Hybridization between distant lineages increases adaptive variation during a biological invasion: stickleback in Switzerland

Authors

  • KAY LUCEK,

    1. Aquatic Ecology and Evolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland
    2. Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
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  • DENIS ROY,

    1. Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
    2. Biology Department, Dalhousie University, 1355 Oxford St., Halifax, NS, Canada B3H 9J1
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  • ETIENNE BEZAULT,

    1. Aquatic Ecology and Evolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland
    2. Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
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  • ARJUN SIVASUNDAR,

    1. Aquatic Ecology and Evolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland
    2. Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
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  • OLE SEEHAUSEN

    1. Aquatic Ecology and Evolution, Institute of Ecology & Evolution, University of Bern, Baltzerstrasse 6, CH-3012 Bern, Switzerland
    2. Department of Fish Ecology and Evolution, EAWAG Swiss Federal Institute of Aquatic Science and Technology, Center for Ecology, Evolution and Biogeochemistry, CH-6047 Kastanienbaum, Switzerland
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Kay Lucek, Fax: +41 3163 14511;
E-mail: kay.lucek@eawag.ch

Abstract

The three-spined stickleback is a widespread Holarctic species complex that radiated from the sea into freshwaters after the retreat of the Pleistocene ice sheets. In Switzerland, sticklebacks were absent with the exception of the far northwest, but different introduced populations have expanded to occupy a wide range of habitats since the late 19th century. A well-studied adaptive phenotypic trait in sticklebacks is the number of lateral plates. With few exceptions, freshwater and marine populations in Europe are fixed for either the low plated phenotype or the fully plated phenotype, respectively. Switzerland, in contrast, harbours in close proximity the full range of phenotypic variation known from across the continent. We addressed the phylogeographic origins of Swiss sticklebacks using mitochondrial partial cytochrome b and control region sequences. We found only five different haplotypes but these originated from three distinct European regions, fixed for different plate phenotypes. These lineages occur largely in isolation at opposite ends of Switzerland, but co-occur in a large central part. Across the country, we found a strong correlation between a microsatellite linked to the high plate ectodysplasin allele and the mitochondrial haplotype from a region where the fully plated phenotype is fixed. Phylogenomic and population genomic analysis of 481 polymorphic amplified fragment length polymorphism loci indicate genetic admixture in the central part of the country. The same part of the country also carries elevated within-population phenotypic variation. We conclude that during the recent invasive range expansion of sticklebacks in Switzerland, adaptive and neutral between-population genetic variation was converted into within-population variation, raising the possibility that hybridization between colonizing lineages contributed to the ecological success of sticklebacks in Switzerland.

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