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Anthropogenic Hybridization Between Endangered Evolutionary Applications Evolutionary Applications ISSN 1752-4571 ORIGINAL ARTICLE Anthropogenic hybridization between endangered migratory and commercially harvested stationary whitefish taxa (Coregonus spp.) Jan Dierking,1 Luke Phelps,1,2 Kim Præbel,3 Gesine Ramm,1,4 Enno Prigge,1 Jost Borcherding,5 Matthias Brunke6 and Christophe Eizaguirre1,* 1 Research Division Marine Ecology, Research Unit Evolutionary Ecology of Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, Kiel, Germany 2 Department of Evolutionary Ecology, Max Planck Institute for Evolutionary Biology, Plon,€ Germany 3 Department of Arctic and Marine Biology, Faculty of Biosciences Fisheries and Economics, University of Tromsø, Tromsø, Norway 4 Faculty of Science, University of Copenhagen, Frederiksberg, Denmark 5 General Ecology & Limnology, Ecological Research Station Grietherbusch, Zoological Institute of the University of Cologne, Cologne, Germany 6 Landesamt fur€ Landwirtschaft, Umwelt und landliche€ Raume€ (LLUR), Flintbek, Germany * Present address: School of Biological and Chemical Sciences, Queen Mary University of London, London, UK Keywords Abstract admixture, anadromous fish, conservation, evolutionarily significant unit, gill raker, Natural hybridization plays a key role in the process of speciation. However, introgression, stocking anthropogenic (human induced) hybridization of historically isolated taxa raises conservation issues. Due to weak barriers to gene flow and the presence of endan- Correspondence gered taxa, the whitefish species complex is an excellent study system to investi- Jan Dierking, Research Division Marine gate the consequences of hybridization in conservation. We focused on three Ecology, Research Unit Evolutionary Ecology of naturally reproductively isolated whitefish taxa in Germany: the endangered, Marine Fishes, GEOMAR Helmholtz Centre for Ocean Research, 24105 Kiel, Germany. anadromous North Sea houting (NSH) and Baltic houting (BH), which were Tel.: +49 431 600 4580; reintroduced after local extinction, and the commercially stocked European fax: +49 431 600 4553; whitefish (EW). To evaluate the genetic integrity of each taxon, source and rein- e-mail: [email protected] troduced populations of NSH and BH, and EW populations were characterized based on two mitochondrial and 17 microsatellite loci. Additionally, we investi- Received: 2 January 2014 gated gill raker counts as an adaptive phenotypic trait. Even though clear genetic Accepted: 30 March 2014 and phenotypic differentiation confirmed the houtings as separate evolutionarily doi:10.1111/eva.12166 significant units, admixture analyses revealed an extensive hybrid zone. Hybrid- izations were introgressive, positively correlated with genetic diversity, and were reflected in the gill raker counts. The BH distribution range showed higher heter- ogeneity and stronger admixture than the NSH range. Erroneous stocking with non-native genotypes best explained these patterns, which pose challenges for the conservation of the endangered NSH and BH. translocations by humans (Allendorf et al. 2001). Particu- Introduction larly, translocation by stocking (i.e., the release of fry reared The present age has been coined ‘the sixth extinction’ (Lea- in hatcheries) can serve to reintroduce endangered species key and Lewin 1996), as current extinction rates driven by or to increase their population sizes. On the other hand, it anthropogenic impacts rival those of the five previous mass can also introduce non-native species or strains that subse- extinction events on earth. The conservation status of diad- quently can hybridize with native taxa and may affect the romous fishes in Europe is a dramatic example, where one- fitness of wild populations (Consuegra and Garcia de Lean- third are classified as endangered (Kottelat and Freyhof iz 2008; Araki et al. 2009; Hansen et al. 2009). 2007). Cryptic drivers contributing to biodiversity loss are The role of hybridization in conservation is a dilemma: introgressive hybridization and reverse speciation (Seehau- Whereas natural hybridization plays an important evolu- sen 2006) associated with habitat modifications and species tionary role in the process of speciation and the 1068 © 2014 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Dierking et al. Hybridization in endangered whitefish maintenance of biodiversity (Dowling and Secor 1997; Nol- three historically geographically isolated whitefish taxa via te and Tautz 2009), hybridization induced by human activ- two possible mechanisms: (i) Anthropogenic translocations ities can be considered as harmful as it threatens the outside the historic ranges by erroneous stocking, which integrity of ancestral species and has contributed directly or could then be followed by diffusion from short-range indirectly to species extinctions (Rhymer and Simberloff migrations, termed ‘stepping stone and diffusion’ (Gozlan 1996). Allendorf et al. (2001) framed the potential out- et al. 2010) and (ii) migrations via the man-made invasion comes of such anthropogenic hybridizations into three corridor created by the Kiel Canal connecting the North clearly determined categories: (i) hybridization without Sea and the Baltic Sea (Gollasch and Rosenthal 2006). The introgression (sterile F1s only), (ii) widespread introgres- houtings have received recent scientific attention, including sion, and (iii) complete admixture, which can result in studies on evolutionary history (Østbye et al. 2005; Jacob- reverse speciation (Seehausen 2006). Each case poses differ- sen et al. 2012), taxonomy (Freyhof and Schoter€ 2005), ent conservation challenges, ranging from wasted repro- conservation genetics in Danish locations (Hansen et al. ductive effort due to sterile F1s under (i) to the loss of 2006, 2008), and ecology (Borcherding et al. 2006, 2008, parental lines under (iii) (Allendorf et al. 2001). 2014; Jepsen et al. 2012). Yet, the presence of hybridiza- The recent postglacial origin of the whitefish species tions between these taxa, and the maintenance of genetic complex (Coregonidae) has resulted in porous barriers to integrity in this system, remains to be investigated. This is gene flow (Østbye et al. 2005; Præbel et al. 2013a), and surprising considering the porous reproductive barriers natural (Schluter 1996) and anthropogenic hybridizations within the whitefish species complex. It is also remarkable (Winkler et al. 2011; Bhat et al. 2014) are frequently when considering ongoing large-scale conservation efforts observed. In Northern Germany, two endangered native that would benefit from this information, including a €14 anadromous whitefish taxa of considerable conservation million EU LIFE project focused on the NSH in Denmark interest exist (IUCN 2013): the North Sea houting (NSH) (Hansen 2006), and large investments in the continuous (Coregonus oxyrinchus or Coregonus maraena, depending stocking of German locations. on the author) and the Baltic houting (BH) (Coregonus lav- Here, we assessed the contemporary history of the two aretus or C. maraena; Freyhof and Schoter€ 2005; Borcherd- endangered houting taxa and the fishery important EW ing et al. 2010). Both taxa are evolutionarily young lineages across the German range, based on two mitochondrial as they diverged only after the last glaciations, and their (mtDNA) and 17 microsatellite loci. We also assessed gill species and taxonomic designation is still under debate raker counts (GRCs), which represent a meristic trait (Jacobsen et al. 2012). However, Hansen et al. (2008) pro- related to feeding ecology (Amundsen et al. 2004; Kahilai- vided evidence that NSH and BH represent separate evolu- nen and Østbye 2006) that is influenced by diversifying tionarily significant units (ESUs), that is, groups of selection (Præbel et al. 2013a) and commonly used in organisms to be considered distinct for conservation pur- whitefish taxonomy. In light of the controversy regarding poses. Throughout this manuscript, we therefore simply the taxonomic and ESU status of houtings, our objectives refer to ‘taxa’ and additionally use the term ‘ESU’ in a con- were to (i) investigate the genotypic and phenotypic integ- servation context. The respective natural ranges of the NSH rity of NSH, BH, and EW, (ii) characterize the population and BH were the North Sea and Baltic Sea and, during the genetic structure of this young system, (iii) where present, reproductive period, the rivers in the hydrographically iso- assess the geographic patterns of hybridizations and their lated drainage basins of these two seas (Jacobsen et al. potential underlying anthropogenic drivers (e.g., stocking 2012). Historically, the houtings sustained fisheries in the or the opening of Kiel Canal), and (iv) assess the evolution- Netherlands, Germany, and Denmark (Thienemann 1922; ary and conservation implications of these findings and Jennerich and Schulz 2011), but faced extinction by the provide recommendations for science-based conservation 1970s due to habitat loss, construction of migration barri- of the endangered NSH and BH in Germany. ers, pollution, and overfishing (Hansen et al. 1999). Since then, conservation programs based on reintroduction by Material and methods stocking from remnant indigenous source populations have led to the return of the NSH (J€ager 1999; Jepsen et al. History of the
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