Genome Wide Analysis Reveals Genetic Divergence Between
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Jansson et al. BMC Genetics (2020) 21:118 https://doi.org/10.1186/s12863-020-00921-8 RESEARCH ARTICLE Open Access Genome wide analysis reveals genetic divergence between Goldsinny wrasse populations Eeva Jansson1* , Francois Besnier1, Ketil Malde1, Carl André2, Geir Dahle1 and Kevin A. Glover1,3 Abstract Background: Marine fish populations are often characterized by high levels of gene flow and correspondingly low genetic divergence. This presents a challenge to define management units. Goldsinny wrasse (Ctenolabrus rupestris) is a heavily exploited species due to its importance as a cleaner-fish in commercial salmonid aquaculture. However, at the present, the population genetic structure of this species is still largely unresolved. Here, full-genome sequencing was used to produce the first genomic reference for this species, to study population-genomic divergence among four geographically distinct populations, and, to identify informative SNP markers for future studies. Results: After construction of a de novo assembly, the genome was estimated to be highly polymorphic and of ~600Mbp in size. 33,235 SNPs were thereafter selected to assess genomic diversity and differentiation among four populations collected from Scandinavia, Scotland, and Spain. Global FST among these populations was 0.015–0.092. Approximately 4% of the investigated loci were identified as putative global outliers, and ~ 1% within Scandinavia. SNPs showing large divergence (FST > 0.15) were picked as candidate diagnostic markers for population assignment. One hundred seventy-three of the most diagnostic SNPs between the two Scandinavian populations were validated by genotyping 47 individuals from each end of the species’ Scandinavian distribution range. Sixty-nine of these SNPs were significantly (p < 0.05) differentiated (mean FST_173_loci = 0.065,FST_69_loci = 0.140). Using these validated SNPs, individuals were assigned with high probability (≥ 94%) to their populations of origin. Conclusions: Goldsinny wrasse displays a highly polymorphic genome, and substantial population genomic structure. Diversifying selection likely affects population structuring globally and within Scandinavia. The diagnostic loci identified now provide a promising and cost-efficient tool to investigate goldsinny wrasse populations further. Keywords: Assignment, Ctenolabrus rupestris, Marker validation, Population genomics, Resequencing, SNP Background [22]. For the conservation and management of wild pop- Thanks to the rapid development of whole-genome se- ulations, studies employing high-throughput sequencing quencing methods during the last decade [36, 93], gen- technologies may provide better estimates than trad- ome wide data is now relatively cost-effective to produce itional population genetics tools for key parameters such and is becoming increasingly commonplace to study as effective population size, genetic structure, and con- evolutionary questions even for non-model organisms nectivity (for reviews, see [2, 85]). Greater resolution from using large numbers of genetic markers and/or by pre-selection of highly divergent markers (i.e., outliers) is * Correspondence: [email protected] 1Institute of Marine Research, P. O. Box 1870, Nordnes, 5817 Bergen, Norway especially useful in population genetic studies of marine Full list of author information is available at the end of the article organisms [33, 83] which are often characterized by very © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Jansson et al. BMC Genetics (2020) 21:118 Page 2 of 15 large census sizes and high levels of connectivity leading reduction in population densities might even lead to cas- to generally low levels of population divergence [43]. cade effects in the coastal ecosystems. Overexploitation However, because the efficiency of natural selection is also increases the risk of loss of genetic variation and dependent on the (effective) population size [1, 17], potentially locally adaptive variants (e.g. [1]). Genetic in- adaptive genetic differences are possible – or even likely tegrity and adaptability of local populations can also be – in large marine populations inhabiting heterogeneous compromised via manmade gene flow from genetically environments [7, 10, 39]. Therefore, finding biologically diverged populations. This concern is of particular im- meaningful differences among populations, and the pos- portance in fisheries management where large-scale sible genetic factors underlying these differences, will population augmentations through deliberate or inad- help define appropriate management units, and thus sus- vertent releases of translocated, captively raised or do- tainably exploit marine species. Better detection and un- mesticated individuals occurs [35, 59, 95]. Wild derstanding of human-mediated introgression [20], a populations of wrasses are not intentionally augmented common problem in many wild fish populations (e.g. but receive human-mediated gene flow via large-scale [12, 34, 60, 75]), is also of high conservation priority, translocations and release or escape of wrasse from fish and now more feasible with the modern sequencing farms [13, 29]. methods at hand. Given the current practise of using cleaner wrasses in Goldsinny wrasse, Ctenolabrus rupestris, is a small (< great numbers, and the associated heavy fishing pressure 18 cm) inshore marine fish belonging to the Labridae placed on wild populations [41], more knowledge of the family that includes over 500 described species world- population genetic structure of wrasses is required. Thus wide. It is a common species in the Eastern Atlantic far, the best-studied of these species is the corkwing coastal waters from Morocco to Norway, and is also wrasse (Symphodus melops) which displays clear popula- found in the Mediterranean and Black Sea. Traditionally, tion subdivisions on different geographic scales [14, 57, goldsinny wrasse had no commercial value and thus 71, 82]. Genetic studies of ballan wrasse (Labrus ber- avoided significant exploitation [26, 41]. However, in re- gylta) have concentrated on investigation of population sponse to its increasing demand as a cleaner-fish in the structure on large geographic scales [4, 21], and on gen- aquaculture industry for delousing cage-reared Atlantic etic divergence of different morphotypes [3, 80]. A newly salmon (Salmo salar) and rainbow trout (Oncorhynchus published study by Seljestad et al. [84] revealed subdiv- mykiss), the species is now extensively harvested to- ision on a more local scale as well, dividing the Scandi- gether with other wrasse species [89]. The demand for navian ballan wrasse population into two distinct genetic cleaner fish in the aquaculture industry has grown al- clusters. An early genetic study of goldsinny wrasse with most exponentially after 2007 [88, 89] due to emerged allozyme markers showed significant differences between resistance to delousing agents of the salmon louse the southern and mid-Norway [92]. The only recent (Lepeophtheirus salmonis)[11, 54]. In Norway alone, ~ study, using a combination of 14 microsatellite and 36 20 million wrasses were caught in 2014–2019 and used SNP markers [47], revealed clear population divergence in commercial aquaculture. Between 8 to 12 million of (FST ~ 0.02–0.05) across the North Sea but only modest these were goldsinny wrasses, which together with differences (FST ≤ 0.02) that increased with geographic corkwing wrasse makes them the numerically most sig- distance (i.e. isolation-by-distance, IBD) within Scandi- nificant of the wild-captured cleaner fish used. In navian populations. These patterns are concordant with addition to wrasses caught in local waters, Norwegian restricted migration and gene flow as the main factor salmon farms received wrasses caught from the Swedish creating genetic patterns for the species but does not west coast (about a million fish per year [72];). The high rule out other possible factors such as selection and/or fishing pressure combined with the high breeding-site demographic history shaping the population structures philopatry of goldsinny wrasse [44], and their slow seen today (see e.g. [71]). In addition, aquaculture- growth rate (4–5 years for minimum commercial size of mediated translocation of wrasses might affect both the 11 cm [88];) indicate that this species is likely to be sen- donor and the recipient population. The primary area to sitive to overexploitation. A study by Halvorsen et al. move wrasses is mid-Norway where there are plenty of [41]