Tench (Tinca tinca L.) has great economic potential due to its high rate of fecundity and long-life span. Population genetic studies based on allozymes, microsatellites, PCR-RFLP and sequence analysis of genes and DNA fragments have revealed the presence of Eastern and Western phylogroups. However, the lack of genomic resources for this species has complicated the development of genetic markers. In this study, the tench transcriptome and genome were sequenced by high-throughput sequencing. A total of 60,414 putative SNPs were identified in the tench transcriptome using a computational pipeline. A set of 96 SNPs was selected for validation and a total of 92 SNPs was validated, resulting in the highest conversion and validation rate for a non-model species obtained to date (95.83%). The validated SNPs were used to genotype 140 individuals belonging to two tench breeds (Tabor and Hungarian), showing low (FST = 0.0450) but significant (<0.0001) genetic differentiation between the two tench breeds. This implies that set of validated SNPs array can be used to distinguish the tench breeds and that it might be useful for studying a range of associations between DNA sequence and traits of importance. These genomic resources created for the tench will provide insight into population genetics, conservation fish stock management, and aquaculture.

Department of Aquaculture and Ecophysiology Leibniz Institute of Freshwater Ecology and Inland Fisheries Berlin Germany

Department of Computer Science and Artificial Intelligence University of the Basque Country UPV EHU San Sebastian Gipuzkoa Spain

Department of Genetics Physical Anthropology and Animal Physiology University of the Basque Country UPV EHU Leioa Bilbao Bizkaia Spain

IKERBASQUE Basque Foundation for Science Bilbao Bizkaia Spain

Research Institute of Fish Culture and Hydrobiology South Bohemian Research Center of Aquaculture and Biodiversity of Hydrocenoses Faculty of Fisheries and Protection of Waters University of South Bohemia in Ceske Budejovice Czech Republic

Zobrazit více v PubMed

Linhart O, Rodina M, Kocour M, Gela D. Insemination, fertilization and gamete management in tench, Tinca tinca (L.). Aquacult Int. 2006;14(1–2):61–73.

Wolnicki J, Kaminski R, Sikorska J. Combined effects of water temperature and daily food availability period on the growth and survival of tench (Tinca tinca) larvae. Aquac Res. 2017;48(7):3809–16.

Welcomme RL. International introductions of inland aquatic species. Rome: Food and Agriculture Organization of the United Nations; 1988. 318 p.

Kocour M, Gela D, Rodina M, Flajshans M. Performance of different tench, Tinca tinca (L.), groups under semi-intensive pond conditions: it is worth establishing a coordinated breeding program. Rev Fish Biol Fisher. 2010;20(3):345–55.

Wang JX, Min WQ, Guan M, Gong LJ, Ren J, Huang Z, et al. Tench farming in China: present status and future prospects. Aquacult Int. 2006;14(1–2):205–8.

Kocour M, Kohlmann K. Growth hormone gene polymorphisms in tench, Tinca tinca L. Aquaculture. 2011;310(3–4):298–304.

FAO. Fishery Statistical Collections, Global aquaculture production 2017. April 20, 2017.

Flajshans M, Gela D, Kocour M, Buchtova H, Rodina M, Psenicka M, et al. A review on the potential of triploid tench for aquaculture. Rev Fish Biol Fisher. 2010;20(3):317–29.

Kvasnicka P, Flajshans M, Rab P, Linhart O. Inheritance studies of blue and golden varieties of tench (Pisces: Tinca tinca L.). Journal of Heredity. 1998;89(6):553–6.

Svobodova Z, Kolarova J. A review of the diseases and contaminant related mortalities of tench (Tinca tinca L.). Vet Med-Czech. 2004;49(1):19–34.

Chen WJ, Mayden RL. Molecular systematics of the Cyprinoidea (Teleostei: Cypriniformes), the world's largest clade of freshwater fishes: further evidence from six nuclear genes. Molecular phylogenetics and evolution. 2009;52(2):544–9. 10.1016/j.ympev.2009.01.006 PubMed DOI

Arslan A, Taki FN. C-banded karyotype and nucleolar organizer regions of Tinca tinca (Cyprinidae) from Turkey. Caryologia. 2012;65(3):246–9.

Leggatt RA, Iwama GK. Occurrence of polyploidy in the fishes. Rev Fish Biol Fisher. 2003;13(3):237–46.

Šlechtová V, Šlechtá V., Valenta M. Genetic protein variability in tench (Tinca tinca L.) stocks in Czech Republic. Polish Archives of Hydrobiology. 1995;42:133–40.

Kohlmann K, Kersten P. Enzyme variability in a wild population of tench (Tinca tinca). Polish Archives of Hydrobiology. 1998;45:303–10.

Kohlmann K, Kersten P, Flajshans M. Comparison of microsatellite variability in wild and cultured tench (Tinca tinca). Aquaculture. 2007;272:S147–S51.

Kohlmann K, Kersten P, Panicz R, Memis D, Flajshans M. Genetic variability and differentiation of wild and cultured tench populations inferred from microsatellite loci. Rev Fish Biol Fisher. 2010;20(3):279–88.

Lo Presti R, Kohlmann K, Kersten P, Gasco L, Lisa C, Di Stasio L. Genetic variability in tench (Tinca tinca L.) as revealed by PCR-RFLP analysis of mitochondrial DNA. Ital J Anim Sci. 2012;11(1).

Lajbner Z, Kotlik P. PCR-RFLP assays to distinguish the Western and Eastern phylogroups in wild and cultured tench Tinca tinca. Molecular ecology resources. 2011;11(2):374–7. 10.1111/j.1755-0998.2010.02914.x PubMed DOI

Lo Presti R, Kohlmann K, Kersten P, Lisa C, Di Stasio L. Sequence variability at the mitochondrial ND1, ND6, cyt b and D-loop segments in tench (Tinca tinca L.). J Appl Ichthyol. 2014;30:15–21.

Lajbner Z, Linhart O, Kotlik P. Human-aided dispersal has altered but not erased the phylogeography of the tench. Evolutionary applications. 2011;4(4):545–61. 10.1111/j.1752-4571.2010.00174.x PubMed DOI PMC

Kocour M, Kohlmann K. Distribution of five growth hormone gene haplogroups in wild and cultured tench, Tinca tinca L., populations. J Appl Ichthyol. 2014;30:22–8.

Metzker ML. Sequencing technologies—the next generation. Nature reviews Genetics. 2010;11(1):31–46. 10.1038/nrg2626 PubMed DOI

Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nature reviews Genetics. 2003;4(12):981–94. 10.1038/nrg1226 PubMed DOI

Beaumont MA, Balding DJ. Identifying adaptive genetic divergence among populations from genome scans. Mol Ecol. 2004;13(4):969–80. PubMed

Morin PA, Luikart G, Wayne RK, Grp SW. SNPs in ecology, evolution and conservation. Trends Ecol Evol. 2004;19(4):208–16.

Bester-Van Der Merwe A, Blaauw S, Du Plessis J, Roodt-Wilding R. Transcriptome-wide single nucleotide polymorphisms (SNPs) for abalone (Haliotis midae): validation and application using GoldenGate medium-throughput genotyping assays. International journal of molecular sciences. 2013;14(9):19341–60. 10.3390/ijms140919341 PubMed DOI PMC

Li S, Liu H, Bai J, Zhu X. Transcriptome assembly and identification of genes and SNPs associated with growth traits in largemouth bass (Micropterus salmoides). Genetica. 2017;145(2):175–87. 10.1007/s10709-017-9956-z PubMed DOI

Liao Z, Wan Q, Shang X, Su J. Large-scale SNP screenings identify markers linked with GCRV resistant traits through transcriptomes of individuals and cell lines in Ctenopharyngodon idella. Sci Rep. 2017;7(1):1184 10.1038/s41598-017-01338-7 PubMed DOI PMC

Ogden R. Unlocking the potential of genomic technologies for wildlife forensics. Molecular ecology resources. 2011;11 Suppl 1:109–16. PubMed

Helyar SJ, Hemmer-Hansen J, Bekkevold D, Taylor MI, Ogden R, Limborg MT, et al. Application of SNPs for population genetics of nonmodel organisms: new opportunities and challenges. Molecular ecology resources. 2011;11 Suppl 1:123–36. PubMed

Helyar SJ, Limborg MT, Bekkevold D, Babbucci M, van Houdt J, Maes GE, et al. SNP discovery using Next Generation Transcriptomic Sequencing in Atlantic herring (Clupea harengus). Plos One. 2012;7(8):e42089 10.1371/journal.pone.0042089 PubMed DOI PMC

Lamichhaney S, Martinez Barrio A, Rafati N, Sundstrom G, Rubin CJ, Gilbert ER, et al. Population-scale sequencing reveals genetic differentiation due to local adaptation in Atlantic herring. Proc Natl Acad Sci U S A. 2012;109(47):19345–50. 10.1073/pnas.1216128109 PubMed DOI PMC

Xu J, Ji P, Zhao Z, Zhang Y, Feng J, Wang J, et al. Genome-wide SNP discovery from transcriptome of four common carp strains. Plos One. 2012;7(10):e48140 10.1371/journal.pone.0048140 PubMed DOI PMC

Zarraonaindia I, Iriondo M, Albaina A, Pardo MA, Manzano C, Grant WS, et al. Multiple SNP markers reveal fine-scale population and deep phylogeographic structure in European anchovy (Engraulis encrasicolus L.). Plos One. 2012;7(7):e42201 10.1371/journal.pone.0042201 PubMed DOI PMC

Hess JE, Campbell NR, Close DA, Docker MF, Narum SR. Population genomics of Pacific lamprey: adaptive variation in a highly dispersive species. Mol Ecol. 2013;22(11):2898–916. 10.1111/mec.12150 PubMed DOI

Montes I, Iriondo M, Manzano C, Santos M, Conklin D, Carvalho GR, et al. No loss of genetic diversity in the exploited and recently collapsed population of Bay of Biscay anchovy (Engraulis encrasicolus, L.). Mar Biol. 2016;163(5).

Montes I, Conklin D, Albaina A, Creer S, Carvalho GR, Santos M, et al. SNP discovery in European anchovy (Engraulis encrasicolus, L) by high-throughput transcriptome and genome sequencing. Plos One. 2013;8(8):e70051 10.1371/journal.pone.0070051 PubMed DOI PMC

Montes I, Zarraonaindia I, Iriondo M, Grant WS, Manzano C, Cotano U, et al. Transcriptome analysis deciphers evolutionary mechanisms underlying genetic differentiation between coastal and offshore anchovy populations in the Bay of Biscay. Mar Biol. 2016;163(10).

Laconcha U, Iriondo M, Arrizabalaga H, Manzano C, Markaide P, Montes I, et al. New Nuclear SNP Markers Unravel the Genetic Structure and Effective Population Size of Albacore Tuna (Thunnus alalunga). Plos One. 2015;10(6):e0128247 10.1371/journal.pone.0128247 PubMed DOI PMC

Martinez Barrio A, Lamichhaney S, Fan G, Rafati N, Pettersson M, Zhang H, et al. The genetic basis for ecological adaptation of the Atlantic herring revealed by genome sequencing. eLife. 2016;5. PubMed PMC

Robledo D, Rubiolo JA, Cabaleiro S, Martinez P, Bouza C. Differential gene expression and SNP association between fast- and slow-growing turbot (Scophthalmus maximus). Sci Rep. 2017;7(1):12105 10.1038/s41598-017-12459-4 PubMed DOI PMC

Alvarez P, Arthofer W, Coelho MM, Conklin D, Estonba A, Grosso AR, et al. Genomic Resources Notes Accepted 1 June 2015–31 July 2015. Molecular ecology resources. 2015;15(6):1510–2. 10.1111/1755-0998.12454 PubMed DOI

Flajshans M, Linhart O, Slechtova V, Slechta V. Genetic resources of commercially important fish species in the Czech Republic: present state and future strategy. Aquaculture. 1999;173(1–4):471–83.

Lajbner Z, Kohlmann K, Linhart O, Kotlik P. Lack of reproductive isolation between the Western and Eastern phylogroups of the tench. Rev Fish Biol Fisher. 2010;20(3):289–300.

Marçais G, Kinsgford C. A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics. 2011; 27(6):764–770. 10.1093/bioinformatics/btr011 PubMed DOI PMC

Vurture GW, Sedlazeck FJ, Nattestad M, Underwood CJ, Fang H, Gurtowski J. GenomeScope: fast reference-free genome profiling from short reads. Bioinformatics. 2017; 33(14):2202–2204. 10.1093/bioinformatics/btx153 PubMed DOI PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England). 2014;30(15):2114–20. PubMed PMC

Cock PJ, Antao T, Chang JT, Chapman BA, Cox CJ, Dalke A, et al. Biopython: freely available Python tools for computational molecular biology and bioinformatics. Bioinformatics (Oxford, England). 2009;25(11):1422–3. PubMed PMC

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature biotechnology. 2011;29(7):644–52. 10.1038/nbt.1883 PubMed DOI PMC

Waterhouse RM, Seppey M, Simão FA, Manni M, Ioannidis P, Klioutchnikov G, Kriventseva EV, Zdobnov EM. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 2018; 35(3):543–548. PubMed PMC

Felipe A. Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–3212. 10.1093/bioinformatics/btv351 PubMed DOI

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. Journal of molecular biology. 1990;215(3):403–10. 10.1016/S0022-2836(05)80360-2 PubMed DOI

Boeckmann B, Bairoch A, Apweiler R, Blatter MC, Estreicher A, Gasteiger E, et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic acids research. 2003;31(1):365–70. PubMed PMC

Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics (Oxford, England). 2007;23(10):1282–8. PubMed

Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic acids research. 2011;39(Web Server issue):W29–37. 10.1093/nar/gkr367 PubMed DOI PMC

Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic acids research. 2014;42(Database issue):D222–30. 10.1093/nar/gkt1223 PubMed DOI PMC

Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic acids research. 2012;40(Database issue):D109–14. 10.1093/nar/gkr988 PubMed DOI PMC

Powell S, Szklarczyk D, Trachana K, Roth A, Kuhn M, Muller J, et al. eggNOG v3.0: orthologous groups covering 1133 organisms at 41 different taxonomic ranges. Nucleic acids research. 2012;40(Database issue):D284–9. 10.1093/nar/gkr1060 PubMed DOI PMC

Bray NL, Pimentel H, Melsted P, Pachter L. Near-optimal probabilistic RNA-seq quantification. Nature biotechnology. 2016;34(5):525–7. 10.1038/nbt.3519 PubMed DOI

Pimentel H, Bray NL, Puente S, Melsted P, Pachter L. Differential analysis of RNA-seq incorporating quantification uncertainty. Nature methods. 2017;14(7):687–90. 10.1038/nmeth.4324 PubMed DOI

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics (Oxford, England). 2009;25(16):2078–9. PubMed PMC

Koster J, Rahmann S. Snakemake—a scalable bioinformatics workflow engine. Bioinformatics (Oxford, England). 2012;28(19):2520–2. PubMed

Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nature methods. 2012;9(4):357–9. 10.1038/nmeth.1923 PubMed DOI PMC

Wang S, Sha Z, Sonstegard TS, Liu H, Xu P, Somridhivej B, et al. Quality assessment parameters for EST-derived SNPs from catfish. BMC Genomics. 2008;9:450 10.1186/1471-2164-9-450 PubMed DOI PMC

Conklin D, Montes, I., Albaina, A., Estonba, A. Improved conversion rates for SNP genotyping of non-model organisms. International Work-Conference on Bioinformatics and Biomedical Engineering; Granada, Spain 2013. p. 127–34.

Piry S, Alapetite A, Cornuet JM, Paetkau D, Baudouin L, Estoup A. GENECLASS2: a software for genetic assignment and first-generation migrant detection. The Journal of heredity. 2004;95(6):536–9. 10.1093/jhered/esh074 PubMed DOI

Rousset F. genepop'007: a complete re-implementation of the genepop software for Windows and Linux. Molecular ecology resources. 2008;8(1):103–6. 10.1111/j.1471-8286.2007.01931.x PubMed DOI

Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics. 2000;155(2):945–59. PubMed PMC

Evanno G, Regnaut S, Goudet J. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol. 2005;14(8):2611–20. 10.1111/j.1365-294X.2005.02553.x PubMed DOI

Francis RM. pophelper: an R package and web app to analyse and visualize population structure. Molecular ecology resources. 2017;17(1):27–32. 10.1111/1755-0998.12509 PubMed DOI

Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008;180(2):977–93. 10.1534/genetics.108.092221 PubMed DOI PMC

Benjamini Y, Hochberg Y. Controlling the False Discovery Rate—a Practical and Powerful Approach to Multiple Testing. J Roy Stat Soc B Met. 1995;57(1):289–300.

Weir BS, Cockerham CC. Estimating f-statistics for the analysis of population structure. Evolution; international journal of organic evolution. 1984;38(6):1358–70. 10.1111/j.1558-5646.1984.tb05657.x PubMed DOI

Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular ecology resources. 2010;10(3):564–7. 10.1111/j.1755-0998.2010.02847.x PubMed DOI

Petit E, Balloux F, Goudet J. Sex-biased dispersal in a migratory bat: a characterization using sex-specific demographic parameters. Evolution; international journal of organic evolution. 2001;55(3):635–40. PubMed

Rice WR. Analyzing tables of statistical tests. Evolution; international journal of organic evolution. 1989;43(1):223–5. 10.1111/j.1558-5646.1989.tb04220.x PubMed DOI

Kumar G, Kohlmann, K., Gela, D., Kocour, M. Phylogroup origin of Tench Tinca tinca L. has no effects on main performance parameters. Aquaculture Europe-14; San-Sebastian, Spain 2014.

Assessing the Impacts of Adaptation to Native-Range Habitats and Contemporary Founder Effects on Genetic Diversity in an Invasive Fish