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Cryptic Diversity in Telestes Pleurobipunctatus (Actinopterygii

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Cryptic Diversity in Telestes Pleurobipunctatus (Actinopterygii Cryptic diversity in Telestes pleurobipunctatus (Actinopterygii; Leuciscidae) as a consequence of historical biogeography in the Ionian Freshwater Ecoregion (Greece, Albania) Ivana Buj, Radek Šanda, Stamatis Zogaris, Jörg Freyhof, Matthias F. Geiger & Jasna Vukić Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Hydrobiologia DOI 10.1007/s10750-019-3935-6 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Nature Switzerland AG. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Hydrobiologia https://doi.org/10.1007/s10750-019-3935-6 (0123456789().,-volV)(0123456789().,-volV) PRIMARY RESEARCH PAPER Cryptic diversity in Telestes pleurobipunctatus (Actinopterygii; Leuciscidae) as a consequence of historical biogeography in the Ionian Freshwater Ecoregion (Greece, Albania) Ivana Buj . Radek Sˇanda . Stamatis Zogaris . Jo¨rg Freyhof . Matthias F. Geiger . Jasna Vukic´ Received: 14 August 2018 / Revised: 6 March 2019 / Accepted: 8 March 2019 Ó Springer Nature Switzerland AG 2019 Abstract It was reported that the complex geolog- corroborates the complexity of historical geologic ical history of the southern Balkans caused diversifi- events in the area. Telestes pleurobipunctatus com- cation of terrestrial species. On the other hand, prises two main clades (northern and southern), which knowledge of the evolutionary history of freshwater have been separated from each other for about seven biota is scarce. In order to contribute to an under- million years and that are further divided. The Louros standing of the historical biogeography of the region’s and Arachthos Rivers were denoted as ancestral freshwaters, as well as to describe intraspecific geographic ranges of the northern clade. The distri- diversity and structure of a species distributed in the bution range of the ancestor of the southern clade Ionian Ecoregion, we have analysed the population seems to comprise rivers flowing into the Patraikos genetic structure and evolutionary history of Telestes Gulf. Structures within the two main clades, as well as pleurobipunctatus. Analyses were based on the mito- timing of diversification events are different, implying chondrial gene for cytochrome b from samples separate evolutionary courses. covering the whole distribution range of this species. A high level of intraspecific structuring was revealed Keywords Conservation priorities Á Geological inside T. pleurobipunctatus. Its evolutionary history history Á Mediterranean biodiversity Á Population genetic structure Á Telestes Handling editor: Diego Fontaneto I. Buj (&) J. Freyhof Department of Zoology, Faculty of Science, University of German Centre for Integrative Biodiversity Research Zagreb, Rooseveltov trg 6, 10000 Zagreb, Croatia (iDiv) Halle-Jena-Leipzig, Deutscher Platz 5a, e-mail: [email protected] 04103 Leipzig, Germany R. Sˇanda M. F. Geiger National Museum, Va´clavske´ na´meˇstı´ 68, 115 79 Prague, Zoologisches Forschungsmuseum Alexander Koenig, Czech Republic Adenauerallee 160, 53113 Bonn, Germany S. Zogaris J. Vukic´ Hellenic Centre for Marine Research, Institute of Marine Department of Ecology, Faculty of Science, Charles Biological Sciences and Inland Waters, Athens-Sounio, University, Vinicˇna´ 7, 128 44 Prague, Czech Republic 19013 Anavissos, Attiki, Greece 123 Author's personal copy Hydrobiologia Introduction might have allowed connections among land masses (presumably between Peloponnese, Corfu and other Historical isolation of the Balkan Peninsula from the islands with the mainland), as well as among adjacent remaining parts of Europe, starting from the Oligocene river basins due to lowering of the sea level (Maurakis with the uplift of the Dinarides–Hellenides range, and et al., 2001). continuing during most of the Neogene (Ro¨gl, The Ionian Freshwater Ecoregion, described as 1998, 1999), induced the emergence of many endemic containing high levels of heterogeneity and harbour- species (Economidis & Banarescu, 1991). Diversifi- ing many endemic species (Oikonomou et al., 2014), cation events were furthermore provoked by a com- comprises an area from the extreme southern tip of plex geological history. The southern Balkan Albania to western Greece and most of the Pelopon- Peninsula has been exposed to significant tectonic nese (Zogaris & Economou, 2017). It is characterized events, volcanism and sea level changes from the by typical karstic features, canyons, small lakes and Oligocene onwards (Ro¨gl, 1998). As a consequence of many small river basins (Oikonomou et al., 2014). movements of the African and Anatolian plates during Economidis and Banarescu (1991), as well as the early Miocene (around 23 million years ago; Banarescu (2004) considered the region of the Ionian ¨ MYA) a continuous landmass (so-called Aga¨is) watershed to be a part of the wider Adriatic-Ionian appeared at the northern coast of the Tethys Ocean. Ecoregion; however, Zogaris et al. (2009a) and In the Middle and Late Miocene (around 12–8 MYA) Oikonomou et al. (2014) denote it as a separate tectonic disturbances provoked the break-up of the ecoregion, based on the freshwater fish diversity. The southern Aegean landmass and initiated the modern evolutionary history of the Ionian Ecoregion was biogeographic history of that area (Poulakakis et al., complex, with palaeo-lakes existing in several areas 2005b). In the same time period, the Mid-Aegean (Oikonomou et al., 2014). Some of the boundaries of Trench (MAT) was formed, beginning from the east of this region have still not been defined with certainty Crete and dividing the Aegean into Asian and (Zogaris & Economou, 2017). European sides (Poulakakis et al., 2005b). During There are several studies showing that the complex the latest part of the Messinian (MSC; 5.96–5.3 geological history of the southern Balkans contributed MYA), the level of the Mediterranean Sea dropped to the diversification and shaping of the distribution (so-called Messinian Salinity Crisis; MSC). Accord- areas of many terrestrial animals (Beerli et al., 1996; ing to Bianco (1990), it was subsequently filled with Sfenthourakis & Legakis, 2001; Poulakakis et al., freshwater from the Paratethys so it might have 2003, 2005a) and plants (Dimopoulos et al., 2016). allowed dispersal of freshwater fishes. Even though However, knowledge on the evolutionary history of there is a lack of evidence on the freshwater phase of freshwater fishes, which have different dispersal ways the Mediterranean Sea during the MSC (Roveri et al., than terrestrial animals or plants, is scarce (Economou 2014), some authors recognized MSC as the most et al., 2007). The Balkan Peninsula, with more than important event causing a great level of endemism in 193 native freshwater fish species, has the highest southern Greece (Zardoya & Doadrio, 1999). How- ichthyofaunal species richness in Europe (Oikonomou ever, there is evidence that older events played even a et al., 2014). In the Aegean-Anatolian realm, there are more important role (Perea et al., 2010). Uplift of the evidences of rich fish community from the Early Pindos Mountains was further reported to mark Miocene (Vasileiadou et al., 2017). In the area of division of zoogeographic regions on land, but also Lapsarna (on the Levsos Island), fossils of three the separation of the Aegean and the Ionian water- cyprinid species (Paleoleuciscus sp., Barbus sp. and sheds (Economou et al., 2007). Geologic isolation of Cyprinion sp.) were discovered in lacustrine sedi- the Peloponnese by the sea, presumably also signif- ments and marls of an Early Miocene origin icant for the evolutionary history of various animals, (Vasileiadou et al., 2017). Existence of palaeo-lakes probably occurred 4–3 MYA (Sola et al., 2013)or in the Ionian Ecoregion (Oikonomou et al., 2014), as about 2.5 MYA (Zardoya & Doadrio, 1999; Dubut well as survival of many old fish lineages (Economou et al., 2012). Another event proposed to have shaped et al., 2007) have been reported. recent diversity of the Greek fauna were the Pleis- The fish genus Telestes belongs to the Leuciscidae tocene glaciations (2.58–0.12 MYA). Glaciations family and Leuciscinae subfamily (Scho¨nhuth et al., 123 Author's personal copy Hydrobiologia 2018) and represents a model for investigating the knowledge is important for conservation planning as historical biogeography of European freshwater drai- well. nage systems (Buj et al., 2017). In the south-western Balkans, it is represented with two species: T. pleurobipunctatus (Stephanidis, 1939) and T. beoticus Materials and methods (Stephanidis, 1939) (Kottelat & Freyhof, 2007). Together with Chondrostoma s.l., Phoxinellus and Analyses of T. pleurobipunctatus were based on 114 Pseudophoxinus, Telestes belongs to the linage VI in individuals from 13 localities (number of individuals the molecular phylogeny of the subfamily Leuciscinae per locality = 4–13), covering the whole geographic (Perea et al., 2010).
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