BACKGROUND: The invasive benthic round goby (Neogobius melanostomus) is the most successful temperate invasive fish and has spread in aquatic ecosystems on both sides of the Atlantic. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales and present promising case studies to understand factors involved the impressive ability of some species to colonize novel environments. We seize the unique opportunity presented by the round goby invasion to study genomic substrates potentially involved in colonization success. RESULTS: We report a highly contiguous long-read-based genome and analyze gene families that we hypothesize to relate to the ability of these fish to deal with novel environments. The analyses provide novel insights from the large evolutionary scale to the small species-specific scale. We describe expansions in specific cytochrome P450 enzymes, a remarkably diverse innate immune system, an ancient duplication in red light vision accompanied by red skin fluorescence, evolutionary patterns of epigenetic regulators, and the presence of osmoregulatory genes that may have contributed to the round goby's capacity to invade cold and salty waters. A recurring theme across all analyzed gene families is gene expansions. CONCLUSIONS: The expanded innate immune system of round goby may potentially contribute to its ability to colonize novel areas. Since other gene families also feature copy number expansions in the round goby, and since other Gobiidae also feature fascinating environmental adaptations and are excellent colonizers, further long-read genome approaches across the goby family may reveal whether gene copy number expansions are more generally related to the ability to conquer new habitats in Gobiidae or in fish.

Biocenter University of Basel Klingelbergstrasse 50 70 4056 Basel Switzerland

Centre for Ecological and Evolutionary Synthesis University of Oslo Blindernveien 31 0371 Oslo Norway

Department of Biology McMaster University 1280 Main Street West Hamilton ON Canada

Department of Chemistry and Molecular Biology University of Gothenburg Medicinaregatan 9C 41390 Gothenburg Sweden

Department of Marine Sciences University of Gothenburg Medicinaregatan 9C 41390 Gothenburg Sweden

Department of Zoology Charles University Vinicna 7 12844 Prague Czech Republic

Division of Evolutionary Biology Faculty of Biology Ludwig Maximilians Universität München Grosshaderner Strasse 2 82152 Planegg Martinsried Germany

Genetic Diversity Centre ETH Universitätsstrasse 16 8092 Zurich Switzerland

Institute for Genetics University of Cologne Zülpicher Strasse 47a 50674 Köln Germany

Institute of Evolution and Ecology University of Tuebingen Auf der Morgenstelle 28 72076 Tübingen Germany

Max Planck Institute of Molecular Cell Biology and Genetics Pfotenhauerstrasse 108 01307 Dresden Germany

NBIS Bioinformatics Infrastructure for Life Sciences University of Gothenburg Medicinaregatan 9C 41390 Gothenburg Sweden

Program Man Society Environment Department of Environmental Sciences University of Basel Vesalgasse 1 4051 Basel Switzerland

Research Institute of Molecular Pathology 1030 Vienna Austria

University of Bern Institute for Fish and Wildlife Health Länggassstrasse 122 3012 Bern Austria

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