Phylogeography of Bleaks Alburnus Spp. (Cyprinidae) in Italy, Based on Cytochrome B Data

Journal of Fish Biology (2009) 75, 997–1017 doi:10.1111/j.1095-8649.2009.02357.x, available online at www.interscience.wiley.com Phylogeography of bleaks Alburnus spp. (Cyprinidae) in Italy, based on cytochrome b data V. Ketmaier*†, F. Finamore‡, C. Largiader§,` M. Milone‡ and P. G. Bianco‡ *Unit of Evolutionary Biology–Systematic Zoology, Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Strasse 24-25, Haus 25, D-14476, Potsdam, Germany, ‡Department of Zoology, University of Naples, via Mezzocannone 8, I-80134 Naples, Italy and §University Hospital, University of Bern, Inselspital, CH-3010 Bern, Switzerland (Received 29 January 2009, Accepted 13 May 2009) Sequence variation of a fragment of the mitochondrial DNA encoding for the cytochrome b gene was used to reconstruct the phylogeography of the two species of bleaks occurring in Italy: the alborella Alburnus arborella in northern Italy and the vulturino Alburnus albidus in southern Italy. The study includes four populations of the alborella and 14 populations of the vulturino. A total of 57 haplotypes were identified; these could not be sorted into two reciprocally monophyletic clusters. Multiple phylogenetic methods and nested clade phylogeographical analysis consistently retrieved three well-supported clades, two of which contained both Northern and Southern Italian haplotypes. A third clade is limited to southern Italy. This clade is tentatively assigned to the vulturino. The placement in the same clade of northern and southern Italian haplotypes is explained in light of the introductions of fishes operated from northern to central and southern Italy. The origin of the vulturino dates back to the last two million years. This divergence time estimate identifies the Pleistocene confluences between adjacent river basins along the Adriatic slope of the Italian peninsula and their subsequent isolation as the cause that triggered the diversification of the genus in the area. The existence of a clade endemic to southern Italy supports the recognition of the area as a new peri-Mediterranean ichthyogeographic district, the borders of which correspond to the northern and southern edges of the vulturino range. © 2009 The Authors Journal compilation © 2009 The Fisheries Society of the British Isles Key words: Alburnus; Cyprinidae; Italian peninsula; mitochondrial DNA; phylogeography. INTRODUCTION Italy, like several other peri-Mediterranean countries, hosts a distinctive assemblage of primary freshwater fishes, mostly cyprinids. This has led to the recognition of two ichthyogeographic districts in the country, a Padano-Venetian district (north of Apennines) and a Tuscano-Latium district (south of Apennines from River Arno to River Tiber along the Tyrrhenian slope of central Italy; Fig. 1) (Bianco, 1987). The two districts can be clearly distinguished on the basis of their respective primary freshwater fish fauna. Conversely, very little is known on the freshwater fish fauna †Author to whom correspondence should be addressed. Tel.: +49 331 9775604; fax: +49 331 977 5070; email: [email protected] 997 © 2009 The Authors Journal compilation © 2009 The Fisheries Society of the British Isles 998 (b) 13 Journal compilation 11 Southern Italy 12 10 1-Alento River 9 2-Badolato River (a) 3-Palistro River Tyrrhenian slope 8 PV 4-Fiumarella River © 5 2009 The Fisheries Society of the British Isles, 5-Ripiti River 1 2 3 6 7 4 6-Bussento River TL 7-Sinni River 8-Basento River Ionian slope V. KETMAIER 9-Ofanto River (c) 10-Carapelle River 11-Fortore River Adriatic slope 12-Biferno River 13-Treste River ET AL 16 Padano–Venetian district . Journal of Fish Biology 14 15 14-Adda River 15-Ticino River 16-Maggiore Lake 17 17-Meletta Stream © 2009, 2009 The Authors 75 Fig. 1. (a–c) Schematic maps showing ranges of the alborella Alburnus arborella, original distribution in grey, areas of introduction in pale red (see Introduction for details) , 997–1017 and of the vulturino Alburnus albidus, green; dashed lines indicate the Padano–Venetian (PV) and Tuscano-Latium (TL) district (Bianco, 1995a)–(a) Sampling localities for A. albidus (from 1 to 13; each locality identified by a different colour)–(b) Sampling localities for A. arborella (from 14 to 17; each locality identified by the same shade of grey)–(c) Slopes of the sampled Southern Italian rivers are also indicated. Population numbers are as in Table I. PHYLOGEOGRAPHY OF THE GENUS ALBURNUS IN ITALY 999 of Southern Italy. This lack of knowledge is due to a combination of historical factors (ichthyological researches had focused mainly on central and northern Italy) and environmental conditions. Southern Italy is the poorest drained area of the peninsula; river basins exhibit a typical Mediterranean hydrological regime with wide seasonal and annual fluctuations (Bianco, 1995a). In addition, for nearly 100 years from the end of the 19th century, official massive translocations of fishes were made from northern to central and southern Italy (Bianco, 1995a). This practice has superseded the original fish fauna composition, rendering the recognition of the authochthonous southern Italian fish fauna extremely difficult. Only five cyprinid species have been consistently reported for southern Italian rivers, such as the Apennine barbel Barbus tyberinus Bonaparte, the Italian chub Squalius cephalus squalius (L.), the vairone Telestes muticellus (Bonaparte), the loach Cobitis zanandrei Cavicchioli and the vulturino Alburnus albidus (Costa). Historical records tracking translocations of the first two species across the Italian peninsula render their autochthonous occurrence in the area that is very dubious (Bianco, 1995a,b). Conversely, the other species have very limited ranges with A. albidus being by far the most widespread. In particular, Rivers Volturno and Sinni–Alento mark, respectively, the northern and southern edges of the range of A. albidus (Fig. 1) (Bianco, 1980, 1987; Kottelat, 1997). Alburnus albidus is a warm-adapted, preferentially lacustrine species, typical of the lower section of rivers; it prefers small, shallow, well-oxygenated streams, with aquatic and riparian vegetation, coarse substrata and medium to low or standing flow. The species is currently classified as vulnerable in the IUCN Red List. Indeed, its abundance has been declining steadily in the last 20 years as a consequence of habitat alteration by impoundment and waste discharge, river regulation, introduction of exotic competitive species and hybridization with S. cephalus (Bianco, 1982, 1995a). The Italian fauna includes a second representative of the genus Alburnus, the alborella Alburnus arborella (Bonaparte). Taxonomy of this species has been controversial since the end of the 19th century. Alburnus arborella has been alter- natively considered a subspecies of A. albidus or of the European bleak Alburnus alburnus (L.); only recently the name A. arborella has been formally validated (Kot- telat & Bianco, 2005). The species was originally endemic to the Padano–Venetian district, but it has been largely transplanted into the Tuscano–Latium district (Fig. 1) following the practice to stock central Italian rivers with fishes of northern Italian origin (Bianco, 1995b). No precise data are available on whether and to what extent A. arborella might have been introduced south of the Tiber River. Should this be the case it would represent a further threat for the survival of the A. albidus because of possible hybridization and competition between the two species (Bianco, 1995a). The aims of this study were to produce a comprehensive phylogeographic hypoth- esis for the vulnerable A. albidus throughout its entire geographical range. Hence, 141 individuals from 13 southern Italian rivers (six flowing into the Tyrrhenian Sea, two flowing into the Ionic Sea and five flowing into the Adriatic Sea; Fig. 1) were collected. The sampling covers the entire species range (Bianco, 1980). Each indi- vidual included in the study was screened for sequence polymorphisms of a fragment of 565 base pairs (bp) of the mitochondrial DNA (mtDNA) region encoding for the cytochrome b gene (cyt b). This gene has proven useful in phylogeographic studies on cyprinids (Ketmaier et al., 2004, 2008a and references therein). This is the first molecular study based on an extensive sampling of an endemic Southern Italian © 2009 The Authors Journal compilation © 2009 The Fisheries Society of the British Isles, Journal of Fish Biology 2009, 75, 997–1017 1000 V. KETMAIER ET AL. cyprinid species; it thus might shed light on the tempo and mode of diversification of the strictly freshwater fauna of the area. Second, given the vagaries on the taxo- nomic status of A. alborella, reciprocal monophyly at the cyt b level of Northern and Southern Italian bleaks was tested preliminarily in this study. To this aim, four populations (29 individuals) of the alborella from three tributaries of the Po River and from the Maggiore Lake (Fig. 1) were included in the study. Warm-adapted, preferentially lacustrine species such as those considered in the present study can only exploit coalescences of rivers on lowlands to disperse (Bianco, 1995b;Ketmaieret al., 2004). These occurred intermittently at every Quaternary glacial maximum as a consequence of the global lowering of sea level. Coalescences were particularly pronounced along the Adriatic coast of the Italian peninsula due to the southward extension of the Po River (Bianco, 1995b). They allowed warm-water-adapted species to surmount the geographical barrier represented

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