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Cryptic diversity in Telestes pleurobipunctatus (Actinopterygii; Leuciscidae) as a consequence of historical biogeography in the Ionian Freshwater Ecoregion (Greece, Albania)

  • Ivana BujEmail author
  • Radek Šanda
  • Stamatis Zogaris
  • Jörg Freyhof
  • Matthias F. Geiger
  • Jasna Vukić
Primary Research Paper
  • 22 Downloads

Abstract

It was reported that the complex geological history of the southern Balkans caused diversification of terrestrial species. On the other hand, knowledge of the evolutionary history of freshwater biota is scarce. In order to contribute to an understanding of the historical biogeography of the region’s freshwaters, as well as to describe intraspecific diversity and structure of a species distributed in the Ionian Ecoregion, we have analysed the population genetic structure and evolutionary history of Telestes pleurobipunctatus. Analyses were based on the mitochondrial gene for cytochrome b from samples covering the whole distribution range of this species. A high level of intraspecific structuring was revealed inside T. pleurobipunctatus. Its evolutionary history corroborates the complexity of historical geologic events in the area. Telestes pleurobipunctatus comprises two main clades (northern and southern), which have been separated from each other for about seven million years and that are further divided. The Louros and Arachthos Rivers were denoted as ancestral geographic ranges of the northern clade. The distribution range of the ancestor of the southern clade seems to comprise rivers flowing into the Patraikos Gulf. Structures within the two main clades, as well as timing of diversification events are different, implying separate evolutionary courses.

Keywords

Conservation priorities Geological history Mediterranean biodiversity Population genetic structure Telestes 

Notes

Acknowledgements

This work was supported by the Czech Science Foundation (Project GA15-19382S), institutional resources of the Ministry of Education, Youth, and Sports of the Czech Republic (JV) and Ministry of Culture of the Czech Republic (DKRVO 2019-2023/VI.4.a, National Museum, 00023272) (RS). IB received support from the SYNTHESYS Programme project CZ-TAF-4228 at the National Museum Prague, financed by European Community Research Infrastructure Action under the FP7 “Capacities” Programme. Support came also from the Project FREDIE (www.fredie.eu) funded by the Joint Initiative for Research and Innovation (PAKT) program of the Leibniz Association (JF, MFG). We are grateful to D. Kommatas and L. Vardakas for assistance in the field, as well as to A. N. Economou for discussions on the evolutionary history of T. pleurobipunctatus.

References

  1. Avise, J. C., 1986. Mitochondrial DNA and the evolutionary genetics of higher animals. Philosophical Transactions of the Royal Society B 312: 325–342.CrossRefGoogle Scholar
  2. Ballard, J. W. O., 2000. Comparative genomics of mitochondrial DNA in Drosophila simulans. Journal of Molecular Evolution 51: 64–75.CrossRefGoogle Scholar
  3. Banarescu, P. M., 2004. Distribution patterrn of the aquatic fauna of the Balkan Peninsula. In Griffiths, H. I., B. Kryštufek & J. M. Reed (eds), Balkan Biodiversity. Springer, Dordrecht.Google Scholar
  4. Barbieri, R., A. N. Economou, M. Stoumboudi & P. S. Economidis, 2002. Freshwater fishes of Peloponnese (Greece): distribution, ecology and threats. Conservation of Freshwater Fishes: Options for the Future. pp. 55–64.Google Scholar
  5. Barbieri, R., S. Zogaris, E. Kalogianni, M. Stoumboudi, Y. Chatzinikolaou, S. Giakoumi, Y. Kapakos, D. Kommatas, N. Koutsikos, V. Tachos, L. Vardakas & A. N. Economou, 2015. Freshwater fishes and lampreys of Greece: an annotated checklist. Monographs on Marine Sciences No. 8. Hellenic Center for Marine Research, Athens. ISBN: 978-960-9798-06-8.Google Scholar
  6. Beerli, P., 1998. Estimation of migration rates and population sizes in geographically structured populations. In Carvalho, G. (ed.), Advances in Molecular Ecology., NATO-ASI Workshop Series IOS Press, Amsterdam: 39–53.Google Scholar
  7. Beerli, P., 2009. How to use Migrate or why are markov chain monte carlo programs difficult to use? In Bertorelle, G., M. W. Bruford, H. C. Hauffe, A. Rizolli & C. Vernese (eds), Population Genetics for Animal Conservation, Vol. 17., Conservation Biology Cambridge University Press, Cambridge.Google Scholar
  8. Beerli, P. & J. Felsenstein, 2001. Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proceedings of the National Academy of Sciences of the USA 98: 4563–4568.CrossRefGoogle Scholar
  9. Beerli, P., H. Hotz & T. Uzzell, 1996. Geologically dated sea barriers calibrate a protein clock for Aegean water frogs. Evolution 50: 1676–1678.CrossRefGoogle Scholar
  10. Bianco, P., 1990. Potential role of the paleohistory of the Mediterranean and Paratethys basin on the early dispersal of Euro-Mediterranean freshwater fishes. Ichtyological Exploration Freshwaters 1: 167–184.Google Scholar
  11. Bianco, P. G., 1988. Leuciscus cephalus (Linnaeus), with records of fingerling adult males, Leuciscus pleurobipunctatus (Stphanidis) and their hybrids from western Greece. Journal of Fish Biology 32: 1–16.CrossRefGoogle Scholar
  12. Böhme, M. U., N. Schneeweis, U. Fritz, J. Moravec, I. Majláth, V. Majláthova & T. U. Berendonk, 2006. Genetic differentiation and diversity of Lacerta viridis viridis (Laurenti, 1768) within the northern part of its range: an investigation using mitochondrial haplotypes. Salamandra 42: 29–40.Google Scholar
  13. Brazee, N. J. & D. L. Lindner, 2013. Unravelling the Phellinus pini s.l. complex in North America: a multilocus phylogeny and differentiation analysis of Porodaedalea. Forest Pathology 43: 132–143.CrossRefGoogle Scholar
  14. Buj, I., M. Ćaleta, Z. Marčić, R. Šanda, J. Vukić & M. Mrakovčić, 2015. Different histories, different destinies-impact of evolutionary history and population genetic structure on extinction risk of the Adriatic spined loaches (genus Cobitis; Cypriniformes, Actinopterygii). PLoS ONE 10(7): e0131580.  https://doi.org/10.1371/journal.pone.0131580.CrossRefPubMedPubMedCentralGoogle Scholar
  15. Buj, I., Z. Marčić, M. Ćaleta, R. Šanda, M. F. Geiger, J. Freyhof, A. Machordom & J. Vukić, 2017. Ancient connections among the European rivers and watersheds revealed from the evolutionary history of the genus Telestes (Actinopterygii; Cypriniformes). PLoS ONE 12(12): e0187366.  https://doi.org/10.1371/journal.pone.0187366.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Castresana, J., 2001. Cytochrome b phylogeny and the taxonomy of great apes and mammals. Molecular Biology and Evolution 18: 465–471.CrossRefGoogle Scholar
  17. Dimopoulos, P., T. Raus, E. Bergmeier, T. Constantinidis, G. Iatrou, S. Kokkini, A. Strid & D. Tzanoudakis, 2016. Vascular plants of Greece: an annotated checklist. Willdenowia 46: 301–347.CrossRefGoogle Scholar
  18. 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: 751–761.CrossRefGoogle Scholar
  19. Dubut, V., A. Fouquet, A. Voisin, C. Costedoat, R. Chappaz & A. Gilles, 2012. From late Miocene to Holocene: processes of differentiation within the Telestes genus (Actinopterygii: Cyprinidae). PlosOne 7(3): e34423.CrossRefGoogle Scholar
  20. Durand, J. D., A. R. Templeton, B. Guinand, A. Imsidirou & Y. Bouvet, 1999. Nested clade and phylogeographic analyses of the chub, Leuciscus cephalus (Teleostei, Cyprinidae), in Greece: implications for Balkan Penninsula biogeography. Molecular Phylogenetecs and Evolution 13: 566–580.CrossRefGoogle Scholar
  21. Durand, J. D., E. Unlu, I. Doadrio, S. Pipoyan & A. R. Templeton, 2000. Origin, radiation, dispersion and allopatric hybridization in the chub Leuciscus cephalus. Proceedings of the Royal Society London B 267: 1687–1697.CrossRefGoogle Scholar
  22. Economidis, P. S. & P. M. Banarescu, 1991. The distribution and origins of freshwater fishes in the Balkan Peninsula, especially in Greece. Internationale Revue der gesamten Hydrobiologie und Hydrographie 76: 257–283.CrossRefGoogle Scholar
  23. Economou, A. N., R. Barbieri, C. H. Daoulas, T. Psarras, M. Stoumboudi, I. Bertahas, S. Giakoumi & A. Patsias, 1999. Endangered Freshwater Fish of Western Greece and the Peloponnese: Distribution, Abundance, Threats and Measures for Protection. Final Technical Report, National Centre for Marine Research, 341 pp. (In Greek).Google Scholar
  24. Economou A. N., Y. Chatzinikolaou, U. Dussling, K. Basel, S. Giakoumi & S. Zogaris, 2006. Distribution patterns of fish in mountain streams of western Greece. 10th International Congress on the Zoogeography and Ecology of Greece and Adjacent Regions, Book of Abstracts, Patras, p. 30.Google Scholar
  25. Economou, A. N., S. Giakoumi, L. Vardakas, R. Barbieri, M. Stoumboudi & S. Zogaris, 2007. The freshwater ichthyofaunal of Greece: an update based on a hydrographic basin survey. Mediterranean Marine Science 8: 91–168.CrossRefGoogle Scholar
  26. Farias, I. P., G. Ortí, I. Sampaio, H. Schneider & A. Meyer, 2001. The cytochrome b Gene as a phylogenetic marker: the limits of resolution for analyzing relationships among cichlid fishes. Journal of Molecular Evolution 53: 89–103.CrossRefGoogle Scholar
  27. Frankham, R., J. D. Ballou & D. A. Briscoe, 2010. Introduction to Conservation Genetics. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
  28. Fu, Y. X. & W. H. Li, 1993. Statistical tests of neutrality of mutations. Genetics 133: 693–709.PubMedPubMedCentralGoogle Scholar
  29. Geiger, M. F., F. Herder, M. T. Monaghan, V. Almada, R. Barbieri, M. Bariche, P. Berrebi, J. Bohlen, M. Casal-Lopez, G. B. Delmastro, G. P. J. Denys, A. Dettai, I. Doadrio, E. Kalogianni, H. Kärst, M. Kottelat, M. Kovačić, M. Laporte, M. Lorenzoni, Z. Marčić, M. Özuluğ, A. Perdices, S. Perea, H. Persat, S. Porcelotti, C. Puzzi, J. Robalo, R. Šanda, M. Schneider, V. Šlechtová, M. Stoumboudi, S. Walter & J. Freyhof, 2014. Spatial heterogeneity in the Mediterranean biodiversity hotspot affects barcoding accuracy of its freshwater fishes. Molecular Ecology Resources 14: 1210–1221.CrossRefGoogle Scholar
  30. Guinand, B., J. D. Durand & J. Laroche, 2001. Identifying main evolutionary mechanisms shaping genetic variation of Leuciscus cephalus L. 1758 (Cyprinidae) in Western Greece: discordance between methods. Evolution, Life Sciences 324: 1045–1060.Google Scholar
  31. Hall, G., 2006. Selective constraint and genetic differentiation in geographically distant barley yellow dwarf virus population. Journal of General Virology 87: 3067–3075.CrossRefGoogle Scholar
  32. Hey, J. & J. Wakeley, 1997. A coalescent estimator of the population recombination rate. Genetics 145: 833–846.PubMedPubMedCentralGoogle Scholar
  33. Hudson, R. R., D. D. Boos & N. L. Kaplan, 1992. A statistical test for detecting geographic subdivision. Molecular Biology and Evolution 9: 138–151.PubMedGoogle Scholar
  34. Huelsenbeck, J. P. & F. Ronquist, 2001. MRBAYES: bayesian inference of phylogenetic trees. Bioinformatics 17: 754–755.CrossRefGoogle Scholar
  35. Jolivet, L. & C. Faccenna, 2000. Mediterranean extensions and the Africa-Eurasia collision. Tectonics 19: 1095–1106.CrossRefGoogle Scholar
  36. Ketmaier, V., P. G. Bianco, M. Cobolli, M. Krivokapic, R. Caniglia & E. de Matthaeis, 2004. Molecular phylogeny of two lineages of Leuciscinae cyprinids (Telestes and Scardinius) from the peri-Mediterranean area based on cytochrome b data. Molecular Phylogenetics and Evolution 32: 1061–1071.CrossRefGoogle Scholar
  37. Kottelat, M. & J. Freyhof, 2007. Handbook of European freshwater fishes. Freyhof, Berlin.Google Scholar
  38. Koutsikos, N., S. Zogaris, L. Vardakas, V. Tachos, E. Kalogianni, R. Šanda, Y. Chatzinikolaou, S. Giakoumi, P. S. Economisid & A. N. Economou, 2012. Recent distributional contributions to the freshwater ichthyofaunal of Greece. Mediterranean Marine Science 13: 268–277.CrossRefGoogle Scholar
  39. Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefGoogle Scholar
  40. Lymberakis, P. & N. Poulakakis, 2010. Three continents claiming an archipelago: the evolution of Aegean’s herpetofaunal diversity. Diversity 2: 233–255.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Maurakis, E. G., M. K. Pritchard & P. S. Economidis, 2001. Historical relationships of mainland river drainages in Greece. BIOS 6: 109–124.Google Scholar
  43. Nei, M. & R. K. Chesser, 1983. Estimation of fixation indices and gene diversities. Annals of Human Genetics 47: 253–259.CrossRefGoogle Scholar
  44. Oikonomou, A., F. Leprieur & I. D. Leonardos, 2014. Biogeography of freshwater fishes of the Balkan Peninsula. Hydrobiologia 738: 205–220.CrossRefGoogle Scholar
  45. Papadaki, C., K. Soulis, R. Muñoz-Mas, F. Martinez Capel, S. Zoragis, L. Ntoanidis & E. Dimitriou, 2016. Potential impacts of climate change on flow regime and fish habitat in mountain rivers of the southwestern Balkans. Science of the Total Environment.  https://doi.org/10.1016/j.sctotenv.2015.06.134.CrossRefPubMedGoogle Scholar
  46. Patwardhan, A., S. Ray & A. Roy, 2014. Molecular markers in phylogenetic studies: a review. Journal of Phylogenetics & Evolutionary Biology 2: 131.  https://doi.org/10.4172/2329-9002.1000131.CrossRefGoogle Scholar
  47. Perea, S., M. Bohme, P. Zupancic, J. Freyhof, R. Sanda, M. Ozulug, A. Abdoli & I. Doadrio, 2010. Phylogenetic relationships and biogeographical patterns in circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evolutionary Biology 10: 265.CrossRefGoogle Scholar
  48. Perea, S., J. Vukić, R. Šanda & I. Doadrio, 2016. Ancient mitochondrial capture as factor promoting mitonuclear discordance in freshwater fishes: a case study in the genus Squalius (Actinopterygii, Cyprinidae) in Greece. PloS ONE 11(12): e0166292.  https://doi.org/10.1371/journal.pone.0166292.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Perissoratis, C. & N. Conispoliatis, 2003. The impacts of sea-level changes during latest Pleistocene and Holocene times on the morphology of the Ionian and Aegean seas (SE Alpine Europe). Marine Geology 196: 145–156.CrossRefGoogle Scholar
  50. Poulakakis, N., P. Lymberakis, A. Antoniou, et al., 2003. Molecular phylogeny and biogeography of the wall lizard Podarcis erhardii (Squamata: Lacertidae). Molecular Phylogenetics and Evolution 28: 38–46.CrossRefGoogle Scholar
  51. Poulakakis, N., P. Lymberakis, C. S. Tsigenopoulos, A. Magoulas & M. Mylonas, 2005a. Phylogenetic relationships and evolutionary history of snake-eyed skink Ablepharus kitaibelii (Sauria: Scincidae). Molecular Phylogenetics and Evolution 34: 245–256.CrossRefGoogle Scholar
  52. Poulakakis, N., P. Lymberakis, E. Valakos, P. Pafilis, E. Zouros & M. Mylonas, 2005b. Phylogeography of Balkan wall lizard (Podarcis taurica) and its relatives inferred from mitochondrial DNA sequences. Molecular Ecology 14: 2433–2443.CrossRefGoogle Scholar
  53. Rögl, F., 1998. Palaeographic consideration for Mediterranean and Paratethys seaways (Oligocene to Miocene). Annalen des Naturhistorischen Museums in Wien 99A: 279–310.Google Scholar
  54. Rögl, F., 1999. Mediterranean and Paratethys. Facts and hypotheses of an Oligocene to Miocene paleogeography. Geologica Carpathica 50: 339–349.Google Scholar
  55. Roveri, M., R. Flecker, W. Krijgsman, J. Lofi, S. Lugli, V. Manzi, F. J. Sierro, A. Bertini, A. Camerlenghi, G. De Lange, R. Govers, F. J. Hilgen, C. Hübscher, P Th Meijer & M. Stoica, 2014. The Messinian Salinity Crisis: past and future of a great challenge for marine sciences. Marine Geology 352: 25–58.CrossRefGoogle Scholar
  56. Ryder, O. A., 1986. Species conservation and systematics: the dilemma of subspecies. Trends in Ecology and Evolution 1: 9–10.CrossRefGoogle Scholar
  57. Šanda, R., J. Vukić, L. Choleva, J. Křížek, A. Šedivá, S. Shumka & I. F. Wilson, 2008. Distribution of loach fishes (Cobitidae, Nemacheilidae) in Albania, with genetic analysis of populations of Cobitis ohridana. Folia Zoologica 57: 42–50.Google Scholar
  58. Schönhuth, S., J. Vukić, R. Šanda, L. Yang & R. L. Mayden, 2018. Phylogenetic relationships and classification of the Holarctic family Leuciscidae (Cypriniformes: Cyprinoidei). Molecular Phylogenetics and Evolution 127: 781–799.CrossRefGoogle Scholar
  59. Sfenthourakis, S. & A. Legakis, 2001. Hotspots of endemic terrestrial invertebrates in southern Greece. Biodiversity and Conservation 10: 1387–1417.CrossRefGoogle Scholar
  60. Sola, E., R. Sluys, K. Gritzalis & M. Riutort, 2013. Fluvial basin history in the northeastern Mediterranean region underlies dispersal and speciation patterns in the genus Dugesia (Platyhelmintes, Tricladida, Dugesiidae). Molecular Phylogenetics and Evolution 66: 877–888.CrossRefGoogle Scholar
  61. Swofford, D. L., 2002. PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4 [Computer software and manual]. Sinauer Associates, Sunderland, MA.Google Scholar
  62. Tajima, F., 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585–595.PubMedPubMedCentralGoogle Scholar
  63. Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.CrossRefGoogle Scholar
  64. Tobe, S. S., A. C. Kitchener & A. M. Linacre, 2010. Reconstructing mammalian phylogenies: a detailed comparison of the cytochrome B and cytochrome oxidase subunit I mitochondrial genes. PLoS ONE 5: e14156.CrossRefGoogle Scholar
  65. Tsigenopoulos, C. S. & P. Berrebi, 2000. Molecular phylogeny of North Mediterranean freshwater barbs (genus Barbus: Cyprinidae) Inferred from cytochrome b sequences: biogeographic and systematic implications. Molecular Phylogenetics and Evolution 14: 165–179.CrossRefGoogle Scholar
  66. Vasileiadou, K., M. Böhme, T. A. Neubauer, G. L. Georgalis, G. E. Syrides, L. Papadopoulou & N. Zouros, 2017. Early Miocene gastropod and ectothermic vertebrate remains from the Lesvos Petrified Forest (Greece). PalZ 91: 541–564.CrossRefGoogle Scholar
  67. Vogiatzi, E., E. Kalogianni, B. Zimmerman, S. Giakoumi, R. Barbieri, P. Paschou, A. Magoulas, D. Tsaparis, N. Poulakakis & C. S. Tsigenopoulos, 2014. Reduced genetic variation and strong genetic population structure in the freshwater killifish Valencia letourneuxi (Valenciidae) based on nuclear and mitochondrial markers. Biological Journal of the Linnean Society 111: 334–349.CrossRefGoogle Scholar
  68. Yu, Y., A. J. Harris & X. He, 2010. S-DIVA (Statistical Dispersal-Vicariance Analysis): a tool for inferring biogeographic histories. Molecular Phylogenetic and Evolution 56: 848–850.CrossRefGoogle Scholar
  69. Zardoya, R. & I. Doadrio, 1999. Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. Journal of Molecular Evolution 49: 227–237.CrossRefGoogle Scholar
  70. Zogaris, S., A. Economou & P. Dimopoulos, 2009a. Ecoregions in the Southern Balkans: should they be revised? Journal of Environmental Management 43: 682–697.  https://doi.org/10.1007/s00267-008-9243-y.CrossRefGoogle Scholar
  71. Zogaris, S., Y. Chatzinikolaou & P. Dimopoulos, 2009b. Assessing environmental degradation of montane riparian zones in Greece. Journal of Environmental Biology 30: 719–726.PubMedGoogle Scholar
  72. Zogaris, S. & A. N. Economou, 2017. The biogeographic characteristics of the river basins of Greece. In Skoulikidis, N., I. Karaouzas & E. Dimitriou (eds), The Rivers of Greece: Evolution, Current Status and Perspectives. Springer, NewYork: 53–95.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Zoology, Faculty of ScienceUniversity of ZagrebZagrebCroatia
  2. 2.National MuseumPragueCzech Republic
  3. 3.Hellenic Centre for Marine Research, Institute of Marine Biological Sciences and Inland WatersAnavissosGreece
  4. 4.German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-LeipzigLeipzigGermany
  5. 5.Zoologisches Forschungsmuseum Alexander KoenigBonnGermany
  6. 6.Department of Ecology, Faculty of ScienceCharles UniversityPragueCzech Republic

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