Abstract

BackgroundThe 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.ResultsWe 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.ConclusionsThe 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.

Highlights

  • Since the beginning of global trade and the colonial period, hundreds of species have colonized territories outside their native range

  • The choice of outgroup does not affect the position of the LWS2 gene. These analyses suggest either (1) the presence of an ancient gene duplication event of the long-wavelength sensitive (LWS) gene in the ancestor of teleost and holostean fishes (i.e., Neopterygii) which was retained only in the goby family, or (2) a teleost-specific event, possibly identical to that reported for characins and bony tongues [67], with a subsequent concerted goby-specific sequence diversification in exons 2, 3, and 5

  • We find that round goby, and mudskippers, feature an interesting distribution of Na+/Cl- co-transporters to subgroups; while most zebrafish (Danio rerio) and nile tilapia (Oreochromis niloticus) Na+/Cl- co-transporters belong to the NKCC1 subgroup, Gobiidae feature more genes in the NKCC2 subgroup (Fig. 7)

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Summary

Introduction

Since the beginning of global trade and the colonial period, hundreds of species have colonized territories outside their native range. While invasive species present challenges for biodiversity and ecosystem conservation, they constitute exciting eco-evolutionary models for survival in and adaptation to novel or changing environments [1,2,3,4]. The benthic round goby Neogobius melanostomus (Fig. 1a) is a member of Percomorpha/Gobiiformes (Fig. 1b) and one of the most widespread invasive fish species. 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

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