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Lack of detectable genetic isolation in the cyclic rodent Microtus arvalis despite large landscape fragmentation owing to transportation infrastructures

  • 1.

    Ibisch, P. L. et al. A global map of roadless areas and their conservation status. Science 354, 1423–1427 (2016).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 2.

    Torres, A., Jaeger, J. A. G. & Alonso, J. C. Assessing large-scale wildlife responses to human infrastructure development. PNAS 113, 8472–8477 (2016).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 3.

    Bennett, V. J. Effects of road density and pattern on the conservation of species and biodiversity. Curr. Landsc. Ecol. Rep. 2, 1–11 (2017).

    Article 

    Google Scholar 

  • 4.

    Coffin, A. W. From roadkill to road ecology: a review of the ecological effects of roads. J. Transp. Geogr. 15, 396–406 (2007).

    Article 

    Google Scholar 

  • 5.

    Fahrig, L. & Rytwinski, T. Effects of roads on animal abundance: an empirical review and synthesis. Ecol. Soc. 14, 21 (2009).

    Article 

    Google Scholar 

  • 6.

    Forman, R. T. & Alexander, L. E. Roads and their major ecological effects. Annu. Rev. Ecol. Syst. 29, 207–231 (1998).

    Article 

    Google Scholar 

  • 7.

    Trombulak, S. C. & Frissell, C. A. Review of ecological effects of roads on terrestrial and aquatic communities. Conserv. Biol. 14, 18–30 (2000).

    Article 

    Google Scholar 

  • 8.

    Ascensão, F. et al. Disentangle the causes of the road barrier effect in small mammals through genetic patterns. PLoS ONE 11, e0151500 (2016).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 9.

    Dyer, S. J., O’Neill, J. P., Wasel, S. M. & Boutin, S. Quantifying barrier effects of roads and seismic lines on movements of female woodland caribou in northeastern Alberta. Can. J. Zool. 80, 839–845 (2002).

    Article 

    Google Scholar 

  • 10.

    Glista, D. J., DeVault, T. L. & DeWoody, J. A. A review of mitigation measures for reducing wildlife mortality on roadways. Landsc. Urban Plan. 91, 1–7 (2009).

    Article 

    Google Scholar 

  • 11.

    Taylor, B. D. & Goldingay, R. L. Roads and wildlife: impacts, mitigation and implications for wildlife management in Australia. Wildl. Res. 37, 320–331 (2010).

    Article 

    Google Scholar 

  • 12.

    Tigas, L. A., Van Vuren, D. H. & Sauvajot, R. M. Behavioral responses of bobcats and coyotes to habitat fragmentation and corridors in an urban environment. Biol. Conserv. 108, 299–306 (2002).

    Article 

    Google Scholar 

  • 13.

    Herrmann, H.-W., Pozarowski, K. M., Ochoa, A. & Schuett, G. W. An interstate highway affects gene flow in a top reptilian predator (Crotalus atrox) of the Sonoran Desert. Conserv. Genet. 18, 911–924 (2017).

    CAS 
    Article 

    Google Scholar 

  • 14.

    Holderegger, R. & Di Giulio, M. The genetic effects of roads: a review of empirical evidence. Basic Appl. Ecol. 11, 522–531 (2010).

    Article 

    Google Scholar 

  • 15.

    Keller, L. F. & Waller, D. M. Inbreeding effects in wild populations. Trends Ecol. Evol. 17, 230–241 (2002).

    Article 

    Google Scholar 

  • 16.

    Benítez-López, A., Alkemade, R. & Verweij, P. A. The impacts of roads and other infrastructure on mammal and bird populations: a meta-analysis. Biol. Conserv. 143, 1307–1316 (2010).

    Article 

    Google Scholar 

  • 17.

    Kerley, L. L. et al. Effects of roads and human disturbance on Amur tigers. Conserv. Biol. 16, 97–108 (2002).

    Article 

    Google Scholar 

  • 18.

    Roedenbeck, I. A. & Voser, P. Effects of roads on spatial distribution, abundance and mortality of brown hare (Lepus europaeus) in Switzerland. Eur. J. Wildl. Res. 54, 425–437 (2008).

    Article 

    Google Scholar 

  • 19.

    Clark, R. W., Brown, W. S., Stechert, R. & Zamudio, K. R. Roads, interrupted dispersal, and genetic diversity in timber Rattlesnakes. Conserv. Biol. 24, 1059–1069 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 20.

    Niko, B. & Waits, L. P. Molecular road ecology: exploring the potential of genetics for investigating transportation impacts on wildlife. Mol. Ecol. 18, 4151–4164 (2009).

    Article 

    Google Scholar 

  • 21.

    Frankham, R., Briscoe, D. A. & Ballou, J. D. Introduction to Conservation Genetics (Cambridge University Press, 2002).

    Book 

    Google Scholar 

  • 22.

    Amos, W. & Balmford, A. When does conservation genetics matter?. Heredity 87, 257–265 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 23.

    Frankham, R. Genetics and extinction. Biol. Cons. 126, 131–140 (2005).

    Article 

    Google Scholar 

  • 24.

    Teixeira, J. C. & Huber, C. D. The inflated significance of neutral genetic diversity in conservation genetics. Proc. Natl. Acad. Sci. U. S. A. 118, e2015096118 (2021).

    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 25.

    Keller, I. & Largiadèr, C. R. Recent Habitat fragmentation caused by major roads leads to reduction of gene flow and loss of genetic variability in ground beetles. Proc. Biol. Sci. 270, 417–423 (2003).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 26.

    Noël, S., Ouellet, M., Galois, P. & Lapointe, F.-J. Impact of urban fragmentation on the genetic structure of the eastern red-backed salamander. Conserv. Genet. 8, 599–606 (2007).

    Article 
    CAS 

    Google Scholar 

  • 27.

    Marsh, D. M. et al. Effects of roads on patterns of genetic differentiation in red-backed salamanders, Plethodon cinereus. Conserv. Genet. 9, 603–613 (2008).

    Article 

    Google Scholar 

  • 28.

    Brehme, C. S., Tracey, J. A., Mcclenaghan, L. R. & Fisher, R. N. Permeability of roads to movement of scrubland lizards and small mammals. Conserv. Biol. 27, 710–720 (2013).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 29.

    Ford, A. T. & Clevenger, A. P. Factors affecting the permeability of road mitigation measures to the movement of small mammals. Can. J. Zool. 97, 379–384 (2018).

    Article 

    Google Scholar 

  • 30.

    Claireau, F. et al. Major roads have important negative effects on insectivorous bat activity. Biol. Conserv. 235, 53–62 (2019).

    Article 

    Google Scholar 

  • 31.

    Jacobson, S. L., Bliss-Ketchum, L. L., Rivera, C. E. & Smith, W. P. A behavior-based framework for assessing barrier effects to wildlife from vehicle traffic volume. Ecosphere 7, e01345 (2016).

    Article 

    Google Scholar 

  • 32.

    Assis, J. C., Giacomini, H. C. & Ribeiro, M. C. Road permeability index: evaluating the heterogeneous permeability of roads for wildlife crossing. Ecol. Ind. 99, 365–374 (2019).

    Article 

    Google Scholar 

  • 33.

    Lesbarrères, D., Primmer, C. R., Lodé, T. & Merilä, J. The effects of 20 years of highway presence on the genetic structure of Rana dalmatina populations. Écoscience 13, 531–538 (2006).

    Article 

    Google Scholar 

  • 34.

    Landguth, E. L. et al. Quantifying the lag time to detect barriers in landscape genetics: quantifying the lag time to detect barriers in landscape genetics. Mol. Ecol. 19, 4179–4191 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 35.

    Epps, C. W. & Keyghobadi, N. Landscape genetics in a changing world: disentangling historical and contemporary influences and inferring change. Mol. Ecol. 24, 6021–6040 (2015).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 36.

    Blair, C. et al. A simulation-based evaluation of methods for inferring linear barriers to gene flow. Mol. Ecol. Resour. 12, 822–833 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 37.

    Mona, S., Ray, N., Arenas, M. & Excoffier, L. Genetic consequences of habitat fragmentation during a range expansion. Heredity 112, 291–299 (2014).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 38.

    Weyer, J., Jørgensen, D., Schmitt, T., Maxwell, T. J. & Anderson, C. D. Lack of detectable genetic differentiation between den populations of the Prairie Rattlesnake (Crotalus viridis) in a fragmented landscape. Can. J. Zool. 92, 837–846 (2014).

    Article 

    Google Scholar 

  • 39.

    Frankham, R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 10, 1500–1508 (1996).

    Article 

    Google Scholar 

  • 40.

    Ehrich, D. & Jorde, P. E. High genetic variability despite high-amplitude population cycles in lemmings. J. Mammal. 86, 380–385 (2005).

    Article 

    Google Scholar 

  • 41.

    Gauffre, B. et al. Short-term variations in gene flow related to cyclic density fluctuations in the common vole. Mol. Ecol. 23, 3214–3225 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 42.

    Schweizer, M., Excoffier, L. & Heckel, G. Fine-scale genetic structure and dispersal in the common vole (Microtus arvalis). Mol. Ecol. 16, 2463–2473 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 43.

    Keane, B., Ross, S., Crist, T. O. & Solomon, N. G. Fine-scale spatial patterns of genetic relatedness among resident adult prairie voles. J. Mammal. 96, 1194–1202 (2015).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 44.

    Boyce, C. C. K. & Boyce, J. L. Population biology of Microtus arvalis. II. Natal and breeding dispersal of females. J. Anim. Ecol. 57, 723–736 (1988).

    Article 

    Google Scholar 

  • 45.

    Luque-Larena, J. J. et al. Recent large-scale range expansion and outbreaks of the common vole (Microtus arvalis) in NW Spain. Basic Appl. Ecol. 14, 432–441 (2013).

    Article 

    Google Scholar 

  • 46.

    Salamolard, M., Butet, A., Leroux, A. & Bretagnolle, V. Responses of an avian predator to variations in prey density at a temperate latitude. Ecology 81, 2428–2441 (2000).

    Article 

    Google Scholar 

  • 47.

    Krebs, C. J. & Myers, J. H. Population cycles in small mammals. In Advances in Ecological Research Vol. 8 (ed. MacFadyen, A.) 267–399 (Academic Press, 1974).

    Google Scholar 

  • 48.

    Gerlach, G. & Musolf, K. Fragmentation of landscape as a cause for genetic subdivision in bank voles. Conserv. Biol. 14, 1066–1074 (2000).

    Article 

    Google Scholar 

  • 49.

    Rico, A., Kindlmann, P. & Sedláček, F. Can the barrier effect of highways cause genetic subdivision in small mammals?. Acta Theriol. 54, 297–310 (2009).

    Article 

    Google Scholar 

  • 50.

    Nei, M., Maruyama, T. & Chakraborty, R. The bottleneck effect and genetic variability in populations. Evolution 29, 1–10 (1975).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 51.

    Motro, U. & Thomson, G. On heterozygosity and the effective size of populations subject to size changes. Evolution 36, 1059–1066 (1982).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 52.

    Kirkpatrick, M. & Jarne, P. The effects of a bottleneck on inbreeding depression and the genetic load. Am. Nat. 155, 154–167 (2000).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 53.

    Xenikoudakis, G. et al. Consequences of a demographic bottleneck on genetic structure and variation in the Scandinavian brown bear. Mol. Ecol. 24, 3441–3454 (2015).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 54.

    Parra, G. J. et al. Low genetic diversity, limited gene flow and widespread genetic bottleneck effects in a threatened dolphin species, the Australian humpback dolphin. Biol. Conserv. 220, 192–200 (2018).

    Article 

    Google Scholar 

  • 55.

    Berthier, K., Charbonnel, N., Galan, M., Chaval, Y. & Cosson, J.-F. Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol. Ecol. 15, 2665–2676 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 56.

    Norén, K. & Angerbjörn, A. Genetic perspectives on northern population cycles: bridging the gap between theory and empirical studies: GENETIC structure in cyclic populations. Biol. Rev. 89, 493–510 (2014).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 57.

    Jangjoo, M., Matter, S. F., Roland, J. & Keyghobadi, N. Demographic fluctuations lead to rapid and cyclic shifts in genetic structure among populations of an alpine butterfly, Parnassius smintheus. J. Evol. Biol. 33, 668–681 (2020).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 58.

    ESRI. ArcGIS desktop: release 10.3 Environmental Systems Research Institute, Redlands, CA (2015).

  • 59.

    Saunders, S. C., Mislivets, M. R., Chen, J. & Cleland, D. T. Effects of roads on landscape structure within nested ecological units of the Northern Great Lakes Region, USA. Biol. Conserv. 103, 209–225 (2002).

    Article 

    Google Scholar 

  • 60.

    Fahrig, L. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34, 487–515 (2003).

    Article 

    Google Scholar 

  • 61.

    Schlaepfer, D. R., Braschler, B., Rusterholz, H.-P. & Baur, B. Genetic effects of anthropogenic habitat fragmentation on remnant animal and plant populations: a meta-analysis. Ecosphere 9, e02488 (2018).

    Article 

    Google Scholar 

  • 62.

    Charlesworth, B. Effective population size and patterns of molecular evolution and variation. Nat. Rev. Genet. 10, 195–205 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 63.

    Compton, B. W., McGarigal, K., Cushman, S. A. & Gamble, L. R. A resistant-Kernel model of connectivity for amphibians that breed in vernal pools. Conserv. Biol. 21, 788–799 (2007).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 64.

    Balkenhol, N., Cushman, S., Storfer, A. & Waits, L. Landscape Genetics: Concepts, Methods, Applications (Wiley, 2015).

    Book 

    Google Scholar 

  • 65.

    Aguilar, R., Quesada, M., Ashworth, L., Herrerias-Diego, Y. & Lobo, J. Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol. Ecol. 17, 5177–5188 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 66.

    Lloyd, M. W., Campbell, L. & Neel, M. C. The Power to Detect Recent Fragmentation Events Using Genetic Differentiation Methods. PLoS ONE 8, e63981 (2013).

    ADS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 67.

    Smouse, P. E., Long, J. C. & Sokal, R. R. Multiple regression and correlation extensions of the mantel test of matrix correspondence. Syst. Zool. 35, 627–632 (1986).

    Article 

    Google Scholar 

  • 68.

    Nowak, R. M. Walker’s Mammals of the World (Johns Hopkins University Press, 1999).

    Google Scholar 

  • 69.

    García, J. T. et al. A complex scenario of glacial survival in Mediterranean and continental refugia of a temperate continental vole species (Microtus arvalis) in Europe. J. Zool. Syst. Evol. Res. 58, 459–474 (2020).

    Article 

    Google Scholar 

  • 70.

    Martínková, N. et al. Divergent evolutionary processes associated with colonization of offshore islands. Mol. Ecol. 22, 5205–5220 (2013).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 71.

    Keyghobadi, N. K. The genetic implications of habitat fragmentation for animals. Can. J. Zool. 85(10), 1049–1064 (2007).

    Article 

    Google Scholar 

  • 72.

    Vandergast, A. G., Bohonak, A. J., Weissman, D. B. & Fisher, R. N. Understanding the genetic effects of recent habitat fragmentation in the context of evolutionary history: phylogeography and landscape genetics of a southern California endemic Jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus). Mol. Ecol. 16, 977–992 (2007).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 73.

    Zellmer, A. J. & Knowles, L. L. Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Mol. Ecol. 18, 3593–3602 (2009).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 74.

    Delaney, K. S., Riley, S. P. D. & Fisher, R. N. A rapid, strong, and convergent genetic response to urban habitat fragmentation in four divergent and widespread vertebrates. PLoS ONE 5, e12767 (2010).

    ADS 
    PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 

  • 75.

    Tkadlec, E. & Stenseth, N. C. A new geographical gradient in vole population dynamics. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268, 1547–1552 (2001).

    CAS 
    Article 

    Google Scholar 

  • 76.

    Lambin, X., Bretagnolle, V. & Yoccoz, N. G. Vole population cycles in northern and southern Europe: Is there a need for different explanations for single pattern?. J. Anim. Ecol. 75, 340–349 (2006).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 77.

    Ehrich, D. & Stenseth, N. C. Genetic structure of Siberian lemmings (Lemmus sibiricus) in a continuous habitat: large patches rather than isolation by distance. Heredity 86, 716–730 (2001).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 78.

    Gauffre, B., Estoup, A., Bretagnolle, V. & Cosson, J. F. Spatial genetic structure of a small rodent in a heterogeneous landscape. Mol. Ecol. 17, 4619–4629 (2008).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 79.

    Galliard, J.-F.L., Rémy, A., Ims, R. A. & Lambin, X. Patterns and processes of dispersal behaviour in arvicoline rodents. Mol. Ecol. 21, 505–523 (2012).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 80.

    Gauffre, B., Petit, E., Brodier, S., Bretagnolle, V. & Cosson, J. F. Sex-biased dispersal patterns depend on the spatial scale in a social rodent. Proc. R. Soc. B Biol. Sci. 276, 3487 (2009).

    CAS 
    Article 

    Google Scholar 

  • 81.

    Lidicker, W.Z. Jr. The role of dispersal in the demography of small mammals, in Small Mammals: their production and population dynamics. Eds F.B. Golley, K. Petrusewicz and L. Ryszkowski, 103–28 (Cambridge University Press, London, 1975).

  • 82.

    Gaines, M. S. & McClenaghan, L. R. Dispersal in small mammals. Annu. Rev. Ecol. Syst. 11, 163–196 (1980).

    Article 

    Google Scholar 

  • 83.

    Swingland, I. R. & Greenwood, P. J. The Ecology of Animal Movement (Clarendon Press, 1983).

    Google Scholar 

  • 84.

    Burton, C., Krebs, C. J. & Taylor, E. B. Population genetic structure of the cyclic snowshoe hare (Lepus americanus) in southwestern Yukon, Canada. Mol. Ecol. 11, 1689–1701 (2002).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 85.

    Plante, Y., Boag, P. T. & White, B. N. Microgeographic variation in mitochondrial DNA of meadow voles (Microtus pennsylvanicus) in relation to population density. Evolution 43, 1522–1537 (1989).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 86.

    Encuesta sobre superficies y rendimientos del cultivo 2012. Catálogo de publicaciones de la Administración General del Estado (MAGRAMA, 2013).

  • 87.

    Oñate, J. J. et al. Programa piloto de acciones de conservación de la biodiversidad en sistemas ambientales con usos agrarios en el marco del desarrollo rural. Convenio de colaboración entre la Dirección General para la Biodiversidad (Ministerio de Medio Ambiente) y el Departamento Interuniversitario de Ecología (Universidad Autónoma de Madrid, 2003).

  • 88.

    Ji, S. et al. Impact of different road types on small mammals in Mt. Kalamaili Nature Reserve. Transp. Res. Part D Transp. Environ. 50, 223–233 (2017).

    Article 

    Google Scholar 

  • 89.

    Vignieri, S. N. Streams over mountains: influence of riparian connectivity on gene flow in the Pacific jumping mouse (Zapus trinotatus): connectivity patterns in pacific jumping mice. Mol. Ecol. 14, 1925–1937 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 90.

    Russo, I.-R.M., Sole, C. L., Barbato, M., von Bramann, U. & Bruford, M. W. Landscape determinants of fine-scale genetic structure of a small rodent in a heterogeneous landscape (Hluhluwe-iMfolozi Park, South Africa). Sci. Rep. 6, 29168 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 91.

    Mougeot, F., Lambin, X., Rodríguez-Pastor, R., Romairone, J. & Luque-Larena, J.-J. Numerical response of a mammalian specialist predator to multiple prey dynamics in Mediterranean farmlands. Ecology 100, e02776 (2019).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 92.

    Schwartz, M. K. & McKelvey, K. S. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv. Genet. 10, 441 (2009).

    Article 

    Google Scholar 

  • 93.

    Strauss, W. M. Preparation of genomic DNA from Mammalian tissue. Curr. Protoc. Mol. Biol. 42, 1–3 (1998).

    Article 

    Google Scholar 

  • 94.

    Ishibashi, Y. et al. Polymorphic microsatellite DNA markers in the field vole Microtus montebelli. Mol. Ecol. 8, 163–164 (1999).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 95.

    Gauffre, B., Galan, M., Bretagnolle, V. & Cosson, J. Polymorphic microsatellite loci and PCR multiplexing in the common vole, Microtus arvalis. Mol. Ecol. Notes 7, 830–832 (2007).

    CAS 
    Article 

    Google Scholar 

  • 96.

    Johnson, P. C. D. & Haydon, D. T. Software for quantifying and simulating microsatellite genotyping error. Bioinform. Biol. Insights 1, 71–75 (2009).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 97.

    Paradis, E. pegas: an R package for population genetics with an integrated–modular approach. Bioinformatics 26, 419–420 (2010).

    CAS 
    Article 

    Google Scholar 

  • 98.

    Brookfield, J. F. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5, 453–455 (1996).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 99.

    Adamack, A. T. & Gruber, B. PopGenReport: simplifying basic population genetic analyses in R. Methods Ecol. Evol. 5, 384–387 (2014).

    Article 

    Google Scholar 

  • 100.

    Jones, O. R. & Wang, J. COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol. Ecol. Resour. 10, 551–555 (2010).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 101.

    Keenan, K., McGinnity, P., Cross, T. F., Crozier, W. W. & Prodöhl, P. A. diveRsity: An R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol. Evol. 4, 782–788 (2013).

    Article 

    Google Scholar 

  • 102.

    Coulon, A. genhet: an easy-to-use R function to estimate individual heterozygosity. Mol. Ecol. Resour. 10, 167–169 (2010).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 103.

    Coltman, D. W., Pilkington, J. G. & Pemberton, J. M. Fine-scale genetic structure in a free-living ungulate population. Mol. Ecol. 12, 733–742 (2003).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 104.

    Amos, W. et al. The influence of parental relatedness on reproductive success. Proc. R. Soc. Lond. Ser. B Biol. Sci. 268, 2021–2027 (2001).

    CAS 
    Article 

    Google Scholar 

  • 105.

    Aparicio, J. M., Ortego, J. & Cordero, P. J. What should we weigh to estimate heterozygosity, alleles or loci? Estimating heterozygosity from neutral markers. Mol. Ecol. 15, 4659–4665 (2006).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 106.

    Kamvar, Z. N., Tabima, J. F. & Grünwald, N. J. Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ 2, e281 (2014).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 107.

    Peakall, R. & Smouse, P. E. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28, 2537–2539 (2012).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 108.

    Hedrick, P. W. A standardized genetic differentiation measure. Evolution 59, 1633–1638 (2005).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 109.

    Jost, L. GST and its relatives do not measure differentiation. Mol. Ecol. 17, 4015–4026 (2008).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 110.

    Meirmans, P. G. & Hedrick, P. W. Assessing population structure: FST and related measures. Mol. Ecol. Resour. 11, 5–18 (2011).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 111.

    Nei, M. Analysis of gene diversity in subdivided populations. PNAS 70, 3321–3323 (1973).

    ADS 
    CAS 
    PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 

  • 112.

    Nei, M. & Chesser, R. K. Estimation of fixation indices and gene diversities. Ann. Hum. Genet. 47, 253–259 (1983).

    CAS 
    PubMed 
    MATH 
    Article 
    PubMed Central 

    Google Scholar 

  • 113.

    Bowcock, A. M. et al. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368, 455–457 (1994).

    ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 114.

    Takezaki, N. & Nei, M. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144, 389–399 (1996).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 115.

    Smouse, P. E. & Peakall, R. Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82, 561–573 (1999).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 116.

    Queller, D. C. & Goodnight, K. F. Estimating relatedness using genetic markers. Evolution 43, 258–275 (1989).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 117.

    Ritland, K. Estimators for pairwise relatedness and individual inbreeding coefficients. Genet. Res. 67, 175–185 (1996).

    Article 

    Google Scholar 

  • 118.

    Lynch, M. & Ritland, K. Estimation of pairwise relatedness with molecular markers. Genetics 152, 1753–1766 (1999).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • 119.

    Jombart, T. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24, 1403–1405 (2008).

    CAS 
    Article 

    Google Scholar 

  • 120.

    Legendre, P. Spatial autocorrelation: Trouble or new paradigm?. Ecology 74, 1659–1673 (1993).

    Article 

    Google Scholar 

  • 121.

    Zuur, A., Ieno, E. N. & Smith, G. M. Analyzing Ecological Data (Springer, Berlin, 2007).

    MATH 
    Book 

    Google Scholar 

  • 122.

    Hedges, L. V. & Olkin, I. Statistical Methods for Meta-Analysis (Academic Press, 2014).

    MATH 

    Google Scholar 

  • 123.

    Kirby, K. N. & Gerlanc, D. BootES: an R package for bootstrap confidence intervals on effect sizes. Behav. Res. Methods 45, 905–927 (2013).

    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 124.

    Cohen, J. A power primer. Psychol. Bull. 112, 155–159 (1992).

    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 

  • 125.

    Cohen, J. Statistical Power Analysis for the Behavioral Sciences (Academic Press, 2013).

    MATH 
    Book 

    Google Scholar 

  • 126.

    González-Esteban, J. & Villate I. Microtus arvalis Pallas, 1778. In: Atlas y Libro Rojo de los Mamíferos Terrestres de España, Palomo, L.J., Gisbert, J. & Blanco J.C. (Eds.), Dirección General para la Biodiversidad-SECEM-SECEMU, 426-428 (2007).


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