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Phylogeography and population genetics of the European mudminnow (Umbra krameri) with a time-calibrated phylogeny for the family Umbridae

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Abstract

The genetic structure of European mudminnow populations throughout the species range was examined using mitochondrial DNA and seven microsatellite loci. Ten mitochondrial haplotypes were detected, suggesting three phylogeographic lineages, which likely diverged during the Early and Middle Pleistocene. These three lineages geographically correspond to three regions: the Danube drainage including the Drava system and Dniester Delta, the Sava system and the Tisza system. High genetic diversity observed using mtDNA was confirmed with microsatellite data, suggesting the existence of 14 populations in the studied area. The isolation-with-migration model showed that migration rates between populations were generally low and were highest between the Drava and its tributary Mura. According to the inferred relative population splitting times, Umbra krameri likely spread from the eastern part of the species range to the west, which also showed the highest genetic diversity and largest population size. As reported by the time-calibrated phylogeny, separation of the European and American Umbra occurred roughly at the end of Late Cretaceous and in the first half of the Paleogene (60.57 Ma with 95% highest probability density of 39.57–81.75). Taking these results into account, appropriate guidelines are proposed to conserve European mudminnow populations.

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References

  • Abell, R., 2002. Conservation biology for the biodiversity crisis: a freshwater follow-up. Conservation Biology 16: 1435–1437.

    Article  Google Scholar 

  • Adams, B., P. W. DeHaan, R. Tabor, B. Thompson & D. K. Hawkins, 2013. Characterization of tetranucleotide microsatellite loci for Olympic mudminnow (Novumbra hubbsi). Conservation Genetics Resources 5: 573–575.

    Article  Google Scholar 

  • Agassiz, L., 1853. Recent researches of Prof. Agassiz. American Journal of Science and Arts 16: 134–136.

    Google Scholar 

  • Akaike, H., 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19: 716–723.

    Article  Google Scholar 

  • Akcakaya, H. R., G. Mills & C. P. Doncaster, 2007. The role of metapopulations in conservation. In Macdonald, D. W. & K. Service (eds), Key Topics in Conservation Biology. Blackwell Publishing, Oxford: 64–84.

    Google Scholar 

  • Ayres, D. L., A. Darling, D. J. Zwickl, P. Beerli, M. T. Holder, P. O. Lewis, J. P. Huelsenbeck, F. Ronquist, D. L. Swofford, M. P. Cummings, A. Rambaut & M. A. Suchard, 2012. BEAGLE: an application programming interface and high-performance computing library for statistical phylogenetics. Systematic Biology 61: 170–173.

    Article  PubMed  Google Scholar 

  • Bănăduc, D., 2008. Umbra krameri Walbaum, 1792 a Natura 2000 protected fish species, in Romania. Acta Ichtiologica Romanica 3: 33–44.

    Google Scholar 

  • Bănărescu, P. M. & D. Bănăduc, 2007. Habitats Directive (92/43/EEC) fish species (Osteichthyes) on the Romanian territory. Acta Ichtiologica Romanica 2: 43–78.

    Google Scholar 

  • Bănărescu, P. M., V. Otel & A. Wilhelm, 1995. The present status of Umbra krameri Walbaum in Romania. Annalen des Naturhistorischen Museums in Wien 97B: 496–501.

    Google Scholar 

  • Belkhir, K., P. Borsa, L. Chikhi, N. Raufaste & F. Bonhomme, 1996–2004. GENETIX v. 4.04, Logiciel sous WindowsTM pour la Ge´ne´tique des Populations. Universite´ Montpellier 2, Laboratoire Ge´nome et Population, Montpellier.

  • Brilly, M., 2010. Hydrological Processes of the Danube River Basin: Perspectives from the Danubian Countries. Springer, New York.

    Book  Google Scholar 

  • Brikiatis, L., 2014. The De Geer, Thulean and Beringia routes: key concepts for understanding early Cenozoic biogeography. Journal of Biogeography. doi:10.1111/jbi.12310.

    Google Scholar 

  • Cambray, J., 1997. Freshwater fish—a global biodiversity crisis. Hydrobiologia 353: 199–202.

    Article  Google Scholar 

  • Campbell, M. A. & J. A. López, 2014. Mitochondrial phylogeography of a Beringian relict: the endemic freshwater genus of blackfish Dallia (Esociformes). Journal of Fish Biology 84(2): 523–538.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, M. A., J. A. López, T. Sado & M. Miya, 2013. Pike and salmon as sister taxa: detailed intraclade resolution and divergence time estimation of Esociformes + Salmoniformes based on whole mitochondrial genome sequences. Gene 530: 57–65.

    Article  CAS  PubMed  Google Scholar 

  • Campbell, M. A., G. K. Sage, R. L. DeWilde, J. A. López & S. L. Talbot, 2014. Development and characterization of 16 polymorphic microsatellite loci for the Alaska blackfish (Esociformes: Dallia pectoralis). Conservation Genetics Resources 6(2): 349–351.

    Article  Google Scholar 

  • Clement, M., D. Posada & K. Crandall, 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657–1660.

    Article  CAS  PubMed  Google Scholar 

  • DeHaan, P. W., B. A. Adams, R. A. Tabor, D. K. Hawkins & B. Thompson, 2014. Historical and contemporary forces shape genetic variation in the Olympic mudminnow (Novumbra hubbsi), an endemic fish from Washington State, USA. Conservation Genetics 15: 1417–1431.

    Article  Google Scholar 

  • Denk, T., F. Grimsson, R. Zetter & L. A. Simonarson, 2011. The biogeographic history of Iceland—the North Atlantic Land Bridge revisited. Topics in Geobiology 35: 647–668.

    Article  Google Scholar 

  • Drummond, A. J., S. Y. W. Ho, M. J. Phillips & A. Rambaut, 2006. Relaxed phylogenetics and dating with confidence. PLoS Biology 4: e88. doi:10.1371/journal.pbio.0040088.

    Article  PubMed  PubMed Central  Google Scholar 

  • Drummond, A. J., M. A. Suchard, D. Xie & A. Rambaut, 2012. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Molecular Biology and Evolution 29: 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Estoup, A., P. Jarne & J.-M. Cournet, 2002. Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis. Molecular Ecology 11: 1591–1604.

    Article  CAS  PubMed  Google Scholar 

  • Evanno, G., S. Regnaut & J. Goudet, 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Felsenstein, J., 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.

    Article  Google Scholar 

  • Frankham, R., J. D. Ballou, M. R. Dudash, M. D. B. Eldridge, C. B. Fenster, R. C. Lacy, J. R. Mendelson, I. J. Porton, K. Ralls & O. A. Ryder, 2012. Implications of different species concepts for conserving biodiversity. Biological Conservation 153: 25–31.

    Article  Google Scholar 

  • Freyhof, J., 2013. Umbra krameri. The IUCN Red List of Threatened Species. Version 2014.2. www.iucnredlist.org. Accessed on 11 November 2014.

  • Funk, W. C., J. K. McKay, P. A. Hohenlohe & F. W. Allendorf, 2012. Harnessing genomics for delineating conservation units. Trends in Ecology and Evolution 27(9): 489–496.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gábris, Gy & L. Mari, 2007. The Pleistocene beheading of the Zala River (West Hungary). Földrajzi értesítő 56: 39–50. [In Hungarian with an English summary].

    Google Scholar 

  • Gaudant, J., 2012. An attempt at the palaeontological history of the European mudminnows (Pisces, Teleostei, Umbridae). Neues Jahrbuch Fur Geologie Und Palaontologie-Abhandlungen 263(2): 93–109.

    Article  Google Scholar 

  • Gernhard, T., 2008. The conditioned reconstructed process. Journal Theoretical Biology 253: 769–778.

    Article  Google Scholar 

  • Gibbard, P. & T. van Kolfschoten, 2004. The Pleistocene and Holocene epochs. In Gradstein, F. M., J. G. Ogg & A. G. Smith (eds), A Geologic Time Scale. Cambridge University Press, Cambridge: 441–452.

    Google Scholar 

  • Gladenkov, A. Y., A. E. Oleinik, L. Marincovich & K. B. Barinov, 2002. A refined age for the earliest opening of Bering Strait. Palaeogeography Palaeoclimatology Palaeoecology 183: 321–328.

    Article  Google Scholar 

  • Goudet, J., 2002. FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). http://www2.unil.ch/popgen/softwares/fstat.htm. Accessed 15 October 2009.

  • Govedič, M., 2010. Ribe reke Drave med Mariborom in Hrvaško mejo 35 let po izgradnji hidroelektrarn [Fish of Drava river between Maribor and Croatian border 35 years after construction of hydro power plants]. In Book of Abstracts–International conference on the Drava River–Life in the river basin, Slovenia, Dravograd (30. 09.–01. 10. 2010.). Jovan Hadži Institute of Biology Scientific Research Centre SASA, Municipality Dravograd, RRA Koroška–Regional Development Agency for Koroška, Ljubljana–Dravograd: 22–23.

  • Grande, L., 1999. The first Esox (Esocidae: Teleostei) from the Eocene Green River Formation, and a brief review of esocid fishes. Journal of Vertebrate Paleontology 19: 271–292.

    Article  Google Scholar 

  • Grande, T., H. Laten & J. López, 2004. Phylogenetic relationships of extant Esocid species (Teleostei: Salmoniformes) based on morphological and molecular characters. Copeia, 2004: 743–757.

    Article  Google Scholar 

  • Hajdú, J., L. Várkonyi, J. Ševc & T. Müller, 2015. Corrective notice to the European mudminnow (Umbra krameri Walbaum, 1792) record from the Black Sea. Biologia 70: 1429–1431.

    Article  Google Scholar 

  • Haponski, A. E. & C. A. Stepien, 2013. Phylogenetic and biogeographical relationships of the Sander pikeperches (Percidae: Perciformes): patterns across North America and Eurasia. Biological Journal of the Linnean Society 110: 156–179.

    Article  Google Scholar 

  • Hardy, O. J. & X. Vekemans, 2002. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2: 618.

    Article  Google Scholar 

  • Hardy, O. J., N. Charbonnel, H. Freville & M. Heuertz, 2003. Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163: 1467–1482.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hey, J. & R. Nielsen, 2007. Integration within the Felsenstein equation for improved Markov Chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Sciences 104: 2785–2790.

    Article  CAS  Google Scholar 

  • Ishiguro N. B., M. Miya & M. Nishida, 2003. Basal euteleostean relationships: a mitogenomic perspective on the phylogenetic reality of the “Protacanthopterygii”. Molecular Phylogenetics and Evolution 27: 476–488.

  • Keane, T. M., C. J. Creevey, M. M. Pentony, T. J. Naughton & J. O. McInerney, 2006. Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evolutionary Biology 6: 29. doi:10.1186/1471-2148-6-29.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kimura, M., 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16: 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Kuehne, M. L. & D. J. Olden, 2014. Ecology and conservation of mudminnow species worldwide. Fisheries 39: 341–351.

    Article  Google Scholar 

  • Kuhner, M. K., 2009. Coalescent genealogy samplers: windows into population history. Trends in Ecology and Evolution 24: 86–93.

    Article  PubMed  Google Scholar 

  • Lambeck, R. J., 1997. Focal species: a multi-species umbrella for nature conservation. Conservation Biology 11: 849–856.

    Article  Google Scholar 

  • Langella, O., 2002. Populations 1.2.28. Logiciel de génétique des populations. Laboratoire Populations, génétique et évolution, CNRS UPR 9034, Gif-sur-Yvette. http://www.cnrs-gif.fr/pge/. Accessed 10 October 2009.

  • López, A., P. Bentzen & W. Pietsch, 2000. Phylogenetic relationships of Esocoid fishes (Teleostei) based on partial cytochrome b and 16S mitochondrial DNA sequences. Copeia 2: 420–431.

    Article  Google Scholar 

  • López, A., W. Chen & W. Ortí, 2004. Esociform phylogeny. Copeia 3: 449–464.

    Article  Google Scholar 

  • Mace, G. M., H. P. Possingham & N. Leader-Williams, 2007. Prioritizing choices in conservation. In Macdonald, D. W. & K. Service (eds), Key Topics in Conservation Biology. Blackwell Publishing, Oxford: 17–34.

    Google Scholar 

  • Machordom, A. & I. Doadrio, 2001. Evidence of a Cenozoic Betic–Kabilian connection based on freshwater fish phylogeography (Luciobarbus, Cyprinidae). Molecular Phylogenetics and Evolution 18: 252–263.

    Article  CAS  PubMed  Google Scholar 

  • Marić, S., A. Snoj, N. Sekulić, J. Krpo-Ćetković, R. Šanda & V. Jojić, 2015. Genetic and morphological variability of the European mudminnow Umbra krameri (Teleostei, Umbridae) in Serbia and in Bosnia and Herzegovina—a basis for future conservation activities. Journal of Fish Biology 86(5): 1534–1548.

    Article  PubMed  Google Scholar 

  • Marko, P. B. & M. W. Hart, 2012. Retrospective coalescent methods and the reconstruction of metapopulation histories in the sea. Evolutionary Ecology 26: 291–315.

    Article  Google Scholar 

  • Mangerud, J., M. Jakobsson, H. Alexanderson, V. Astakhov, G. K. C. Clarke, M. Henriksen, C. Hjort, G. Krinner, J. Lunkka, P. Möller, A. Murray, O. Nikolskaya, M. Saarnisto & J. Svendsen, 2004. Ice-dammed lakes and rerouting of the drainage of northern Eurasia during the Last Glaciation. Quaternary Science Reviews 23: 1313–1332.

    Article  Google Scholar 

  • Mikschi, E. & J. Wanzenböck, 1995. Proceedings of the First International Workshop on Umbra krameri. Annalen des Naturhistorischen Museums in Wien 97B: 438–508.

    Google Scholar 

  • Miller, M. A., W. Pfeiffer & T. Schwartz, 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010. New Orleans: 1–8.

  • Moritz, C., K. McGuigan & L. Bernatchez, 2002. Conservation of freshwater fishes: integrating evolution and genetics with ecology. In Collares-Pereira, M. J., I. G. Cowx & M. M. Coelho (eds), Conservation of Freshwater Fishes: Options for the Future. Fishing News Books, Blackwell Science, Oxford: 293–310.

    Google Scholar 

  • Nelson, G. J., 1972. Cephalic sensory canals, pitlines, and the classification of esocoid fishes, with notes on galaxiids and other teleosts. American Museum Novitates 2492: 1–49.

    Google Scholar 

  • Olden, J. D., 2016. Challenges and opportunities for fish conservation in dam-impacted waters. In Closs, G. P., M. Krkosek & J. D. Olden (eds), Conservation of Freshwater Fishes. Cambridge University Press, Cambridge: 107–142.

    Chapter  Google Scholar 

  • Pekárik, L., J. Hajdú & J. Koščo, 2014. Identifying the key habitat characteristics of threatened European mudminnow (Umbra krameri, Walbaum 1792). Fundamental and Applied Limnology 184: 151–159.

    Article  Google Scholar 

  • Penck, A. & E. Brückner, 1909. Die Alpen im Eiszeitalter. Taunitz, Leipzig.

    Google Scholar 

  • Pickens, D. C., 2003. Genetic Evidence for a Population Bottleneck in the Olympic Mudminnow (Novumbra hubbsi). B.S. Degree, University of Puget Sound, Tacoma.

    Google Scholar 

  • Pritchard, J. K., M. Stephens & P. Donnelly, 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut, A., M. A. Suchard, D. Xie & A. J. Drummond, 2014. Tracer v1.6, Available from http://beast.bio.ed.ac.uk/Tracer. Accessed 1 Dec 2015.

  • Raykov, V. St., M. Panayotova, P. Ivanova, I. Dobrovolov & V. Maximov, 2012. First record and allozyme data of European mudminnow Umbra krameri Walbaum, 1792 (Pisces: Umbridae) in the Black Sea. Comptes rendus de l’Académie bulgare des Sciences 65(1): 49–52.

    Google Scholar 

  • Sambrook, J., E. F. Fritseh & T. Maniatis, 1989. Molecular Cloning. A Laboratory Manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.

    Google Scholar 

  • Scotese, C. R., 2001. Atlas of Earth History, Volume 1, Paleogeography, PALEOMAP Project, Arlington.

  • Sekulić, N., S. Marić, L. Galamboš, D. Radošević & J. Krpo-Ćetković, 2013. New distribution data and population structure of the European mudminnow Umbra krameri in Serbia and Bosnia and Herzegovina. Journal of Fish Biology 83: 659–666.

    Article  PubMed  Google Scholar 

  • Shedko, S. V., I. L. Miroshnichenko & G. A. Nemkova, 2013. Phylogeny of Salmonids (Salmoniformes: Salmonidae) and its molecular dating: analysis of mtDNA data. Russian Journal of Genetics 49: 623–637.

    Article  CAS  Google Scholar 

  • Skog, A., L. A. Vøllestad, N. C. Stenseth, A. Kasumyan & K. S. Jakobsen, 2014. Circumpolar phylogeography of the northern pike (Esox lucius) and its relationship to the Amur pike (E. reichertii). Frontiers in Zoology 11: 67.

  • Stepien C. A., J. Behrmann-Godel & L. Bernatchez, 2015. Evolutionary relationships, population genetics, and ecological and genomic adaptations of perch (Perca). In Couture, P., G. Pyle (eds), Biology of perch. CRC Press, Taylor and Francis Group, Boka Raton: 7–46.

  • Szpiech, Z. A., M. Jakobsson & N. A. Rosenberg, 2008. ADZE: a rarefaction approach for counting alleles private to combinations of populations. Bioinformatics 24: 2498–2504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takács, P., T. Erős, A. Specziár, P. Sály, Z. Vitál, Á. Ferincz, T. Molnár, Z. Szabolcsi, P. Bíró & E. Csoma, 2015. Population genetic patterns of threatened European Mudminnow (Umbra krameri Walbaum, 1792) in a fragmented landscape: implications for conservation management. PLoS ONE 10(9): e0138640.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tamura, K. & M. Nei, 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10: 512–526.

    CAS  PubMed  Google Scholar 

  • Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei & S. Kumar, 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731–2739.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin & D. G. Higgins, 1997. The CLUSTAL_X windows interface, flexible strategies for multiple sequence alignment aided by quality analysis tool. Nucleic Acids Research 25: 4876–4882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiffney, B. H., 1985. The Eocene North Atlantic Land Bridge: its importance in Tertiary and modern phytogeography of the Northern Hemisphere. Journal of the Arnold Arboretum 66: 243–273.

    Article  Google Scholar 

  • Trombitsky, I., V. Lobcenco & A. Moshu, 2001. The European mudminnow, Umbra krameri, still populates the Dniester River in Moldova. Folia Zoologica 50: 159–160.

    Google Scholar 

  • Vähä, J. P., J. Erkinaro, E. Niemelä & C. R. Primmer, 2007. Life-history and habitat features influence the within-river genetic structure of Atlantic salmon. Molecular Ecology 16: 2638–2654.

    Article  PubMed  Google Scholar 

  • Van Oosterhout, C., W. F. D. Hutchinson, P. M. Wills & P. Shipley, 2004. MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4: 535–538.

    Article  Google Scholar 

  • Velkov, B., L. Pehlivanov & M. Vassilev, 2004. Umbra krameri (Pisces: Umbridae): a reinstated species for the Bulgarian ichthyofauna. Acta Zoologica Bulgarica 56: 233–235.

    Google Scholar 

  • Wakeley, J., 2000. The effects of subdivision on the genetic divergence of populations and species. Evolution 54: 1092–1101.

    Article  CAS  PubMed  Google Scholar 

  • Wanzenböck, J., 1995. Current knowledge on the European mudminnow Umbra krameri Walbaum, 1792. Annalen des Naturhistorischen Museums in Wien 97B: 439–449.

    Google Scholar 

  • Wanzenböck, J., 2004. European mudminnow (Umbra krameri) in the Austrian floodplain of the River Danube–Conservation of an indicator species for endangered wetland ecosystems in Europe. In Akcakaya, H. R., M. A. Burgman, O. Kindvall, C. C. Wood, P. Sjögren-Gulve, J. S. Hatfield & M. A. McCarthy (eds), Species Conservation and Management. Oxford University Press, New York: 200–207.

    Google Scholar 

  • Wilson, M. V. H., D. B. Brinkman & A. G. Neuman, 1992. Cretaceous Esocoidei (Teleostei): early radiation of the pikes in North American fresh waters. Journal of Paleontology 66: 839–846.

    Article  Google Scholar 

  • Winkler, K. A. & S. Weiss, 2009. Nine new tetranucleotide microsatellite DNA markers for the European mudminnow Umbra krameri. Conservation Genetics 10: 1155–1157.

    Article  CAS  Google Scholar 

  • Yang, Z., 1993. Maximum likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Molecular Biology and Evolution 10: 1396–1401.

    CAS  PubMed  Google Scholar 

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Acknowledgements

This study received support from the Slovenian Research Agency, the Ministry of Education, Science and Technological Development of the Republic of Serbia (Grant No. 173045) and the SYNTHESYS Project (CZ-TAF-5090; http://www.synthesys.info/) financed by European Community Research Infrastructure Action under the FP7 Integrating Activities Programme. RŠ was supported by the Ministry of Culture of the Czech Republic (DKRVO 2016/15, National Museum, 00023272) and DS by the DIANET postdoctoral fellowship programme (FP1527385002). TE, PT and ASp would like to express their thanks for Eszter Csoma for the DNA extraction of the Hungarian samples. Many thanks to dr Ladislav Pekarik for collected samples of European mudminnow from the Slovak Republic.

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Authors and Affiliations

  1. Institute of Zoology, Faculty of Biology, University of Belgrade, Studentski trg 16, Belgrade, 11001, Serbia

    Saša Marić

  2. Department of Animal Science, Biotechnical Faculty, University of Ljubljana, Groblje 3, 1230, Domžale, Slovenia

    David Stanković & Aleš Snoj

  3. Department of Life Sciences, University of Trieste, Via Licio Giorgieri 5, 34127, Trieste, Italy

    David Stanković

  4. Research Institute for Limnology, University of Innsbruck, Mondseestraße 9, 5310, Mondsee, Austria

    Josef Wanzenböck

  5. Department of Zoology, National Museum, Václavské náměstí 68, 115 79, Prague 1, Czech Republic

    Radek Šanda

  6. MTA Centre for Ecological Research, Balaton Limnological Institute, Klebelsberg Kuno u. 3, Tihany, 8237, Hungary

    Tibor Erős, Péter Takács & András Specziár

  7. Institute for Nature Conservation of Serbia, Dr Ivana Ribara 91, Novi Beograd, 11070, Serbia

    Nenad Sekulić

  8. Faculty of Sciences, Lucian Blaga University of Sibiu, Dr. Ion Raţiu 5-7, 550012, Sibiu, Romania

    Doru Bănăduc

  9. Faculty of Teacher Education, University of Zagreb, Savska cesta 77, 10000, Zagreb, Croatia

    Marko Ćaleta

  10. Eco-TIRAS International Association of Dniester River Keepers, Teatrala 11A, 2012, Chisinau, Moldova

    Ilya Trombitsky

  11. Institute for Nature Conservation of Vojvodina, Radnička 20a, Novi Sad, 21000, Serbia

    László Galambos

  12. Department of Biology and Ecology, Faculty of Science, University of Novi Sad, Trg D. Obradovića 2, Novi Sad, Serbia

    Sándor Sipos

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Marić, S., Stanković, D., Wanzenböck, J. et al. Phylogeography and population genetics of the European mudminnow (Umbra krameri) with a time-calibrated phylogeny for the family Umbridae. Hydrobiologia 792, 151–168 (2017). https://doi.org/10.1007/s10750-016-3051-9

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