also illustrates the use of geneland as a powerful method to infer population structure, even in situations of young populations exhibiting low genetic differentiation.

[1]  Koen J. F. Verhoeven,et al.  Implementing false discovery rate control: increasing your power , 2005 .

[2]  A. Jones gerud 2.0: a computer program for the reconstruction of parental genotypes from half‐sib progeny arrays with known or unknown parents , 2005 .

[3]  L. Fahrig,et al.  Connectivity is a vital element of landscape structure , 1993 .

[4]  Contrasting dispersal patterns in two Scandinavian roe deer Capreolus capreolus populations , 1995, Wildlife Biology.

[5]  A Coulon,et al.  Landscape connectivity influences gene flow in a roe deer population inhabiting a fragmented landscape: an individual–based approach , 2004, Molecular ecology.

[6]  L. K. Wahlstrm The significance of male-male aggression for yearling dispersal in roe deer ( Capreolus capreolus ) , 1994 .

[7]  J. Gaillard,et al.  Behavioural Ecology of Siberian and European Roe Deer , 1995 .

[8]  N. Stenseth,et al.  Genetic structure of Siberian lemmings (Lemmus sibiricus) in a continuous habitat: large patches rather than isolation by distance , 2001, Heredity.

[9]  G. W. Arnold,et al.  Factors affecting the distribution and abundance of Western grey kangaroos (Macropus fuliginosus) and euros (M. robustus) in a fragmented landscape , 1995, Landscape Ecology.

[10]  F. Allendorf,et al.  Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape , 2005, Molecular ecology.

[11]  L. Luiselli,et al.  Influences of area, isolation and habitat features on distribution of snakes in Mediterranean fragmented woodlands , 1997, Biodiversity & Conservation.

[12]  H. Ellegren,et al.  Cryptic population structure in a large, mobile mammalian predator: the Scandinavian lynx , 2003, Molecular ecology.

[13]  J. Goudet FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet (1995) , 2001 .

[14]  J. Millar,et al.  Microgeographic genetic structure in the yellow‐pine chipmunk (Tamias amoenus) , 2001, Molecular ecology.

[15]  M. Moran Arguments for rejecting the sequential Bonferroni in ecological studies , 2003 .

[16]  L. Ratcliffe,et al.  Changes in singing behavior of male black-capped chickadees (Parus atricapillus) following mate removal , 1993, Behavioral Ecology and Sociobiology.

[17]  Arnaud Estoup,et al.  A Spatial Statistical Model for Landscape Genetics , 2005, Genetics.

[18]  John D. Storey A direct approach to false discovery rates , 2002 .

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

[20]  G. Nascetti,et al.  Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius) , 2005, Molecular ecology.

[21]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[22]  J. Joachim,et al.  The effects of woodland fragmentation and human activity on roe deer distribution in agricultural landscapes , 2001 .

[23]  François Rousset,et al.  GENEPOP (version 1.2): population genetic software for exact tests and ecumenicism , 1995 .

[24]  R. Gill,et al.  Behavioral Ecology of Siberian and European Roe Deer , 1996 .

[25]  M. Sillanpää,et al.  Bayesian analysis of genetic differentiation between populations. , 2003, Genetics.

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

[27]  S. Aulagnier,et al.  Cross‐amplification tests of ungulate primers in roe deer (Capreolus capreolus) to develop a multiplex panel of 12 microsatellite loci , 2003 .

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

[29]  Magnus Wang,et al.  The impact of habitat fragmentation and social structure on the population genetics of roe deer (Capreolus capreolus L.) in Central Europe , 2001, Heredity.

[30]  C. Largiadèr,et al.  Recent habitat fragmentation due to roads can lead to significant genetic differentiation in an abundant flightless ground beetle , 2004, Molecular ecology.

[31]  B. Rannala,et al.  The Bayesian revolution in genetics , 2004, Nature Reviews Genetics.

[32]  David L. Hawksworth,et al.  Biodiversity and Conservation , 2007, Biodiversity & Conservation.

[33]  N. Gyllenstrand,et al.  Conservation genetics of the wood ant, Formica lugubris, in a fragmented landscape , 2003, Molecular ecology.

[34]  R. Andersen,et al.  The European roe deer: the biology of success. , 2000 .

[35]  L. Wahlström,et al.  The significance of male-male aggression for yearling dispersal in roe deer (Capreolus capreolus) , 2004, Behavioral Ecology and Sociobiology.

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

[37]  J. Rasplus,et al.  Population genetic structure of rock ptarmigan Lagopus mutus in Northern and Western Europe , 2003, Molecular ecology.

[38]  J. Hampton,et al.  Molecular techniques, wildlife management and the importance of genetic population structure and dispersal: a case study with feral pigs , 2004 .

[39]  G. Gerlach,et al.  Fragmentation of Landscape as a Cause for Genetic Subdivision in Bank Voles , 2000 .

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

[41]  R. Haight,et al.  A Regional Landscape Analysis and Prediction of Favorable Gray Wolf Habitat in the Northern Great Lakes Region , 1995 .

[42]  K. Bailey,et al.  Inverse relationship between FST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure , 2004, Molecular ecology.

[43]  David Reby,et al.  Space use by roe deer in a fragmented landscape some preliminary results , 2002, Revue d'Écologie (La Terre et La Vie).

[44]  C. Peeters,et al.  Population genetic structure and male‐biased dispersal in the queenless ant Diacamma cyaneiventre , 2002, Molecular ecology.

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

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

[47]  Pierre Taberlet,et al.  Landscape genetics: combining landscape ecology and population genetics , 2003 .

[48]  C. Moritz Defining 'Evolutionarily Significant Units' for conservation. , 1994, Trends in ecology & evolution.