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Genomic insights into the origin of trans‐Mediterranean disjunct distributions

dc.contributor.authorNoguerales, Víctor
dc.contributor.authorCordero, Pedro J.
dc.contributor.authorKnowles, L. Lacey
dc.contributor.authorOrtego, Joaquín
dc.date.accessioned2021-03-02T21:46:54Z
dc.date.available2022-03-02 16:46:53en
dc.date.available2021-03-02T21:46:54Z
dc.date.issued2021-02
dc.identifier.citationNoguerales, Víctor ; Cordero, Pedro J.; Knowles, L. Lacey; Ortego, Joaquín (2021). "Genomic insights into the origin of trans‐Mediterranean disjunct distributions." Journal of Biogeography (2): 440-452.
dc.identifier.issn0305-0270
dc.identifier.issn1365-2699
dc.identifier.urihttps://hdl.handle.net/2027.42/166420
dc.description.abstractAimTwo main biogeographical hypotheses have been proposed to explain the Mediterranean‐Turanian disjunct distributions exhibited by numerous steppe‐dwelling organisms, namely (a) dispersal during the Messinian salinity crisis (∼5.96–5.33 Ma) followed by range fragmentation and vicariance, and (b) Pleistocene colonization and recent processes of population subdivision (<2 Ma). Despite the two hypotheses postulate the role of climatic alterations and changes in landmass configuration on determining such disjunct distributions, estimates of the timing of lineage diversification have not been complemented so far with spatially‐explicit tests providing independent evidence on the proximate processes underlying geographical patterns of population genetic connectivity/fragmentation.LocationMediterranean‐Turanian region.TaxonSaltmarsh band‐winged grasshopper (Mioscirtus wagneri).MethodsWe integrate different sources of genetic (mtDNA and ddRADseq) and spatial information (configuration of emerged lands and niche modelling) to evaluate competing hypotheses of lineage diversification in the saltmarsh band‐winged grasshopper, a halophile species showing a classical Mediterranean‐Turanian disjunct distribution.ResultsPhylogenomic analyses reveal the presence of two North African cryptic lineages and support that trans‐Mediterranean populations of the species diverged in the Pleistocene, with evidence of post‐Messinian permeability of the Strait of Gibraltar to gene flow likely associated with sea level drops during glacial periods. Accordingly, spatial patterns of genetic differentiation are best explained by a scenario of population connectivity defined by the configuration of emerged landmasses and environmentally suitable habitats during glacial periods, a time when effective population sizes of the species peaked as inferred by genomic‐based demographic reconstructions.Main conclusionsOur results support post‐Messinian colonization and Pleistocene diversification as the biogeographical scenario best explaining the trans‐Mediterranean disjunct distributions of halophilous organisms.
dc.publisherWiley Periodicals, Inc.
dc.publisherOxford University Press
dc.subject.otherbiogeographical scenarios
dc.subject.otherddRADseq
dc.subject.otherdisjunct distributions
dc.subject.otherMessinian
dc.subject.otherphylogenomics
dc.subject.otherbathymetry
dc.subject.otherPleistocene
dc.titleGenomic insights into the origin of trans‐Mediterranean disjunct distributions
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelGeography and Maps
dc.subject.hlbtoplevelSocial Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/166420/1/jbi14011.pdf
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/166420/2/jbi14011_am.pdf
dc.identifier.doi10.1111/jbi.14011
dc.identifier.sourceJournal of Biogeography
dc.identifier.citedreferenceOrtego, J., Aguirre, M. P., & Cordero, P. J. ( 2010 ). Population genetics of Mioscirtus wagneri, a grasshopper showing a highly fragmented distribution. Molecular Ecology, 19, 472 – 483. https://doi.org/10.1111/j.1365‐294X.2009.04512.x
dc.identifier.citedreferenceWang, I. J. ( 2010 ). Recognizing the temporal distinctions between landscape genetics and phylogeography. Molecular Ecology, 19, 2605 – 2608. https://doi.org/10.1111/j.1365‐294X.2010.04715.x
dc.identifier.citedreferenceLitcher, M., Zviely, D., Klein, M., & Sivan, D. ( 2010 ). Sea‐level changes in the Mediterranean: Past, present and future – a review. In A. Israel, R. Eina, & J. Seckbach (Eds.), Seaweeds and their role in globally changing environment. Cellular origin, life in extreme habitats and astrobiology (pp. 5 – 17 ). London, New York: Springer.
dc.identifier.citedreferenceLiu, X., & Fu, Y.‐X. ( 2015 ). Exploring population size changes using SNP frequency spectra. Nature Genetics, 47, 555 – 559. https://doi.org/10.1038/ng.3254
dc.identifier.citedreferenceLuján, M., Crespo‐Blanc, A., & Comas, M. ( 2011 ). Morphology and structure of the Camarinal Sill from high‐resolution bathymetry: Evidence of fault zones in the Gibraltar Strait. Geo‐Marine Letters, 31, 163 – 174. https://doi.org/10.1007/s00367‐010‐0222‐y
dc.identifier.citedreferenceMcRae, B. H. ( 2006 ). Isolation by resistance. Evolution, 60, 1551 – 1561. https://doi.org/10.1111/j.0014‐3820.2006.tb00500.x
dc.identifier.citedreferenceMcRae, B. H., & Beier, P. ( 2007 ). Circuit theory predicts gene flow in plant and animal populations. Proceedings of the National Academy of Sciences of the United States of America, 104, 19885 – 19890. https://doi.org/10.1073/pnas.0706568104
dc.identifier.citedreferenceNaskrecki, P., & Ünal, M. ( 1995 ). The Orthoptera of Hatay Province. S. Turkey. Beiträge Zur Entomologie, 45, 393 – 419.
dc.identifier.citedreferenceNoguerales, V., Cordero, P. J., & Ortego, J. ( 2018 ). Integrating genomic and phenotypic data to evaluate alternative phylogenetic and species delimitation hypotheses in a recent evolutionary radiation of grasshoppers. Molecular Ecology, 27, 1229 – 1244. https://doi.org/10.1111/mec.14504
dc.identifier.citedreferenceOrtego, J., Bonal, R., Cordero, P. J., & Aparicio, J. M. ( 2009 ). Phylogeography of the Iberian populations of Mioscirtus wagneri (Orthoptera: Acrididae), a specialized grasshopper inhabiting highly fragmented hypersaline environments. Biological Journal of the Linnean Society, 97, 623 – 633. https://doi.org/10.1111/j.1095‐8312.2009.01206.x
dc.identifier.citedreferenceOrtego, J., García‐Navas, V., Noguerales, V., & Cordero, P. J. ( 2015 ). Discordant patterns of genetic and phenotypic differentiation in five grasshopper species codistributed across a microreserve network. Molecular Ecology, 24, 5796 – 5812. https://doi.org/10.1111/mec.13426
dc.identifier.citedreferenceOrtiz, M. A., Tremetsberger, K., Talavera, S., Stuessy, T., & García‐Castaño, J. L. ( 2007 ). Population structure of Hypochaeris salzmanniana DC. (Asteraceae), an endemic species to the Atlantic coast on both sides of the Strait of Gibraltar, in relation to Quaternary sea level changes. Molecular Ecology, 16, 541 – 552. https://doi.org/10.1111/j.1365‐294X.2006.03157.x
dc.identifier.citedreferencePapadopoulou, A., Anastasiou, I., & Vogler, A. P. ( 2010 ). Revisiting the insect mitochondrial molecular clock: The Mid‐Aegean trench calibration. Molecular Biology and Evolution, 27, 1659 – 1672. https://doi.org/10.1093/molbev/msq051
dc.identifier.citedreferencePapadopoulou, A., & Knowles, L. L. ( 2015 ). Species‐specific responses to island connectivity cycles: Refined models for testing phylogeographic concordance across a Mediterranean Pleistocene Aggregate Island Complex. Molecular Ecology, 24, 4252 – 4268. https://doi.org/10.1111/mec.13305
dc.identifier.citedreferencePapadopoulou, A., & Knowles, L. L. ( 2017 ). Linking micro‐ and macroevolutionary perspectives to evaluate the role of Quaternary sea‐level oscillations in island diversification. Evolution, 71, 2901 – 2917. https://doi.org/10.1111/evo.13384
dc.identifier.citedreferencePérez‐Collazos, E., Sánchez‐Gómez, P., Jiménez, J. F., & Catalán, P. ( 2009 ). The phylogeographical history of the Iberian steppe plant Ferula loscosii (Apiaceae): A test of the abundant‐centre hypothesis. Molecular Ecology, 18, 848 – 861. https://doi.org/10.1111/j.1365‐294X.2008.04060.x
dc.identifier.citedreferencePeterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S., & Hoekstra, H. E. ( 2012 ). Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non‐model species. PLoS ONE One, 7, e37135. https://doi.org/10.1371/journal.pone.0037135
dc.identifier.citedreferenceRaj, A., Stephens, M., & Pritchard, J. K. ( 2014 ). faststructure: Variational inference of population structure in large SNP data sets. Genetics, 197, 573 – U207. https://doi.org/10.1534/genetics.114.164350
dc.identifier.citedreferenceRibera, I., & Blasco‐Zumeta, J. ( 1998 ). Biogeographical links between steppe insects in the Monegros region (Aragón, NE Spain), the eastern Mediterranean, and central Asia. Journal of Biogeography, 25, 969 – 986. https://doi.org/10.1046/j.1365‐2699.1998.00226.x
dc.identifier.citedreferenceRissler, L. J. ( 2016 ). Union of phylogeography and landscape genetics. Proceedings of the National Academy of Sciences of the United States of America, 113, 8079 – 8086. https://doi.org/10.1073/pnas.1601073113
dc.identifier.citedreferenceRohling, E. J., Hibbert, F. D., Williams, F. H., Grant, K. M., Marino, G., Foster, G. L., Hennekam, R., de Lange, G. J., Roberts, A. P., Yu, J., Webster, J. M., & Yokoyama, Y. ( 2017 ). Differences between the last two glacial maxima and implications for ice‐sheet, δ 18 O, and sea‐level reconstructions. Quaternary Science Reviews, 176, 1 – 28. https://doi.org/10.1016/j.quascirev.2017.09.009
dc.identifier.citedreferenceRozas, 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, 3299 – 3302. https://doi.org/10.1093/molbev/msx248
dc.identifier.citedreferenceSánchez‐Goñi, M. F., Eynaud, F., Turon, J. L., & Shackleton, N. J. ( 1999 ). High resolution palynological record off the Iberia margin: Direct land‐sea correlation for the Last Interglacial complex. Earth and Planetary Science Letters, 171, 123 – 137. https://doi.org/10.1016/S0012‐821X(99)00141‐7
dc.identifier.citedreferenceSanmartín, I. ( 2003 ). Dispersal vs. vicariance in the Mediterranean: Historical biogeography of the Palearctic Pachydeminae (Coleoptera, Scarabaeoidea). Journal of Biogeography, 30, 1883 – 1897. https://doi.org/10.1046/j.0305‐0270.2003.00982.x
dc.identifier.citedreferenceToews, D. P. L., & Brelsford, A. ( 2012 ). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology, 21, 3907 – 3930. https://doi.org/10.1111/j.1365‐294X.2012.05664.x
dc.identifier.citedreferenceÜnal, M. ( 2011 ). Turkish Orthoptera Site (TOS). http://www.orthoptera-tr.org
dc.identifier.citedreferenceWang, I. J. ( 2013 ). Examining the full effects of landscape heterogeneity on spatial genetic variation: A multiple matrix regression approach for quantifying geographic and ecological isolation. Evolution, 67, 3403 – 3411. https://doi.org/10.1111/evo.12134
dc.identifier.citedreferenceWeising, K., & Freitag, H. ( 2007 ). Phylogeography of halophytes from European coastal and inland habitats. Zoologischer Anzeiger, 246, 279 – 292. https://doi.org/10.1016/j.jcz.2007.07.005
dc.identifier.citedreferenceAllegrucci, G., Trucchi, E., & Sbordoni, V. ( 2011 ). Tempo and mode of species diversification in Dolichopoda cave crickets (Orthoptera, Rhaphidophoridae). Molecular Phylogenetics and Evolution, 60, 108 – 121. https://doi.org/10.1016/j.ympev.2011.04.002
dc.identifier.citedreferenceAvise, J. C. ( 2009 ). Phylogeography: Retrospect and prospect. Journal of Biogeography, 36, 3 – 15. https://doi.org/10.1111/j.1365‐2699.2008.02032.x
dc.identifier.citedreferenceBaele, G., Lemey, P., & Suchard, M. A. ( 2016 ). Genealogical working distributions for Bayesian model testing with phylogenetic uncertainty. Systematic Biology, 65, 250 – 264. https://doi.org/10.1093/sysbio/syv083
dc.identifier.citedreferenceBates, D., Maechler, M., Bolker, B. M., & Walker, S. C. ( 2015 ). Fitting linear mixed‐effects models using lme4. Journal of Statistical Software, 67, 1 – 48. https://doi.org/10.18637/jss.v067.i01
dc.identifier.citedreferenceBeddek, M., Zenboudji‐Beddek, S., Geniez, P., Fathalla, R., Sourouille, P., Arnal, V., Dellaoui, B., Koudache, F., Telailia, S., Peyre, O., & Crochet, P.‐A. ( 2018 ). Comparative phylogeography of amphibians and reptiles in Algeria suggests common causes for the east‐west phylogeographic breaks in the Maghreb. PLoS One, 13, e0201218. https://doi.org/10.1371/journal.pone.0201218
dc.identifier.citedreferenceBlondel, J., & Aronson, J. ( 1999 ). Biology and wildlife of the Mediterranean region. Oxford: Oxford University Press.
dc.identifier.citedreferenceCapella, W., Barhoun, N., Flecker, R., Hilgen, F. J., Kouwenhoven, T., Matenco, L. C., Sierro, F. J., Tulbure, M. A., Yousfi, M. Z., & Krijgsman, W. ( 2018 ). Palaeogeographic evolution of the late Miocene Rifian Corridor (Morocco): Reconstructions from surface and subsurface data. Earth‐Science Reviews, 180, 37 – 59. https://doi.org/10.1016/j.earscirev.2018.02.017
dc.identifier.citedreferenceCarrión, J. S., Fernández, S., Fierro, E., López‐Merino, L., & Munuera, M. ( 2012 ). Paleoflora y paleovegetación de la Península Ibérica e Islas Baleares: Plioceno‐Cuaternario. Murcia, Spain: Ministerio de Economía y Competitividad.
dc.identifier.citedreferenceCatchen, J., Hohenlohe, P. A., Bassham, S., Amores, A., & Cresko, W. A. ( 2013 ). stacks: An analysis tool set for population genomics. Molecular Ecology, 22, 3124 – 3140. https://doi.org/10.1111/mec.12354
dc.identifier.citedreferenceChifman, J., & Kubatko, L. ( 2014 ). Quartet inference from SNP data under the coalescent model. Bioinformatics, 30, 3317 – 3324. https://doi.org/10.1093/bioinformatics/btu530
dc.identifier.citedreferenceChueca, L. J., Madeira, M. J., & Gómez‐Moliner, B. J. ( 2015 ). Biogeography of the land snail genus Allognathus (Helicidae): Middle Miocene colonization of the Balearic Islands. Journal of Biogeography, 42, 1845 – 1857. https://doi.org/10.1111/jbi.12549
dc.identifier.citedreferenceCigliano, M. M., Braun, H., Eades, D. C., & Otte, D. ( 2020 ). Orthoptera Species File (OSF). http://orthoptera.speciesfile.org (accessed 10 March 2020).
dc.identifier.citedreferenceCordero, P. J., Llorente, V., & Aparicio, J. M. ( 2007 ). New data on morphometrics, distribution and ecology of Mioscirtus wagneri (Kittary, 1859) (Orthoptera, Acrididae) in Spain: Is maghrebi a well defined subspecies? Graellsia, 63, 3 – 16.
dc.identifier.citedreferenceCosson, J. F., Hutterer, R., Libois, R., Sara, M., Taberlet, P., & Vogel, P. ( 2005 ). Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: A case study with the greater white‐toothed shrew, Crocidura russula (Mammalia: Soricidae). Molecular Ecology, 14, 1151 – 1162. https://doi.org/10.1111/j.1365‐294X.2005.02476.x
dc.identifier.citedreferenceDarriba, D., Taboada, G. L., Doallo, R., & Posada, D. ( 2012 ). jmodeltest 2: More models, new heuristics and parallel computing. Nature Methods, 9, 772. https://doi.org/10.1038/nmeth.2109
dc.identifier.citedreferenceDrummond, A. J., Suchard, M. A., Xie, D., & Rambaut, A. ( 2012 ). Bayesian phylogenetics with beauti and the beast 1.7. Molecular Biology and Evolution, 29, 1969 – 1973. https://doi.org/10.1093/molbev/mss075
dc.identifier.citedreferenceEaton, D. A. R. ( 2014 ). pyrad: Assembly of de novo RADseq loci for phylogenetic analyses. Bioinformatics, 30, 1844 – 1849. https://doi.org/10.1093/bioinformatics/btu121
dc.identifier.citedreferenceEscudero, M., Vargas, P., Arens, P., Ouborg, N. J., & Luceño, M. ( 2010 ). The east‐west‐north colonization history of the Mediterranean and Europe by the coastal plant Carex extensa (Cyperaceae). Molecular Ecology, 19, 352 – 370. https://doi.org/10.1111/j.1365‐294X.2009.04449.x
dc.identifier.citedreferenceExcoffier, L., & Lischer, H. E. L. ( 2010 ). arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564 – 567. https://doi.org/10.1111/j.1755‐0998.2010.02847.x
dc.identifier.citedreferenceFernandes, J. A. ( 1968 ). A new subspecies of Mioscirtus wagneri Evers. Arquivos do Museu Bocage, Segunda Série‐ Notas E Suplementos, 2, 1 – 3.
dc.identifier.citedreferenceFlouri, T., Jiao, X., Rannala, B., & Yang, Z. ( 2018 ). Species tree inference with bpp using genomic sequences and the multispecies coalescent. Molecular Biology and Evolution, 35, 2585 – 2593. https://doi.org/10.1093/molbev/msy147
dc.identifier.citedreferenceGarcía‐Alix, A., Minwer‐Barakat, R., Martín‐Suarez, E., Freudenthal, M., Aguirre, J., & Kaya, F. ( 2016 ). Updating the Europe‐Africa small mammal exchange during the late Messinian. Journal of Biogeography, 43, 1336 – 1348. https://doi.org/10.1111/jbi.12732
dc.identifier.citedreferenceGarcía‐Castellanos, D., Estrada, F., Jiménez‐Munt, I., Gorini, C., Fernández, M., Verges, J., & De Vicente, R. ( 2009 ). Catastrophic flood of the Mediterranean after the Messinian salinity crisis. Nature, 462, 778 – U796. https://doi.org/10.1038/nature08555
dc.identifier.citedreferenceGonzález‐Serna, M. J., Cordero, P. J., & Ortego, J. ( 2019 ). Spatiotemporally explicit demographic modelling supports a joint effect of historical barriers to dispersal and contemporary landscape composition on structuring genomic variation in a red‐listed grasshopper. Molecular Ecology, 28, 2155 – 2172. https://doi.org/10.1111/mec.15086
dc.identifier.citedreferenceGonzález‐Serna, M. J., Ortego, J., & Cordero, P. J. ( 2018 ). A review of cross‐backed grasshoppers of the genus Dociostaurus Fieber (Orthoptera: Acrididae) from the western Mediterranean: Insights from phylogenetic analyses and DNA‐based species delimitation. Systematic Entomology, 43, 136 – 146. https://doi.org/10.1111/syen.12258
dc.identifier.citedreferenceGraciá, E., Giménez, A., Anadón, J. D., Harris, D. J., Fritz, U., & Botella, F. ( 2013 ). The uncertainty of Late Pleistocene range expansions in the western Mediterranean: A case study of the colonization of south‐eastern Spain by the spur‐thighed tortoise, Testudo graeca. Journal of Biogeography, 40, 323 – 334. https://doi.org/10.1111/jbi.12012
dc.identifier.citedreferenceGriffin, D. L. ( 2002 ). Aridity and humidity: Two aspects of the late Miocene climate of North Africa and the Mediterranean. Palaeogeography, Palaeoclimatology, Palaeoecology, 182, 65 – 91. https://doi.org/10.1016/S0031‐0182(01)00453‐9
dc.identifier.citedreferenceHabel, J. C., Zachos, F. E., Dapporto, L., Rodder, D., Radespiel, U., Tellier, A., & Schmitt, T. ( 2015 ). Population genetics revisited ‐ towards a multidisciplinary research field. Biological Journal of the Linnean Society, 115, 1 – 12. https://doi.org/10.1111/bij.12481
dc.identifier.citedreferenceHuang, J.‐P., Hill, J., Ortego, J., & Knowles, L. L. ( 2020 ). Paraphyletic species no more – genomic data resolve a Pleistocene radiation and validate morphological species of the Melanoplus scudderi complex (Insecta: Orthoptera). Systematic Entomology, 45, 594 – 605. https://doi.org/10.1111/syen.12415
dc.identifier.citedreferenceHusemann, M., Schmitt, T., Zachos, F. E., Ulrich, W., & Habel, J. C. ( 2014 ). Palaearctic biogeography revisited: Evidence for the existence of a North African refugium for Western Palaearctic biota. Journal of Biogeography, 41, 81 – 94. https://doi.org/10.1111/jbi.12180
dc.identifier.citedreferenceJiménez‐Moreno, G., Fauquette, S., & Suc, J.‐P. ( 2010 ). Miocene to Pliocene vegetation reconstruction and climate estimates in the Iberian Peninsula from pollen data. Review of Palaeobotany and Palynology, 162, 403 – 415. https://doi.org/10.1016/j.revpalbo.2009.08.001
dc.identifier.citedreferenceJouzel, J., Masson‐Delmotte, V., Cattani, O., Dreyfus, G., Falourd, S., Hoffmann, G., Minster, B., Nouet, J., Barnola, J. M., Chappellaz, J., Fischer, H., Gallet, J. C., Johnsen, S., Leuenberger, M., Loulergue, L., Luethi, D., Oerter, H., Parrenin, F., Raisbeck, G., … Wolff, E. W. ( 2007 ). Orbital and millennial Antarctic climate variability over the past 800,000 years. Science, 317, 793 – 796. https://doi.org/10.1126/science.1141038
dc.identifier.citedreferenceKadereit, G., & Yaprak, A. E. ( 2008 ). Microcnemum coralloides (Chenopodiaceae‐ Salicornioideae): An example of intraspecific East‐West disjunctions in the Mediterranean region. Anales Del Jardín Botánico De Madrid, 65, 415 – 426.
dc.identifier.citedreferenceKajtoch, L., Cieslak, E., Varga, Z., Paul, W., Mazur, M. A., Sramko, G., & Kubisz, D. ( 2016 ). Phylogeographic patterns of steppe species in Eastern Central Europe: A review and the implications for conservation. Biodiversity and Conservation, 25, 2309 – 2339. https://doi.org/10.1007/s10531‐016‐1065‐2
dc.identifier.citedreferenceKatbeh‐Bader, A. ( 2001 ). Acridoidae (Orthoptera) of Jordan. Zoology in the Middle East, 21, 89 – 100. https://doi.org/10.1080/09397140.2001.10637873
dc.identifier.citedreferenceKeightley, P. D., Ness, R. W., Halligan, D. L., & Haddrill, P. R. ( 2014 ). Estimation of the spontaneous mutation rate per nucleotide site in a Drosophila melanogaster full‐sib family. Genetics, 196, 313 – 320. https://doi.org/10.1534/genetics.113.158758
dc.identifier.citedreferenceKirschner, P., Záveská, E., Gamisch, A., Hilpold, A., Trucchi, E., Paun, O., & Schönswetter, P. ( 2020 ). Long term isolation of European steppe outposts boots the biome´s conservation value. Nature Communications, 11, 1968. https://doi.org/10.1038/s41467‐020‐15620‐2
dc.identifier.citedreferenceKnowles, L. L. ( 2009 ). Statistical phylogeography. Annual Review of Ecology Evolution and Systematics, 40, 593 – 612. https://doi.org/10.1146/annurev.ecolsys.38.091206.095702
dc.identifier.citedreferenceKrijgsman, W., Hilgen, F. J., Raffi, I., Sierro, F. J., & Wilson, D. S. ( 1999 ). Chronology, causes and progression of the Messinian salinity crisis. Nature, 400, 652 – 655. https://doi.org/10.1038/23231
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