Evolved for success in novel environments: The round goby genome

Since the beginning of global trade, hundreds of species have colonized territories outside of their native range. Some of these species proliferate at the expense of native ecosystems, i.e., have become invasive. Invasive species constitute powerful in situ experimental systems to study fast adaptation and directional selection on short ecological timescales. They also present promising case studies for ecological and evolutionary success in novel environments. We seize this unique opportunity to study genomic substrates for ecological success and adaptability to novel environments in a vertebrate. We report a highly contiguous long-read based genome assembly for the most successful temperate invasive fish, the benthic round goby (Neogobius melanostomus), and analyse gene families that may promote its impressive ecological success. Our approach provides 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 in epigenetic regulators, and the presence of 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 are gene expansions. This suggests that gene duplications may promote ecological flexibility, superior performance in novel environments, and underlie the impressive colonization success of the round goby. Gobiidae generally feature fascinating adaptations and are excellent colonizers. Further long-read genome approaches across the goby family may reveal whether the ability to conquer new habitats relates more generally to gene copy number expansions.


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Since the beginning of global trade and the colonial period, hundreds of species have colonized 63 territories outside their native range. A fraction of those species proliferates at the expense of native 64 species and ecosystems, i.e., they are invasive. While invasive species present challenges for

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The spectral sensitivity of photopigments, i.e. their excitation wavelength can be modified by 242 substitutions in certain key amino acids (Yokoyama, 2008). We find that round goby LWS1 and LWS2 243 differ in the key spectral tuning site at amino acid 277 (position 261 of bovine rhodopsin, Table 2) 244 suggesting a sensitivity shift of 10 nm.

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To find a possible link to the ecological significance of the red opsin duplication, we checked for the 247 presence of red skin fluorescence in the round goby. Interestingly, round goby individuals of both 248 sexes and of all sizes (n=10) feature weakly red fluorescent crescents above the eyes (Figure 3).

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Whether such pattern has any relevance for the putatively enhanced vision in the red spectrum

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CYP8, and CYP39 genes as CYP8 is unlikely given the colocalization and high sequence similarity.

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The function of the expansion is presently unclear, although expression patterns in zebrafish suggest

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Finally, fish produce osmolytes to actively take up and retain water. In particular, the cyclic polyol myo-424 inositol is used by euryhaline teleosts to acclimate to high salinity. Two enzymes are required for its It has been speculated that invasion success may relate to the ability to fight novel immune challenges 437 (Lee and Klasing, 2004). We therefore characterized key genes related to the immune system,

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focusing on genes that span both the innate and adaptive immune system such as pattern recognition

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We find that the round goby genome features a classical adaptive immunity setup ( Table 3).     conserved across vertebrates, and most vertebrate genomes contain one to three copies of each type.

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As expected for a teleost, the round goby genome does not contain the LPS-detecting TLR4 genes.

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However, in total we find 56 TLRs, of which 40 appear to originate from an expansion of Toll-Like

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Receptor 23-like genes (Figure 9). Small expansions of specific TLRs are somewhat common in fish

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When rooting with Australian ghost shark, teleost EZH2 genes cluster with EZH1 (data not shown).

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Round goby is indicated in orange.

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America, and the ability to accumulate osmolytes may impact its range expansion in three ways.

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Firstly, 0-25 PSU (common for coastal waters, but lower than the ocean) is the species' current limit

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We find that the round goby genome contains multiple copies of genes for inflammasome assembly, 741 activation, and function. This is interesting because the fish inflammasome complex is much more

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In order to assess the completeness and quality of the current assembly and the associated gene 918 models, the assembly and the predicted protein sequences were run against reference sets at two   the identification of repeats with RepeatModeler (as described above), we used TRF (Benson, 1999) 1188 to predict tandem repeats. RepeatMasker (Smit et al. 2013(Smit et al. -2015, a homology-based approach was 1189 used to produce a genome-wide overview of interspersed repeats. LTR Finder (Xu and Wang, 2007)

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Various Illumina reads are available under the accessions indicated in Table 1.