[en] Historical factors (colonization scenarios, demographic oscillations) and contemporary processes (population connectivity, current population size) largely contribute to shaping species’ present-day genetic diversity and structure. In this study, we use a combination of mitochondrial and nuclear DNA markers to understand the role of Quaternary climatic oscillations and present-day gene flow dynamics in determining the genetic diversity and structure of the newt Calotriton asper (Al. Dugès, 1852), endemic to the Pyrenees. Mitochondrial DNA did not show a clear phylogeographic pattern and presented low levels of variation. In contrast, microsatellites revealed five major genetic lineages with admixture patterns at their boundaries. Approximate Bayesian computation analyses and linear models indicated that the five lineages likely underwent separate evolutionary histories and can be tracked back to distinct glacial refugia. Lineage differentiation started around the Last Glacial Maximum at three focal areas (western, central and eastern Pyrenees) and extended through the end of the Last Glacial Period in the central Pyrenees, where it led to the formation of two more lineages. Our data revealed no evidence of recent dispersal between lineages, whereas borders likely represent zones of secondary contact following expansion from multiple refugia. Finally, we did not find genetic evidence of sex-biased dispersal. This work highlights the importance of integrating past evolutionary processes and present-day gene flow and dispersal dynamics, together with multilocus approaches, to gain insights into what shaped the current genetic attributes of amphibians living in montane habitats.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Disciplines :
Life sciences: Multidisciplinary, general & others Zoology
Author, co-author :
Lucati, Federica; University of Lisbon
Poignet, Manon
Miró, Alexandre
Trochet, Audrey
Aubret, Fabien
Barthe, Laurent
Bertrand, Romain
Buchaca, Teresa
Calvez, Olivier
Caner, Jenny
Darnet, Elodie
Denoël, Mathieu ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Laboratoire d'Écologie et de Conservation des Amphibiens
Guillaume, Olivier
Le Chevalier, Hugo
Martínez-Silvestre, Albert
Mossoll-Torres, Marc
O’Brien, David
Osorio, Víctor
Pottier, Gilles
Richard, Murielle
Sabás, Ibor
Souchet, Jérémie
Tomàs, Jan
Ventura, Marc; Center for advanced Studies of Blanes (CSIC)
Abellán, P., & Svenning, J.-C. (2014). Refugia within refugia–patterns in endemism and genetic divergence are linked to Late Quaternary climate stability in the Iberian Peninsula. Biological Journal of the Linnean Society, 113(1), 13–28. https://doi.org/10.1111/bij.12309
Allentoft, M. E., Siegismund, H. R., Briggs, L., & Andersen, L. W. (2009). Microsatellite analysis of the natterjack toad (Bufo calamita) in Denmark: Populations are islands in a fragmented landscape. Conservation Genetics, 10(1), 15–28. https://doi.org/10.1007/s10592-008-9510-8
Alley, R. B., Mayewski, P. A., Sowers, T., Stuiver, M., Taylor, K. C., & Clark, P. U. (1997). Holocene climatic instability: A prominent, widespread event 8200 yr ago. Geology, 25(6), 483–486. https://doi.org/10.1130/0091-7613(1997)025<0483:HCIAPW>2.3.CO;2
Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge, MA: Harvard University Press.
Bazin, E., Glémin, S., & Galtier, N. (2006). Population size does not influence mitochondrial genetic diversity in animals. Science, 312(5773), 570–572. https://doi.org/10.1126/science.1122033
Bensch, S., Irwin, D. E., Irwin, J. H., Kvist, L., & Åkesson, S. (2006). Conflicting patterns of mitochondrial and nuclear DNA diversity in Phylloscopus warblers. Molecular Ecology, 15(1), 161–171. https://doi.org/10.1111/j.1365-294X.2005.02766.x
Bidegaray-Batista, L., Sánchez-Gracia, A., Santulli, G., Maiorano, L., Guisan, A., Vogler, A. P., & Arnedo, M. A. (2016). Imprints of multiple glacial refugia in the Pyrenees revealed by phylogeography and palaeodistribution modelling of an endemic spider. Molecular Ecology, 25(9), 2046–2064. https://doi.org/10.1111/mec.13585
Bosch, J., Tejedo, M., Lecis, R., Miaud, C., Lizana, M., Edgar, P., …Marquez, R. G. P. (2009). Calotriton asper. The IUCN Red List of Threatened Species, 2009, e.T59448A11943040. https://doi.org/10.2305/IUCN.UK.2009.RLTS.T59448A11943040.en
Burns, E. L., Eldridge, M. D., & Houlden, B. A. (2004). Microsatellite variation and population structure in a declining Australian Hylid Litoria aurea. Molecular Ecology, 13(7), 1745–1757. https://doi.org/10.1111/j.1365-294X.2004.02190.x
Cabrera, A. A., & Palsbøll, P. J. (2017). Inferring past demographic changes from contemporary genetic data: A simulation-based evaluation of the ABC methods implemented in DIYABC. Molecular Ecology Resources, 17(6), e94–e110. https://doi.org/10.1111/1755-0998.12696
Calvet, M. (2004). The Quaternary glaciation of the Pyrenees. Developments in Quaternary Sciences, 2, 119–128. https://doi.org/10.1016/S1571-0866(04)80062-9
Caplat, P., Edelaar, P., Dudaniec, R. Y., Green, A. J., Okamura, B., Cote, J., … Petit, E. J. (2016). Looking beyond the mountain: Dispersal barriers in a changing world. Frontiers in Ecology and the Environment, 14(5), 262–269. https://doi.org/10.1002/fee.1280
Carranza, S., & Amat, F. (2005). Taxonomy, biogeography and evolution of Euproctus (Amphibia: Salamandridae), with the resurrection of the genus Calotriton and the description of a new endemic species from the Iberian Peninsula. Zoological Journal of the Linnean Society, 145(4), 555–582. https://doi.org/10.1111/j.1096-3642.2005.00197.x
Carranza, S., Arnold, E., Mateo, J. A., & López-Jurado, L. F. (2000). Long-distance colonization and radiation in gekkonid lizards, Tarentola (Reptilia: Gekkonidae), revealed by mitochondrial DNA sequences. Proceedings of the Royal Society of London. Series B: Biological Sciences, 267(1444), 637–649. https://doi.org/10.1098/rspb.2000.1050
Cayuela, H., Valenzuela-Sánchez, A., Teulier, L., Martínez-Solano, Í., Léna, J.-P., Merilä, J., … Schmidt, B. R. (2020). Determinants and consequences of dispersal in vertebrates with complex life cycles: A review of pond-breeding amphibians. The Quarterly Review of Biology, 95(1), 1–36. https://doi.org/10.1086/707862
Chan, L. M., & Zamudio, K. R. (2009). Population differentiation of temperate amphibians in unpredictable environments. Molecular Ecology, 18(15), 3185–3200. https://doi.org/10.1111/j.1365-294X.2009.04273.x
Chapuis, M.-P., & Estoup, A. (2006). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24(3), 621–631. https://doi.org/10.1093/molbev/msl191
Charrier, O., Dupont, P., Pornon, A., & Escaravage, N. (2014). Microsatellite marker analysis reveals the complex phylogeographic history of Rhododendron ferrugineum (Ericaceae) in the Pyrenees. PLoS One, 9(3), e92976. https://doi.org/10.1371/journal.pone.0092976
Chiucchi, J. E., & Gibbs, H. (2010). Similarity of contemporary and historical gene flow among highly fragmented populations of an endangered rattlesnake. Molecular Ecology, 19(24), 5345–5358. https://doi.org/10.1111/j.1365-294X.2010.04860.x
Clergue-Gazeau, M., & Martínez-Rica, J. (1978). Les différents biotopes de l’urodèle pyrénéen, Euproctus asper. Bulletin De La Société D'histoire Naturelle De Toulouse, 114(3–4), 461–471.
Clobert, J., Le Galliard, J. F., Cote, J., Meylan, S., & Massot, M. (2009). Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecology Letters, 12(3), 197–209. https://doi.org/10.1111/j.1461-0248.2008.01267.x
Cornuet, J.-M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M., Leblois, R., … Estoup, A. (2014). DIYABC v2. 0: A software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics, 30(8), 1187–1189. https://doi.org/10.1093/bioinformatics/btt763
Darriba, D., Taboada, G. L., Doallo, R., & Posada, D. (2012). jmodeltest 2: More models, new heuristics and parallel computing. Nature Methods, 9(8), 772. https://doi.org/10.1038/nmeth.2109
Denoël, M., Dalleur, S., Langrand, E., Besnard, A., & Cayuela, H. (2018). Dispersal and alternative breeding site fidelity strategies in an amphibian. Ecography, 41(9), 1543–1555. https://doi.org/10.1111/ecog.03296
Dray, S., & Dufour, A.-B. (2007). The ade4 package: Implementing the duality diagram for ecologists. Journal of Statistical Software, 22(4), 1–20. https://doi.org/10.18637/jss.v022.i04
Drechsler, A., Geller, D., Freund, K., Schmeller, D. S., Kuenzel, S., Rupp, O., … Steinfartz, S. (2013). What remains from a 454 run: Estimation of success rates of microsatellite loci development in selected newt species (Calotriton asper, Lissotriton helveticus, and Triturus cristatus) and comparison with Illumina-based approaches. Ecology and Evolution, 3(11), 3947–3957. https://doi.org/10.1002/ece3.764
Epps, C. W., & Keyghobadi, N. (2015). Landscape genetics in a changing world: Disentangling historical and contemporary influences and inferring change. Molecular Ecology, 24(24), 6021–6040. https://doi.org/10.1111/mec.13454
Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14(8), 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x
Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics, 131(2), 479–491.
Favre, L., Balloux, F., Goudet, J., & Perrin, N. (1997). Female-biased dispersal in the monogamous mammal Crocidura russula: Evidence from field data and microsatellite patterns. Proceedings of the Royal Society of London. Series B: Biological Sciences, 264(1378), 127–132. https://doi.org/10.1098/rspb.1997.0019
Felsenstein, J. (2005). phylip (phylogeny inference package) version 3.6. Distributed by the author. Seattle, WA: Department of Genome Sciences, University of Washington.
Ferchaud, A. L., Eudeline, R., Arnal, V., Cheylan, M., Pottier, G., Leblois, R., & Crochet, P. A. (2015). Congruent signals of population history but radically different patterns of genetic diversity between mitochondrial and nuclear markers in a mountain lizard. Molecular Ecology, 24(1), 192–207. https://doi.org/10.1111/mec.13011
Francis, R. M. (2017). pophelper: An r package and web app to analyse and visualize population structure. Molecular Ecology Resources, 17(1), 27–32. https://doi.org/10.1111/1755-0998.12509
García-Ruiz, J. M., Valero-Garcés, B. L., Martí-Bono, C., & González-Sampériz, P. (2003). Asynchroneity of maximum glacier advances in the central Spanish Pyrenees. Journal of Quaternary Science, 18(1), 61–72. https://doi.org/10.1002/jqs.715
Gill, D. E. (1978). The metapopulation ecology of the red-spotted newt, Notophthalmus viridescens (Rafinesque). Ecological Monographs, 48(2), 145–166. https://doi.org/10.2307/2937297
Gómez, A., & Lunt, D. H. (2007). Refugia within refugia: Patterns of phylogeographic concordance in the Iberian Peninsula. In S. Weiss, & N. Ferrand (Eds.), Phylogeography of southern European refugia (pp. 155–188). Amsterdam, The Netherlands: Springer.
González-Sampériz, P., Valero-Garcés, B. L., Moreno, A., Jalut, G., García-Ruiz, J. M., Martí-Bono, C., … Dedoubat, J. J. (2006). Climate variability in the Spanish Pyrenees during the last 30,000 yr revealed by the El Portalet sequence. Quaternary Research, 66(1), 38–52. https://doi.org/10.1016/j.yqres.2006.02.004
Goudet, J. (2002). fstat version 2.9. 3.2, a program to estimate and test gene diversities and fixation indices. Lausanne, Switzerland: Institute of Ecology http://www2.unil.ch/popgen/softwares/fstat.htm
Goudet, J., & Jombart, T. (2015). hierfstat: Estimation and tests of hierarchical F-statistics. R package version 0.04-22.
Goudet, J., Perrin, N., & Waser, P. (2002). Tests for sex-biased dispersal using bi-parentally inherited genetic markers. Molecular Ecology, 11(6), 1103–1114. https://doi.org/10.1046/j.1365-294X.2002.01496.x
Grant, E. H. C., Nichols, J. D., Lowe, W. H., & Fagan, W. F. (2010). Use of multiple dispersal pathways facilitates amphibian persistence in stream networks. Proceedings of the National Academy of Sciences, 107(15), 6936–6940. https://doi.org/10.1073/pnas.1000266107
Helfer, V., Broquet, T., & Fumagalli, L. (2012). Sex-specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian, the alpine salamander (Salamandra atra). Molecular Ecology, 21(19), 4706–4720. https://doi.org/10.1111/j.1365-294X.2012.05742.x
Hewitt, G. M. (1999). Post-glacial re-colonization of European biota. Biological Journal of the Linnean Society, 68(1–2), 87–112. https://doi.org/10.1006/bijl.1999.0332
Hewitt, G. M. (2000). The genetic legacy of the Quaternary ice ages. Nature, 405(6789), 907–913. https://doi.org/10.1038/35016000
Hewitt, G. M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 359(1442), 183–195; discussion 195. https://doi.org/10.1098/rstb.2003.1388
Hewitt, G. M., & Butlin, R. K. (1997). Causes and consequences of population structure. In J. R. Krebs, & N. Davies (Eds.), Behavioral ecology, 4th ed. (pp. 350–372). Oxford, UK: Blackwell.
Holderegger, R., & Thiel-Egenter, C. (2009). A discussion of different types of glacial refugia used in mountain biogeography and phylogeography. Journal of Biogeography, 36(3), 476–480. https://doi.org/10.1111/j.1365-2699.2008.02027.x
Jakobsson, M., & Rosenberg, N. A. (2007). clumpp: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics, 23(14), 1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Johnson, M. L., & Gaines, M. S. (1990). Evolution of dispersal: Theoretical models and empirical tests using birds and mammals. Annual Review of Ecology and Systematics, 21(1), 449–480. https://doi.org/10.1146/annurev.es.21.110190.002313
Jones, O. R., & Wang, J. (2010). COLONY: A program for parentage and sibship inference from multilocus genotype data. Molecular Ecology Resources, 10(3), 551–555. https://doi.org/10.1111/j.1755-0998.2009.02787.x
Kalinowski, S. T. (2005). hp-rare 1.0: A computer program for performing rarefaction on measures of allelic richness. Molecular Ecology Notes, 5(1), 187–189. https://doi.org/10.1111/j.1471-8286.2004.00845.x
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., … Drummond, A. (2012). geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kraaijeveld-Smit, F. J., Beebee, T. J., Griffiths, R. A., Moore, R. D., & Schley, L. (2005). Low gene flow but high genetic diversity in the threatened Mallorcan midwife toad Alytes muletensis. Molecular Ecology, 14(11), 3307–3315. https://doi.org/10.1111/j.1365-294X.2005.02614.x
Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7), 1870–1874. https://doi.org/10.1093/molbev/msw054
Li, X. Y., & Kokko, H. (2019). Sex-biased dispersal: A review of the theory. Biological Reviews, 94(2), 721–736. https://doi.org/10.1111/brv.12475
Liberal, I. M., Burrus, M., Suchet, C., Thebaud, C., & Vargas, P. (2014). The evolutionary history of Antirrhinum in the Pyrenees inferred from phylogeographic analyses. BMC Evolutionary Biology, 14(1), 146. https://doi.org/10.1186/1471-2148-14-146
Lucati, F., Poignet, M., Miró, A., Trochet, A., Aubret, F., Barthe, L., … Ventura, M. (2020). Data from: Multiple glacial refugia and contemporary dispersal shape the genetic structure of an endemic amphibian from the Pyrenees. Dryad Digital Repository, https://doi.org/10.5061/dryad.5tb2rbp23
Magri, D., Vendramin, G. G., Comps, B., Dupanloup, I., Geburek, T., Gomory, D., … de Beaulieu, J.-L. (2006). A new scenario for the Quaternary history of European beech populations: Palaeobotanical evidence and genetic consequences. New Phytologist, 171(1), 199–221. https://doi.org/10.1111/j.1469-8137.2006.01740.x
Mantel, N., & Valand, R. S. (1970). A technique of nonparametric multivariate analysis. Biometrics, 26(3), 547–558. https://doi.org/10.2307/2529108
Martínez-Rica, J., & Clergue-Gazeau, M. (1977). Données nouvelles sur la répartition géographique de l’espèce Euproctus asper Dugès, Urodèle, Salamandridae. Bulletin De La Société D’histoire Naturelle De Tolouse, 113(3–4), 318–330.
Milá, B., Carranza, S., Guillaume, O., & Clobert, J. (2010). Marked genetic structuring and extreme dispersal limitation in the Pyrenean brook newt Calotriton asper (Amphibia: Salamandridae) revealed by genome-wide AFLP but not mtDNA. Molecular Ecology, 19(1), 108–120. https://doi.org/10.1111/j.1365-294X.2009.04441.x
Montero-Pau, J., Gómez, A., & Muñoz, J. (2008). Application of an inexpensive and high-throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography: Methods, 6(6), 218–222. https://doi.org/10.4319/lom.2008.6.218
Montori, A., & Llorente, G. A. (2014). Tritón pirenaico–Calotriton asper (Dugès, 1852). In A. Salvador, & I. Martínez-Solano (Eds.), Enciclopedia Virtual de los Vertebrados (pp. 28). Madrid, Spain: Museo Nacional de Ciencias Naturales.
Montori, A., Llorente, G. A., & García-París, M. (2008). Allozyme differentiation among populations of the Pyrenean newt Calotriton asper (Amphibia: Caudata) does not mirror their morphological diversification. Zootaxa, 1945, 39–50. https://doi.org/10.11646/zootaxa.1945.1.2
Montori, A., Llorente, G. A., & Richter-Boix, A. (2008). Habitat features affecting the small-scale distribution and longitudinal migration patterns of Calotriton asper in a Pre-Pyrenean population. Amphibia-Reptilia, 29(3), 371–381. https://doi.org/10.1163/156853808785112048
Montori, A., Richter-Boix, A., Franch, M., Santos, X., Garriga, N., & Llorente, G. A. (2012). Natural fluctuations in a stream dwelling newt as a result of extreme rainfall: A 21-year survey of a Calotriton asper population. Basic and Applied Herpetology, 26, 43–56. https://doi.org/10.11160/bah.12001
Mouret, V., Guillaumet, A., Cheylan, M., Pottier, G., Ferchaud, A. L., & Crochet, P. A. (2011). The legacy of ice ages in mountain species: Post-glacial colonization of mountain tops rather than current range fragmentation determines mitochondrial genetic diversity in an endemic Pyrenean rock lizard. Journal of Biogeography, 38(9), 1717–1731. https://doi.org/10.1111/j.1365-2699.2011.02514.x
Nei, M., Tajima, F., & Tateno, Y. (1983). Accuracy of estimated phylogenetic trees from molecular data. Journal of Molecular Evolution, 19(2), 153–170. https://doi.org/10.1007/bf02300753
Nichols, R. A., & Beaumont, M. A. (1996). Is it ancient or modern history that we can read in the genes? In M. E. Hochberg, J. Clobert, & R. Barbault (Eds.), Aspects of the Genesis and Maintenance of Biological Diversity (pp. 69–87). Oxford, UK: Oxford University Press.
Noguerales, V., Cordero, P. J., & Ortego, J. (2016). Hierarchical genetic structure shaped by topography in a narrow-endemic montane grasshopper. BMC Evolutionary Biology, 16(1), 96. https://doi.org/10.1186/s12862-016-0663-7
Noguerales, V., Cordero, P. J., & Ortego, J. (2017). Testing the role of ancient and contemporary landscapes on structuring genetic variation in a specialist grasshopper. Ecology and Evolution, 7(9), 3110–3122. https://doi.org/10.1002/ece3.2810
Oromi, N., Valbuena-Ureña, E., Soler-Membrives, A., Amat, F., Camarasa, S., Carranza, S., … Denoël, M. (2018). Genetic structure of lake and stream populations in a Pyrenean amphibian (Calotriton asper) reveals evolutionary significant units associated with paedomorphosis. Journal of Zoological Systematics and Evolutionary Research, 57, 418–430. https://doi.org/10.1111/jzs.12250
Orsini, L., Vanoverbeke, J., Swillen, I., Mergeay, J., & De Meester, L. (2013). Drivers of population genetic differentiation in the wild: Isolation by dispersal limitation, isolation by adaptation and isolation by colonization. Molecular Ecology, 22(24), 5983–5999. https://doi.org/10.1111/mec.12561
Ortego, J., Noguerales, V., Gugger, P. F., & Sork, V. L. (2015). Evolutionary and demographic history of the Californian scrub white oak species complex: An integrative approach. Molecular Ecology, 24(24), 6188–6208. https://doi.org/10.1111/mec.13457
Paetkau, D., Slade, R., Burden, M., & Estoup, A. (2004). Genetic assignment methods for the direct, real-time estimation of migration rate: A simulation-based exploration of accuracy and power. Molecular Ecology, 13(1), 55–65. https://doi.org/10.1046/j.1365-294X.2004.02008.x
Piry, S., Alapetite, A., Cornuet, J. M., Paetkau, D., Baudouin, L., & Estoup, A. (2004). GENECLASS2: A software for genetic assignment and first-generation migrant detection. Journal of Heredity, 95(6), 536–539. https://doi.org/10.1093/jhered/esh074
Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155(2), 945–959.
Pritchard, J. K., Wen, X., & Falush, D. (2010). Documentation for structure software, version 2.3. Oxford, UK: Department of Human Genetics. University of Chicago, Department of Statistics University of Oxford.
Prugnolle, F., & De Meeus, T. (2002). Inferring sex-biased dispersal from population genetic tools: A review. Heredity, 88(3), 161–165. https://doi.org/10.1038/sj.hdy.6800060
R Core Team. (2018). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/
Rato, C., Carranza, S., Perera, A., Carretero, M. A., & Harris, D. J. (2010). Conflicting patterns of nucleotide diversity between mtDNA and nDNA in the Moorish gecko, Tarentola mauritanica. Molecular Phylogenetics and Evolution, 56(3), 962–971. https://doi.org/10.1016/j.ympev.2010.04.033
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution, 43(1), 223–225. https://doi.org/10.1111/j.1558-5646.1989.tb04220.x
Rioux Paquette, S. (2011). popgenkit: Useful functions for (batch) file conversion and data resampling in microsatellite datasets. R Package Version, 1.0.
Roffler, G. H., Talbot, S. L., Luikart, G., Sage, G. K., Pilgrim, K. L., Adams, L. G., & Schwartz, M. K. (2014). Lack of sex-biased dispersal promotes fine-scale genetic structure in alpine ungulates. Conservation Genetics, 15(4), 837–851. https://doi.org/10.1007/s10592-014-0583-2
Ronce, O. (2007). How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annual Review of Ecology, Evolution, and Systematics, 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(4), 1219–1228.
Rousset, F. (2008). genepop’007: A complete re-implementation of the genepop software for Windows and Linux. Molecular Ecology Resources, 8(1), 103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x
Rozas, J., Ferrer-Mata, A., Sánchez-DelBarrio, J. C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S. E., & Sánchez-Gracia, A. (2017). DnaSP 6: DNA sequence polymorphism analysis of large data sets. Molecular Biology and Evolution, 34(12), 3299–3302. https://doi.org/10.1093/molbev/msx248
Saccheri, I., Kuussaari, M., Kankare, M., Vikman, P., Fortelius, W., & Hanski, I. (1998). Inbreeding and extinction in a butterfly metapopulation. Nature, 392(6675), 491–494. https://doi.org/10.1038/33136
Salzburger, W., Ewing, G. B., & Von Haeseler, A. (2011). The performance of phylogenetic algorithms in estimating haplotype genealogies with migration. Molecular Ecology, 20(9), 1952–1963. https://doi.org/10.1111/j.1365-294X.2011.05066.x
Saura, S., Bodin, Ö., & Fortin, M. J. (2014). Stepping stones are crucial for species' long-distance dispersal and range expansion through habitat networks. Journal of Applied Ecology, 51(1), 171–182. https://doi.org/10.1111/1365-2664.12179
Schmitt, T. (2009). Biogeographical and evolutionary importance of the European high mountain systems. Frontiers in Zoology, 6, 9. https://doi.org/10.1186/1742-9994-6-9
Schmitt, T., Hewitt, G. M., & Muller, P. (2006). Disjunct distributions during glacial and interglacial periods in mountain butterflies: Erebia epiphron as an example. Journal of Evolutionary Biology, 19(1), 108–113. https://doi.org/10.1111/j.1420-9101.2005.00980.x
Smith, M. A., & Green, D. M. (2005). Dispersal and the metapopulation paradigm in amphibian ecology and conservation: Are all amphibian populations metapopulations? Ecography, 28(1), 110–128. https://doi.org/10.1111/j.0906-7590.2005.04042.x
Smith, M. A., & Green, D. M. (2006). Sex, isolation and fidelity: Unbiased long-distance dispersal in a terrestrial amphibian. Ecography, 29(5), 649–658. https://doi.org/10.1111/j.2006.0906-7590.04584.x
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690. https://doi.org/10.1093/bioinformatics/btl446
Taberlet, P., Fumagalli, L., Wust-Saucy, A. G., & Cosson, J. F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology, 7(4), 453–464. https://doi.org/10.1046/j.1365-294x.1998.00289.x
Takezaki, N., Nei, M., & Tamura, K. (2014). poptreew: Web version of POPTREE for constructing population trees from allele frequency data and computing some other quantities. Molecular Biology and Evolution, 31(6), 1622–1624. https://doi.org/10.1093/molbev/msu093
Tallmon, D. A., Luikart, G., & Waples, R. S. (2004). The alluring simplicity and complex reality of genetic rescue. Trends in Ecology & Evolution, 19(9), 489–496. https://doi.org/10.1016/j.tree.2004.07.003
Trochet, A., Courtois, E. A., Stevens, V. M., Baguette, M., Chaine, A., Schmeller, D. S., … Wiens, J. J. (2016). Evolution of sex-biased dispersal. The Quarterly Review of Biology, 91(3), 297–320. https://doi.org/10.1086/688097
Tucker, J. M., Allendorf, F. W., Truex, R. L., & Schwartz, M. K. (2017). Sex-biased dispersal and spatial heterogeneity affect landscape resistance to gene flow in fisher. Ecosphere, 8(6), e01839. https://doi.org/10.1002/ecs2.1839
Valbuena-Ureña, E., Amat, F., & Carranza, S. (2013). Integrative phylogeography of Calotriton newts (Amphibia, Salamandridae), with special remarks on the conservation of the endangered Montseny brook newt (Calotriton arnoldi). PLoS One, 8(6), e62542. https://doi.org/10.1371/journal.pone.0062542
Valbuena-Ureña, E., Oromi, N., Soler-Membrives, A., Carranza, S., Amat, F., Camarasa, S., … Steinfartz, S. (2018). Jailed in the mountains: Genetic diversity and structure of an endemic newt species across the Pyrenees. PLoS One, 13(8), e0200214. https://doi.org/10.1371/journal.pone.0200214
Van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., & Shipley, P. (2004). micro-checker: Software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4(3), 535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x
Ventura, M., Petrusek, A., Miró, A., Hamrová, E., Buñay, D., De Meester, L., & Mergeay, J. (2014). Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential. Molecular Ecology, 23, 1014–1027. https://doi.org/10.1111/mec.12656
Vos, C. C., Antonisse-De Jong, A. G., Goedhart, P. W., & Smulders, M. J. M. (2001). Genetic similarity as a measure for connectivity between fragmented populations of the moor frog (Rana arvalis). Heredity, 86, 598–608. https://doi.org/10.1046/j.1365-2540.2001.00865.x
Wallis, G. P., Waters, J. M., Upton, P., & Craw, D. (2016). Transverse alpine speciation driven by glaciation. Trends in Ecology & Evolution, 31(12), 916–926. https://doi.org/10.1016/j.tree.2016.08.009
Werth, S., Gugerli, F., Holderegger, R., Wagner, H. H., Csencsics, D., & Scheidegger, C. (2007). Landscape-level gene flow in Lobaria pulmonaria, an epiphytic lichen. Molecular Ecology, 16(13), 2807–2815. https://doi.org/10.1111/j.1365-294X.2007.03344.x
Zellmer, A., & Knowles, L. L. (2009). Disentangling the effects of historic vs. contemporary landscape structure on population genetic divergence. Molecular Ecology, 18(17), 3593–3602. https://doi.org/10.1111/j.1365-294X.2009.04305.x
