Abstract
Context
In a global context of erosion of biodiversity, the current environmental policy in Europe is oriented towards the creation and the preservation of ecological networks for wildlife. However, most of the management guidelines arose from a structural landscape diagnostic without truly taking into consideration species’ needs.
Objectives
We tested whether and how landscape elements influence the functional connectivity of landscapes for a forest specialist species, the European pine marten (Martes martes), in Northeastern France.
Methods
We collected pine marten scats and tissues from 13 evenly distributed study sites across the whole study area in order to test several types of barriers such as highways, waterways, and open agricultural fields. We crossed the results of several methods: spatial autocorrelation analysis, causal modelling framework, and clustering methods.
Results
The study indicates significant genetic differentiation among the sampling sites. A signal of isolation by distance was detected but disappeared after partialling out landscape or barrier resistance. The only model that was fully supported by causal modelling was the one identifying waterways as the main driver of genetic differentiation. Moreover, clustering analyses indicated the presence of genetic clusters, suggesting that pine marten spatial genetic pattern could be explained by the presence of waterways but also by their reluctance to cross open fields.
Conclusions
The current ecological network could thus be improved by increasing permeability of waterways, in particular navigation canals, and by maintaining and restoring forested corridors in agricultural plains.
Similar content being viewed by others
References
Baguette M, Blanchet S, Legrand D, Stevens VM, Turlure C (2013) Individual dispersal, landscape connectivity and ecological networks. Biol Rev 88:310–326
Balestrieri A, Remonti L, Ruiz-Gonzalez A, Gomez-Moliner BJ, Vergara M, Priogioni C (2010) Range expansion of the pine marten (Martes martes) in an agricultural landscape matrix (NW Italy). Mamm Biol 75:412–419
Balkenhol N, Gugerli F, Cushman SA, Waits LP, Coulon A, Arntzen JW, Holderegger R, Wagner HH, Participants of the Landscape Genetics Research Agenda Workshop 2007 (2009) Identifying future research needs in landscape genetics: where to from here? Land Ecol 24:455–463
Basto MP, Rodrigues M, Santos-Reis M, Bruford MW, Fernandes CA (2010) Isolation and characterization of 13 tetranucleotide microsatellite loci in the Stone marten (Martes foina). Conserv Genet Resour 2:317–319
Beier P (2005) Dispersal of juvenile cougars in fragmented habitat. J Wildlife Manag 59:228–237
Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (1996–2004) GENETIX 4.05, logiciel Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, Université de Montpellier II, Montpellier
Bennett AF (1999) Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. International Union for Conservation of Nature and Natural Resources, Gland
Brainerd SM (1990) The pine marten and forest fragmentation: a review and synthesis. In: Myrberget S (ed), Transaction of the 19th IUGB Congress, Trondheim, pp 421–434
Broquet T, Ray N, Petit E, Fryxell JM, Burel F (2006) Genetic isolation by distance and landscape connectivity in the American marten (Martes americana). Landscape Ecol 21(6):877–889
Chen XY (2000) Effects of habitat fragmentation on genetic structure of plant populations and implications for the biodiversity conservation. Acta Ecol Sin 20:884–892
Coulon A, Fitzpatrick JW, Bowman R, Stith BM, Makarewich CA, Stenzler LM, Lovette IJ (2008) Congruent population structure inferred from dispersal behaviour and intensive genetic surveys of the threatened Florida scrub-jay (Aphelocoma coerulescens). Mol Ecol 17:1685–1701
Coulon A, Guillot G, Cosson J-F, Angibault JM, Aulagnier S, Cargnelutti B, Galan M, Hewison AJ (2006) Genetic structure is influenced by landscape features: empirical evidence from a roe deer population. Mol Ecol 15:1669–1679
Cushman SA, Landguth EL (2010) Spurious correlations and inference in landscape genetics. Mol Ecol 19:3592–3602
Cushman SA, McKelvey KS, Hayden J, Schwartz MK (2006) Gene flow in complex landscapes: testing multiple hypotheses with causal modeling. Am Nat 168:486–499
Cushman SA, Shirk AJ, Landguth EL (2013a) Landscape genetics and limiting factors. Conserv Genet 14:263–274
Cushman SA, Wasserman TN, Landguth EL, Shirk AJ (2013b) Re-evaluating causal modeling with Mantel tests in landscape genetics. Diversity 5:51–72
Davis CS, Strobeck C (1998) Isolation, variability, and cross-species amplification of polymorphic microsatellite loci in the family Mustelidae. Mol Ecol 7:1776–1778
Díaz-Muñoz SL (2012) Role of recent and old riverine barriers in fine-scale population genetic structure of Geoffroy’s tamarin (Saguinus geoffroyi) in the Panama Canal watershed. Ecol Evol 2:298–309
Earl DA, von Holdt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361
Epps CW, Palsboll PJ, Wehausen JD, Roderick GK, Ramey RR, McCullough DR (2005) Highways block gene flow and cause a rapid decline in genetic diversity of desert bighorn sheep. Ecol Lett 8:1029–1038
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Syst 34:487–515
Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587
Frantz AC, Bertouille S, Eloy MC, Licoppe A, Chaumont F, Flamand MC (2012) Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus), but not wild boars (Sus scrofa). Mol Ecol 14:3445–3457
Galpern P, Manseau M, Hettinga P, Wilson P, Smith K (2012) ALLELEMATCH: an R package for identifying unique multilocus genotypes where genotyping error and missing data may be present. Mol Ecol Res. doi:10.1111/j.1755-0998.2012.03137.x
Gillies CS, St. Clair CC (2008) Riparian corridors enhance movement of a forest specialist bird in fragmented tropical forest. Proc Natl Acad Sci 105(50):19774–19779
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Heredity 86(6):485–486
Haag T, Santos AS, Sana DA, Morato RG, Cullen L Jr, Crawshaw PG Jr, De Angelo C, Di Bitetti MS, Salzano FM, Eizirik E (2010) The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca). Mol Ecol 19:4906–4921
Holderegger R, Wagner HH (2008) Landscape genetics. Bioscience 58:199–207
Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinform 23:1801–1806
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinform 24:1403–1405
Kimura M, Weiss GH (1964) The stepping stone model of population structure and the decrease of genetic correlation with distance. Genetics 49:561–576
Kindlmann P, Burel F (2008) Connectivity measures: a review. Landscape Ecol 23:879–890
Larroque J, Ruette S, Vandel J-M, Devillard S (2016) Divergent landscape effects on genetic differentiation in two populations of the European pine marten (Martes martes). Landscape Ecol 31(3):517–531
Legendre P (1993) Spatial auto-correlation: trouble or newparadigm. Ecology 74:1659–1673
Legendre P, Trousselier M (1988) Aquatic heterotrophic bacteria: modeling in the presence of spatial autocorrelation. Limnol Oceanogr 33:1055–1067
Lindenmayer D, Hobbs RJ, Montague-Drake R, Alexandra J, Bennett A, Burgman M, Cale P, Calhoun A, Cramer V, Cullen P, Driscoll D, Fahrig L, Fischer J, Franklin J, Haila Y, Hunter M, Gibbons P, Lake S, Luck G, MacGregor G, McIntyre S, Mac Nally R, Manning A, Miller J, Mooney H, Noss R, Possingham H, Saunders D, Schmiegelow F, Scott M, Simberloff D, Sisk T, Tabor G, Walker B, Wiens J, Woinarski J, Zavaleta E (2008) A checklist for ecological management of landscapes for conservation. Ecol Lett 11:78–91
Luoy D, Habel JC, Schmitt T, Assmann T, Meyer M, Müller P (2007) Strongly diverging population genetic patterns of three skipper species: role of habitat fragmentation and dispersal ability. Conserv Genet 8:671–681
Manel S, Schwartz MK, Luikart G, Taberlet P (2003) Landscape genetics: combining landscape ecology and population genetics. Trends Ecol Evol 18:189–197
McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724
Mergey M, Helder R, Roeder JJ (2011) Effect of forest fragmentation on space use patterns in the European pine marten (Martes martes). J Mamm 92:328–335
Mergey M, Larroque J, Ruette S, Vandel J, Helder R, Queney G, Devillard S (2012) Linking habitat characteristics with genetic diversity of the European pine marten (Martes martes) in France. Eur J Wildl Res 58:909–922
Natali C, Banchi E, Ciofi C, Manzo E, Bartolommei P, Cozzolino R (2010) Characterization of 13 polymorphic microsatellite loci in the European pine marten Martes martes. Conserv Genet Resour 2:397–399
Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) Vegan: Community Ecology Package. R package version 2.2-1. University of Oulu: Oulu, Finland. http://cran.r-project.org
Paetkau D, Strobeck C (1994) Microsatellite analysis of genetic variation in black bear populations. Mol Ecol 3:489–495
Peakall R, Smouse PE (2005) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295
Pertoldi C, Barker SF, Madsen AB, Jørgensen H, Randi E, Muñoz J, Baagoe HJ, Loeschcke V (2008) Spatio-temporal population genetics of the Danish pine marten (Martes martes). Biol J Linn Soc 93:457–464
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
R Development Core Team (2007) R: a language and environment for statistical computing. R foundation for Statistical Computing, Vienna
Rayfield B, Fortin MJ, Fall A (2010) The sensitivity of least-cost habitat graphs to relative cost surface values. Landscape Ecol 25:519–532
Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138
Ruiz-Gonzalez A, Cushman SA, Madeira MJ, Randi E, Gómez-Moliner BJ (2015) Isolation by distance, resistance and/or clusters? Lessons learned from a forest-dwelling carnivore inhabiting a heterogeneous landscape. Mol Ecol 24:5110–5129
Ruiz-González A, Gurrutxaga M, Cushman SA, Madeira MJ, Randi E, Gómez-Moliner BJ (2014) Landscape genetics for the empirical assessment of resistance surfaces: the European pine marten (Martes martes) as a target-species of a regional ecological network. PLoS ONE 9:e110552
Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452
Slatkin M (1973) Gene flow and selection in a cline. Genetics 75:733–756
Smouse P, Long J, Sokal R (1986) Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Syst Zool 35:627–632
Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573
Smouse PE, Peakall R, Gonzales E (2008) A heterogeneity test for fine-scale genetic structure. Mol Ecol 17(14):3389–3400
Storfer A, Murphy MA, Evans JS, Goldberg CS, Robinson S, Spear SF, Dezzani R, Delmelle E, Vierling L, Waits LP (2007) Putting the ‘landscape’ in landscape genetics. Heredity 98:128–142
Sunnucks P (2000) Efficient genetic markers for populationbiology. Trends Ecol Evol 15:199–203
Templeton AR (2006) Population genetics and microevolutionary theory. Wiley, Hoboken
Valière N (2002) Gimlet: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379
Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
Virgos E, Zalewski A, Rosalino LM, Mergey M (2012) Habitat ecology of genus Martes in Europe: a review of the evidences. In: Aubry KB, Zielinski WJ, Proulx G, Buskirk SW (eds) Biology and Conservation of Martens, sables, and fishers. A new synthesis. Cornell University Press, New York, pp 255–266
Wade TG, Riitters KH, Wickham JD, Jones KB (2003) Distribution and causes of global forest fragmentation. Conserv Ecol 7:7
Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256
Walker CW, Vila C, Landa A, Linden M, Ellegren H (2001) Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations. Mol Ecol 10(1):53–63
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370
Wright S (1943) Isolation by distance. Genetics 28:114–138
Zalewski A, Jedrzejewski W (2006) Spatial organisation and dynamics of the pine marten Martes martes population in Bialowieza Forest (E Poland) compared with other European woodlands. Ecography 29:31–43
Acknowledgements
This study has been funded by the Regional Concil of Champagne-Ardenne, by the University of Reims Champagne-Ardenne (URCA) through In Situ research program, by the French system of transmission system operators for electricity (Réseau de Transport Electrique, RTE), and by the Regional natural park of Avesnois. Data used in this work were partly produced through the technical facilities of the Centre Méditerranéen Environnement Biodiversité and of the Laboratoire des Pyrénées et des Landes. We thank all people who collaborated for samples collection and especially all hunters and trappers. We are also grateful to Eva Bellemain (SpyGen) for discussions on how to improve DNA amplification. Finally, we would like to thank Bertrand Gauffre and the two reviewers for comments that greatly improved the manuscript.
Funding
The Regional Concil of Champagne-Ardenne and the University of Reims Champagne-Ardenne through In Situ research program.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Mergey, M., Bardonnet, C., Quintaine, T. et al. Identifying environmental drivers of spatial genetic structure of the European pine marten (Martes martes). Landscape Ecol 32, 2261–2279 (2017). https://doi.org/10.1007/s10980-017-0567-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10980-017-0567-y