Genetic variation in brown trout Salmo truttaacross the Danube, Rhine, and Elbe headwaters: a failure of the phylogeographic paradigm?

Abstract

BackgroundBrown trout Salmo trutta have been described in terms of five major mtDNA lineages, four of which correspond to major ocean basins, and one, according to some authors, to a distinct taxon, marbled trout Salmo marmoratus. The Atlantic and Danubian lineages of brown trout meet in a poorly documented contact zone in Central Europe. The natural versus human mediated origin of the Atlantic lineage in the upper Danube is a question of both theoretical and practical importance with respect to conservation management. We provide a comprehensive population genetic analysis of brown trout in the region with the aim of evaluating the geographic distribution and genetic integrity of these two lineages in and around their contact zone.ResultsGenetic screening of 114 populations of brown trout across the Danube/Rhine/Elbe catchments revealed a counter-intuitive phylogeographic structure with near fixation of the Atlantic lineage in the sampled portions of the Bavarian Danube. Along the Austrian Danube, phylogeographic informative markers revealed increasing percentages of Danube-specific alleles with downstream distance. Pure Danube lineage populations were restricted to peri-alpine isolates within previously glaciated regions. Both empirical data and simulated hybrid comparisons support that trout in non-glaciated regions north and northeast of the Alps have an admixed origin largely based on natural colonization. In contrast, the presence of Atlantic basin alleles south and southeast of the Alps stems from hatchery introductions and subsequent introgression. Despite extensive stocking of the Atlantic lineage, little evidence of first generation stocked fish or F1 hybrids were found implying that admixture has been established over time.ConclusionsA purely phylogeographic paradigm fails to describe the distribution of genetic lineages of Salmo in Central Europe. The distribution pattern of the Atlantic and Danube lineages is extremely difficult to explain without invoking very strong biological mechanisms.The peri-alpine distribution of relict populations of pure Danubian lineage brown trout implies that they colonized headwater river courses post-glacially ahead of the expansion of the Atlantic lineage. The recognition of natural as opposed to anthropogenic introgression of the Atlantic lineage into Danubian gene pools is of fundamental importance to management strategies.

Selection and genetic drift in captive versus wild populations: an assessment of neutral and adaptive (MHC-linked) genetic variation in wild and hatchery brown trout (Salmo trutta) populations

“…Whereas some tissue samples are identical to those used in Lerceteau-Köhler et al (2013), sample sizes were increased in 2012 and 2013 using non-invasive tissue sampling during standard electrofishing monitoring, approved by the local responsible authorities. The three wild populations (Etrachbach-ETR, Lohnbach-LOH and Wolfsgrabenbach-WOL) represent the native Danubian lineage with no sign of introgression from foreign sources (Lerceteau-Köhler et al 2013;Schenekar et al 2014). Etrachbach and Wolfsgrabenbach are in the southern provinces of Austria (Styria and Carinthia), whereas Lohnbach lies in Lower Austria, a province northeast of the Alps.…”

“…Genetic studies on Austrian brown trout have shown that stocked hatchery fish are mainly of the Atlantic mtDNA lineage whereas limited numbers of native populations were found to consist mainly of Danubian mtDNA lineage fish (Bernatchez 2001;Lerceteau-Köhler et al 2013).…”

“…Rhine or Elbe), the Danubian and Atlantic lineages existed largely in allopatry before human stocking activities began (Lerceteau-Köhler et al 2013). The natural range of the Danubian lineage encompasses the drainages of the Black, Caspian, Azov and Aral seas, reaching from Bavaria, Germany (upper Danube) to eastern tributaries of the Aral Sea in Afghanistan and Pakistan.…”

Haplotype diversity of brown trout Salmo trutta (L.) in the broader Iron Gate area

“…For this reason, only brown trout with the Da haplotypes are considered indigenous in this region, while the occurrence of other lineages is considered a consequence of introduction (Bernatchez et al, 1992;Bernatchez, 2001;Duftner et al, 2003;Snoj, 2004;Marić et al, 2006). Although there are some disagreements about the modes of settlement of Atlantic populations in Austrian Danube drainages (Balon, 1968;Weiss et al, 2001;Lerceteau-Kohler et al, 2013), there is no evidence of the natural occurrence of this lineage south and southeast of the Alps. This is supported by the fact that Romanian rivers are exclusively inhabited by brown trout of the Danubian lineage (Popa et al, 2013).…”

“…In addition to these, Bardakci et al (2006) proposed a seventh, the Tigris lineage, from the Tigris River basin in southeastern Anatolia. Lerceteau-Kohler et al (2013) questioned the allopatric origin of the Mediterranean lineage, suggesting the possibility of independent origin in particular (e.g., Adriatic) mtDNA lineages with respect to both their broad dispersal range and phenotypic divergence, and emphasized that brown trout of the Danubian lineage exhibit extensive life-history diversity and stretch across the entire Ponto-Caspian basin, leaving some uncertainty about where the lineage actually arose as well as its significance related to evolutionary or taxonomic debate. In Serbia and the Balkans, the most common brown trout are those of the Da mtDNA lineage.…”