Abstract
Human activities have a major impact on habitat connectivity and landscape structure. In this context, it is critical to better understand animal movements and gene flow to develop appropriate conservation and land management measures. It is also important to better understand difference between sexes in space use and spatial scale of dispersal. We studied the common adder (Vipera berus), an elusive snake species with low mobility that is facing a substantial decline in Europe. A systematic sampling was carried out to clarify the dispersal pattern at a fine spatial scale (10 × 7 km2) in a rural landscape with both semi-natural (preserved heathlands, hedgerow networks) and degraded (crops, roads) habitats. Based on 280 captured adults and using 11 microsatellite markers, we detected no marked genetic differentiation, however, we detected relatively strong isolation-by-distance (IBD). Under IBD, we quantified a low neighborhood size (Ns ≈ 50) associated with limited natal dispersal (σ ≤ 1 km). We detected sex-biased dispersal in favor of males, but the pattern was dependent on the spatial scale considered. Our results also suggest that there is higher genetic diversity in the preserved habitat, notably among males. Overall, our study underlines the importance of sex variation in dispersal, and the spatial scale of landscape effects. This contrast between sexes should be considered to improve functional connectivity at fine spatial scales for reptile conservation.
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Data availability
Data are stored in the file named “INPUT_R_Data” in.csv format with semicolon separator. These data were used to create the file named “INPUT_GENEALEX” in.xlsx format. Its “export data” function was used to generate the other software input files. Depending on the software, inputs files are stored according to “INPUT_ SOFTWARE” in.txt format with tabulation for Spagedi, in.txt format with space for Structure and in.dat or.lab format for Fstat. Euclidean distances between individuals are stored in the files named “OUTPUT_Arcgis” in.csv format with semicolon separator. The datasets generated during and/or analysed during the current study are not publicly available due to threats to the species (e.g. disturbance or destruction of habitats or individuals) and its protection status in Brittany, but are available from the corresponding author on reasonable request.
Code availability
The R code is stored in the “R_script_Francois_et_al” in.Rmd format but is only available from the corresponding author on reasonable request (see above).
References
Amos JN, Harrisson KA, Radford JQ et al (2014) Species-and sex-specific connectivity effects of habitat fragmentation in a suite of woodland birds. Ecology 95:1556–1568. https://doi.org/10.1890/13-1328.1
Angelone S, Kienast F, Holderegger R (2011) Where movement happens: scale-dependent landscape effects on genetic differentiation in the European tree frog. Ecography 34:714–722. https://doi.org/10.1111/j.1600-0587.2010.06494.x
Aparicio JM, Ortego J, Cordero PJ (2006) What should we weigh to estimate heterozygosity, alleles or loci? Mol Ecol 15:4659–4665. https://doi.org/10.1111/j.1365-294X.2006.03111.x
Arntzen JW, Abrahams C, Meilink WRM et al (2017) Amphibian decline, pond loss and reduced population connectivity under agricultural intensification over a 38 year period. Biodivers Conserv 26:1411–1430. https://doi.org/10.1007/s10531-017-1307-y
Ball S, Hand N, Willman F et al (2020) Genetic and demographic vulnerability of adder populations: Results of a genetic study in mainland Britain. PLoS ONE 15:e0231809. https://doi.org/10.1371/journal.pone.0231809
Banks SC, Peakall R (2012) Genetic spatial autocorrelation can readily detect sex-biased dispersal. Mol Ecol 21:2092–2105. https://doi.org/10.1111/j.1365-294X.2012.05485.x
Bea A, Brana F, Baron J-P, Saint Girons H (1992) Régimes et cycles alimentaires des vipères européennes (Reptilia, Viperidae): étude comparée. Année Biol 31:25–44
Blair C, Weigel DE, Balazik M et al (2012) A simulation-based evaluation of methods for inferring linear barriers to gene flow. Mol Ecol Resour 12:822–833. https://doi.org/10.1111/j.1755-0998.2012.03151.x
Böhm M, Collen B, Baillie JEM et al (2013) The conservation status of the world’s reptiles. Biol Conserv 157:372–385. https://doi.org/10.1016/j.biocon.2012.07.015
Bonte D, Van Dyck H, Bullock JM et al (2012) Costs of dispersal. Biol Rev 87:290–312. https://doi.org/10.1111/j.1469-185X.2011.00201.x
Borcard D, Legendre P (2012) Is the Mantel correlogram powerful enough to be useful in ecological analysis? A simulation study. Ecology 93:1473–1481. https://doi.org/10.1890/11-1737.1
Borcard D, Gillet F, Legendre P (2011) Numerical ecology with R. Springer, New York
Brook BW, Sodhi NS, Bradshaw CJA (2008) Synergies among extinction drivers under global change. Trends Ecol Evol 23:453–460. https://doi.org/10.1016/j.tree.2008.03.011
Broquet PE (2009) Molecular estimation of dispersal for ecology and population genetics. Annu Rev Ecol Evol Syst 40:193–216. https://doi.org/10.1146/annurev.ecolsys.110308.120324
Burel F, Baudry J (1990) Structural dynamic of a hedgerow network landscape in Brittany France. Landsc Ecol 4:197–210. https://doi.org/10.1007/BF00129828
Canty A, Ripley BD (2017) boot: Bootstrap R (S-Plus) Functions
Carlsson M (2003) Phylogeography of the adder. University of Upssala, Vipera berus
Clark RW, Brown WS, Stechert R, Zamudio KR (2008) Integrating individual behaviour and landscape genetics: the population structure of timber rattlesnake hibernacula. Mol Ecol 17:719–730. https://doi.org/10.1111/j.1365-294X.2007.03594.x
Clutton-Brock TH, Lukas D (2012) The evolution of social philopatry and dispersal in female mammals. Mol Ecol 21:472–492. https://doi.org/10.1111/j.1365-294X.2011.05232.x
Coulon A (2010) genhet: an easy-to-use R function to estimate individual heterozygosity. Mol Ecol Resour 10:167–169. https://doi.org/10.1111/j.1755-0998.2009.02731.x
Coulon A, Cosson J-F, Morellet N et al (2006) Dispersal is not female biased in a resource-defence mating ungulate, the European roe deer. Proc R Soc B 273:341–348. https://doi.org/10.1098/rspb.2005.3329
Davison AC, Hinkley DV (1997) Bootstrap methods and their application. Cambridge University Press, Cambridge, NY
de Fraga R, Lima AP, Magnusson WE et al (2017) Contrasting patterns of gene flow for Amazonian snakes that actively forage and those that wait in ambush. J Hered 108:524–534. https://doi.org/10.1093/jhered/esx051
DiLeo MF, Rouse JD, Dávila JA, Lougheed SC (2013) The influence of landscape on gene flow in the eastern massasauga rattlesnake (Sistrurus c. catenatus): insight from computer simulations. Mol Ecol 22:4483–4498. https://doi.org/10.1111/mec.12411
Doherty TS, Balouch S, Bell K et al (2020) Reptile responses to anthropogenic habitat modification: a global meta-analysis. Glob Ecol Biogeogr 29:1265–1279. https://doi.org/10.1111/geb.13091
Dubey S, Brown GP, Madsen T, Shine R (2008) Male-biased dispersal in a tropical Australian snake (Stegonotus cucullatus, Colubridae). Mol Ecol 17:3506–3514. https://doi.org/10.1111/j.1365-294X.2008.03859.x
Dupont L, Grésille Y, Richard B et al (2015) Dispersal constraints and fine-scale spatial genetic structure in two earthworm species. Biol J Linn Soc 114:335–347
Durso AM, Willson JD, Winne CT (2011) Needles in haystacks: estimating detection probability and occupancy of rare and cryptic snakes. Biol Conserv 144:1508–1515. https://doi.org/10.1016/j.biocon.2011.01.020
Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361. https://doi.org/10.1007/s12686-011-9548-7
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. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. https://doi.org/10.1111/j.1466-8238.2006.00287.x
Flavenot T, Fellous S, Abdelkrim J et al (2015) Impact of quarrying on genetic diversity: an approach across landscapes and over time. Conserv Genet 16:181–194. https://doi.org/10.1007/s10592-014-0650-8
Folt B, Bauder J, Spear S et al (2019) Taxonomic and conservation implications of population genetic admixture, mito-nuclear discordance, and male-biased dispersal of a large endangered snake, Drymarchon couperi. PLOS ONE 14:e0214439. https://doi.org/10.1371/journal.pone.0214439
Gardner E, Julian A, Monk C, Baker J (2019) Make the Adder Count: population trends from a citizen science survey of UK adders. Herpetol J 29:57–70. https://doi.org/10.33256/hj29.1.5770
Gauffre B, Petit E, Brodier S et al (2009) Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proc R Soc B 276:3487–3494. https://doi.org/10.1098/rspb.2009.0881
Geser S, Kaiser L, Zwahlen V, Ursenbacher S (2013) Development of polymorphic microsatellite loci markers for the Asp viper (Vipera aspis) using high-throughput sequencing and their use for other European vipers. Amphib-Reptil 34:109–113. https://doi.org/10.1163/15685381-00002861
Goslee SC, Urban DL (2007) The ecodist package for dissimilarity-based analysis of ecological data. J Stat Softw 22:1–19
Goudet J (1995) FSTAT (version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486. https://doi.org/10.1093/oxfordjournals.jhered.a111627
Goudet J, Jombart T (2015) hierfstat: estimation and tests of hierarchical F-statistics. R package version 0.04-22
Graitson E, Ursenbacher S, Lourdais O (2020) Snake conservation in anthropized landscapes: considering artificial habitats and questioning management of semi-natural habitats. Eur J Wildl Res. https://doi.org/10.1007/s10344-020-01373-2
Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Anim Behav 28:1140–1162
Guerrini M, Gennai C, Panayides P et al (2014) Large-scale patterns of genetic variation in a female-biased dispersing Passerine: the importance of sex-based analyses. PLoS ONE 9:e98574. https://doi.org/10.1371/journal.pone.0098574
Guiller G, Legentilhomme J (2015) Classification de classes d’âges (nouveau-né, immature et mature) en fonction de la taille chez six espèces d’ophidiens du département de la Loire-Atlantique. Bull Soc Sci Nat Ouest Fr 37:135–142
Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620. https://doi.org/10.1046/j.1471-8278.2002.00305.x
Hillman SS, Drewes RC, Hedrick MS, Hancock TV (2014a) Physiological vagility: correlations with dispersal and population genetic structure of amphibians. Physiol Biochem Zool 87:105–112. https://doi.org/10.1086/671109
Hillman SS, Drewes RC, Hedrick MS, Hancock TV (2014b) Physiological vagility and its relationship to dispersal and neutral genetic heterogeneity in vertebrates. J Exp Biol 217:3356–3364. https://doi.org/10.1242/jeb.105908
Hofmann S, Fritzsche P, Solhøy T et al (2012) Evidence of sex-biased dispersal in Thermophis baileyi inferred from microsatellite markers. Herpetologica 68:514–522. https://doi.org/10.1655/HERPETOLOGICA-D-12-00017
Jackson HB, Fahrig L (2012) What size is a biologically relevant landscape? Landsc Ecol 27:929–941. https://doi.org/10.1007/s10980-012-9757-9
Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Glob Ecol Biogeogr 24:52–63. https://doi.org/10.1111/geb.12233
Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. https://doi.org/10.1093/bioinformatics/btn129
Keller D, Holderegger R, van Strien MJ (2013) Spatial scale affects landscape genetic analysis of a wetland grasshopper. Mol Ecol 22:2467–2482. https://doi.org/10.1111/mec.12265
Keller D, Holderegger R, van Strien MJ, Bolliger J (2015) How to make landscape genetics beneficial for conservation management? Conserv Genet 16:503–512. https://doi.org/10.1007/s10592-014-0684-y
Kéry M (2002) Inferring the absence of a species: a case study of snakes. J Wildl Manag 66:330–338. https://doi.org/10.2307/3803165
King RB (2009) Population and conservation genetics. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Comstock Pub. Associates/Cornell University Press, Ithaca, pp 78–122
King RB, Lawson R (2001) Patterns of population subdivision and gene flow in three sympatric natricine snakes. Copeia 2001:602–614
Landguth EL, Cushman SA, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191. https://doi.org/10.1111/j.1365-294X.2010.04808.x
Lawson Handley LJ, Perrin N (2007) Advances in our understanding of mammalian sex-biased dispersal. Mol Ecol 16:1559–1578. https://doi.org/10.1111/j.1365-294X.2006.03152.x
Lechner AM, Langford WT, Jones SD et al (2012) Investigating species–environment relationships at multiple scales: Differentiating between intrinsic scale and the modifiable areal unit problem. Ecol Complex 11:91–102. https://doi.org/10.1016/j.ecocom.2012.04.002
Legendre P, Legendre L (2012) Numerical ecology, 3rd English edn. Elsevier, Amsterdam
Li X-Y, Kokko H (2019) Sex-biased dispersal: a review of the theory. Biol Rev 94:721–736. https://doi.org/10.1111/brv.12475
Lorioux S, Angelier F, Lourdais O (2016) Are glucocorticoids good indicators of pregnancy constraints in a capital breeder? Gen Comp Endocrinol 232:125–133. https://doi.org/10.1016/j.ygcen.2016.04.007
Lourdais O, Gartner GE, Brischoux F (2014) Ambush or active life: foraging mode influences haematocrit levels in snakes. Biol J Linn Soc 111:636–645
Lowe WH, Allendorf FW (2010) What can genetics tell us about population connectivity? Mol Ecol 19:3038–3051. https://doi.org/10.1111/j.1365-294X.2010.04688.x
Luiselli L (1993) High philopatry can produce strong sexual competition in male adders, Vipera berus. Amphib-Reptil 14:310–311. https://doi.org/10.1163/156853893X00516
Madsen T, Shine R (1992a) Sexual competition among brothers may influence offspring sex ratio in snakes. Evolution 46:1549–1552. https://doi.org/10.2307/2409957
Madsen T, Shine R (1992b) Determinants of reproductive success in female adders, Vipera berus. Oecologia 92:40–47
Madsen T, Shine R (1993) Costs of reproduction in a population of European adders. Oecologia 94:488–495
Madsen T, Shine R, Loman J, Håkansson T (1993) Determinants of mating success in male adders, Vipera berus. Anim Behav 45:491–499. https://doi.org/10.1006/anbe.1993.1060
Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:35–35. https://doi.org/10.1038/46944
Madsen T, Stille B, Shine R (1996) Inbreeding depression in an isolated population of adders Vipera berus. Biol Conserv 75:113–118. https://doi.org/10.1016/0006-3207(95)00067-4
Madsen T, Ujvari B, Olsson M (2004) Novel genes continue to enhance population growth in adders (Vipera berus). Biol Conserv 120:145–147. https://doi.org/10.1016/j.biocon.2004.01.022
Manier MK, Arnold SJ (2005) Population genetic analysis identifies source-sink dynamics for two sympatric garter snake species (Thamnophis elegans and Thamnophis sirtalis). Mol Ecol 14:3965–3976. https://doi.org/10.1111/j.1365-294X.2005.02734.x
Matthysen E (2012) Multicausality of dispersal: a review. In: Clobert J, Baguette M, Benton TG, Bullock JM (eds) Dispersal ecology and evolution, 1st edn. Oxford University Press, Oxford, pp 3–18
Meister B, Ursenbacher S, Baur B (2012) Grass snake population differentiation over different geographic scales. Herpetologica 68:134–145. https://doi.org/10.1655/HERPETOLOGICA-D-11-00036.1
Metzger C, Ferchaud A-L, Geiser C, Ursenbacher S (2011) New polymorphic microsatellite markers of the endangered meadow viper (Vipera ursinii) identified by 454 high-throughput sequencing: when innovation meets conservation. Conserv Genet Resour 3:589–592. https://doi.org/10.1007/s12686-011-9411-x
Moore JA, Miller HC, Daugherty CH, Nelson NJ (2008) Fine-scale genetic structure of a long-lived reptile reflects recent habitat modification. Mol Ecol 17:4630–4641. https://doi.org/10.1111/j.1365-294X.2008.03951.x
Motro U (1991) Avoiding inbreeding and sibling competition: the evolution of sexual dimorphism for dispersal. Am Nat 137:108–115
Moya Ó, Mansilla P-L, Madrazo S et al (2015) APHIS: A new software for photo-matching in ecological studies. Ecol Inform 27:64–70. https://doi.org/10.1016/j.ecoinf.2015.03.003
Mullin SJ, Seigel RA (eds) (2009) Snakes: ecology and conservation. Comstock Pub. Associates/Cornell University Press, Ithaca
Neumeyer R (1987) Density and seasonal movements of the adder (Vipera berus L. 1758) in a subalpine environment. Amphib-Reptil 8:259–276. https://doi.org/10.1163/156853887X00306
Newbold T, Hudson LN, Hill SLL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50. https://doi.org/10.1038/nature14324
Niebuhr BBS, Wosniack ME, Santos MC et al (2015) Survival in patchy landscapes: the interplay between dispersal, habitat loss and fragmentation. Sci Rep. https://doi.org/10.1038/srep11898
Öckinger E, Schweiger O, Crist TO et al (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13:969–979. https://doi.org/10.1111/j.1461-0248.2010.01487.x
Oden NL, Sokal RR (1986) Directional autocorrelation: an extension of spatial correlograms to two dimensions. Syst Zool 35:608–617
Oksanen J, Blanchet FG, Kindt R, et al (2016) vegan: Community Ecology Package. R package version 2.3–4
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Pernetta AP, Allen JA, Beebee TJC, Reading CJ (2011) Fine-scale population genetic structure and sex-biased dispersal in the smooth snake (Coronella austriaca) in southern England. Heredity 107:231–238. https://doi.org/10.1038/hdy.2011.7
Perrin N, Mazalov V (2000) Local competition, inbreeding, and the evolution of sex-biased dispersal. Am Nat 155:116–127
Pike DA (2016) Conservation management. In: Dodd CKJ (ed) Reptile ecology and conservation: a handbook of techniques. Oxford University Press, Oxford, pp 419–435
Powers RP, Jetz W (2019) Global habitat loss and extinction risk of terrestrial vertebrates under future land-use-change scenarios. Nat Clim Chang 9:323–329. https://doi.org/10.1038/s41558-019-0406-z
Prestt I (1971) An ecological study of the viper Vipera berus in southern Britain. J Zool 164:373–418. https://doi.org/10.1111/j.1469-7998.1971.tb01324.x
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Prunier JG, Kaufmann B, Fenet S et al (2013) Optimizing the trade-off between spatial and genetic sampling efforts in patchy populations: towards a better assessment of functional connectivity using an individual-based sampling scheme. Mol Ecol 22:5516–5530. https://doi.org/10.1111/mec.12499
R Core Development Team (2020) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna
Reading CJ, Luiselli LM, Akani GC et al (2010) Are snake populations in widespread decline? Biol Lett 6:777–780. https://doi.org/10.1098/rsbl.2010.0373
Rivera PC, Gardenal CN, Chiaraviglio M (2006) Sex-biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor, Boa constrictor occidentalis. Austral Ecol 31:948–955. https://doi.org/10.1111/j.1442-9993.2006.01661.x
Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253. https://doi.org/10.1146/annurev.ecolsys.38.091206.095611
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228
Rousset F (2000) Genetic differentiation between individuals. J Evol Biol 13:58–62. https://doi.org/10.1046/j.1420-9101.2000.00137.x
Saint Girons H (1980) Biogéographie et évolution des vipères européennes. C R Soc Biogéogr 496:146–172
Santos X, Brito JC, Sillero N et al (2006) Inferring habitat-suitability areas with ecological modelling techniques and GIS: a contribution to assess the conservation status of Vipera latastei. Biol Conserv 130:416–425. https://doi.org/10.1016/j.biocon.2006.01.003
Sheldon S, Bradley C (1989) Identification of individual adders (Vipera berus) by their head markings. Herpetol J 1:392–395
Sokal (1986) Spatial data analysis and historical processes. In: Diday E, International Symposium on Data Analysis and Informatics, Institut National de Recherche en Informatique et en Automatique (eds) Data analysis and informatics, IV. North-Holland, Amsterdam, pp 29–43
Stow AJ, Sunnucks P, Briscoe DA, Gardner MG (2001) The impact of habitat fragmentation on dispersal of Cunningham’s skink (Egernia cunninghami): evidence from allelic and genotypic analyses of microsatellites. Mol Ecol 10:867–878. https://doi.org/10.1046/j.1365-294X.2001.01253.x
Sumner J, Rousset F, Estoup A, Moritz C (2001) ‘Neighbourhood’size, dispersal and density estimates in the prickly forest skink (Gnypetoscincus queenslandiae) using individual genetic and demographic methods. Mol Ecol 10:1917–1927. https://doi.org/10.1046/j.0962-1083.2001.01337.x
Sumner J, Jessop T, Paetkau D, Moritz C (2004) Limited effect of anthropogenic habitat fragmentation on molecular diversity in a rain forest skink, Gnypetoscincus queenslandiae. Mol Ecol 13:259–269. https://doi.org/10.1046/j.1365-294X.2003.02056.x
Trochet A, Courtois EA, Stevens VM et al (2016) Evolution of sex-biased dispersal. Q Rev Biol 91:297–320. https://doi.org/10.1086/688097
Ursenbacher S, Monney J-C, Fumagalli L (2009) Limited genetic diversity and high differentiation among the remnant adder (Vipera berus) populations in the Swiss and French Jura Mountains. Conserv Genet 10:303–315. https://doi.org/10.1007/s10592-008-9580-7
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. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Viitanen P (1967) Hibernation and seasonal movements of the viper, Vipera berus berus (L.), in southern Finland. Ann Zool Fenn 4:472–546
Weatherhead PJ, Madsen T (2009) Linking behavioral ecology to conservation objectives. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Comstock Pub. Associates/Cornell University Press, Ithaca, pp 149–171
Webb JK, Shine R (1997) A field study of spatial ecology and movements of a threatened snake species, Hoplocephalus bungaroides. Biol Conserv 82:203–217
Acknowledgements
This work was funded by the Ministère de l’Enseignement Supérieur et de la Recherche (Ph.D grant to DF) and the Service du Patrimoine Naturel du Département d’Ille-et-Vilaine which manages the Natura 2000 site of “Vallée du Canut” as an “Espace Naturel Sensible” (ENS). We address special thanks to all the field workers: Régis Morel (Chargé de mission Bretagne-Vivante), Manon Vasseur, Mélaine Rouault, Morgan Le Vot and Maxime Spagnol. We thank Valerie Zwahlen (laboratory technician) for carrying out the genetic analyses at the University of Basel. We also thank Juan José Robledo-Arnuncio and Jérôme Prunier for advice about statistics. Finally, we thank Jean-Pierre Vacher, Sydney Hope and the two anonymous reviewers for their helpful comments on the manuscript.
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This work was financially supported by the Ministère de l’Enseignement supérieur et de la recherche (Ph.D grant to DF) and the Service du patrimoine naturel du Département d’Ille-et-Vilaine which manages the Natura 2000 site of “Vallée du Canut” as an “Espace naturel sensible” (ENS).
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DF and FY applied for grants for the project. DF designed the experiments with the help of SU and OL. DF and OL participated to field work and enhanced its implementation. SU supervised the laboratory work. DF and SU analysed the data. DF wrote most of the manuscript. AB, DF, FY, OL and SU discussed the results, the analyses, and commented or modified the manuscript.
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François, D., Ursenbacher, S., Boissinot, A. et al. Isolation-by-distance and male-biased dispersal at a fine spatial scale: a study of the common European adder (Vipera berus) in a rural landscape. Conserv Genet 22, 823–837 (2021). https://doi.org/10.1007/s10592-021-01365-y
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DOI: https://doi.org/10.1007/s10592-021-01365-y