Abstract
Background
The species Capoeta aculeata (Valenciennes, 1844) is one of the most important freshwater species endemic to Iran. However, the investigation of the population genetic structure of this species is limited by the low number of molecular markers currently described.
Methods and results
In this study, we implemented next generation sequencing technology to identify polymorphic microsatellite markers and investigate the population genetic structure of C. aculeata sampled from three geographical sites in Iran. We characterized and developed 36 novel polymorphic microsatellite markers and these loci were examined in 120 individuals from three populations occurring in the Zagros basin. The average number of alleles per locus varied from 1.7 to 16 (average = 7.89). The results showed that, the polymorphism information content (PIC) of these simple sequence repeat (SSR) loci varied from 0.254 to 0.888. The observed heterozygosity (HO) per locus ranged from 0.170 to 0.881, while the expected heterozygosity (HE) per locus was from 0.170 to 0.881. Among these SSR loci, 20 loci deviated significantly from the Hardy–Weinberg equilibrium after Bonferroni correction (p < 0.05).
Conclusions
These microsatellite markers could provide a valuable tool for future population and conservation genetics studies of C. aculeate and other closely related species.
Similar content being viewed by others
Data availability
The datasets generated are available from the corresponding author upon request.
References
Zareian H, Esmaeili HR, Freyhof J (2016) Capoeta anamisensis, a new species from the Minab and Hasan Langhi River drainages in Iran (Teleostei: Cyprinidae). Zootaxa 4083:126–142
Bektas Y, Turan D, Aksu I, Ciftci Y, Eroglu O, Kalayci G, Belduz AO (2017) Molecular phylogeny of the genus Capoeta (Teleostei: Cyprinidae) in Anatolia. Turkey Biochem Syst Ecol 70:80–94
Freyhof J, Esmaeili HR, Sayyadzadeh G, Geiger M (2014) Review of the crested loaches of the genus Paracobitis from Iran and Iraq with the description of four new species (Teleostei:Nemacheilidae). Ichthyol Explor Fresh 25(1):11–38
Nazari S, Paknejad H, Jalali A, Khorshidi Z (2021) Molecular genetic divergence of five genera of cypriniform fish in Iran assessed by DNA barcoding. Iran J Fish Sci 20(3):628–645
Parmaksız A, Eksi E (2017) Genetic diversity of the cyprinid fish Capoeta trutta (Heckel, 1843) populations from Euphrates and Tigris rivers in Turkey based on mtDNA COI sequences. Indian J Fish 64(1):18–22
Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203
Zane L, Bargelloni L, Patarnello T (2002) Strategies for microsatellite isolation: a review. Mol Ecol 11:1–16
Chang Y, Feng Z, Yu J, Ding J (2009) Genetic variability analysis in five populations of the sea cucumber Stichopus (Apostichopus) japonicus from China, Russia, South Korea and Japan as revealed by microsatellite markers. Mar Ecol 30:455–461
Xue D, Zhang T, Liu J (2014) Microsatellite evidence for high frequency of multiple paternity in the marine gastropod Rapana venosa. PLoS ONE. https://doi.org/10.1371/journal.pone.0086508
Montanari S, Perchepied L, Renault D, Frijters L, Velasco R, Horner M, Gardiner SE, Chagné D, Bus VGM, Durel CE, Malnoy M (2016) A QTL detected in an inter specific pear population confers stable fire blight resistance across different environments and genetic backgrounds. Mol Breeding 36:1–16
Jia SW, Liu P, Li J, Li JT, Pan LQ (2013) Isolation and characterization of polymorphic microsatellite loci in the ridgetail white prawn Exopalaemon carinicauda. Genet Mol Res 12:2816–2820
Perina A, Gonzlez-Tizn AM, Vizcano A, Gonzlez-Ortegn E, Martnez-Lage A (2016) Isolation and characterization of 20 polymorphic microsatellite loci in Palaemon serratus and cross-amplification in Palaemon species by 454 pyrosequencing. Conserv Genet Resour 8:169–196
Gandomkar H, Shekarabi SPH, Abdolhay HA, Nazari S, Mehrjan MS (2020) Genetic structure of the Capoeta aculeata populations inferred from microsatellite DNA loci. Biodiversitas 21:4565–4570. https://doi.org/10.13057/biodiv/d211014
Dutta N, Singh RK, Mohindra V, Pathak A, Kumar R, Sah P, Mandal S, Kaur G, Lal KK (2019) Microsatellite marker set for genetic diversity assessment of primitive Chitala chitala (Hamilton, 1822) derived through SMRT sequencing technology. Mol Biol Rep 46(1):41–49
Qiu B, Fang S, Ikhwanuddin M, Wong L, Ma H (2020) Genome survey and development of polymorphic microsatellite loci for Sillago sihama based on Illumina sequencing technology. Mol Biol Rep 47(4):3011–3017
Feng N, Ma H, Ma C et al (2014) Characterization of 40 single nucleotide polymorphism (SNP) via T m-shift assay in the mud crab (Scylla paramamosain). Mol Biol Rep 41:5467–5471. https://doi.org/10.1007/s11033-014-3420-2
Xiao M, Hu Q, Zhao Y, Bao F, Cui F, Zheng R (2018) Development of 36 SNP markers in Ophiocephalus argus Cantor base on high throughput sequencing. Conserv Genet Resour 10(1):35–38. https://doi.org/10.1007/s12686-017-0757-6
Khoshkholgh M, Nazari S (2020) Characterization of single nucleotide polymorphism markers for the narrow-clawed crayfish Pontastacus leptodactylus (Eschscholtz, 1823) based on RAD sequencing. Conserv Genet Resour. https://doi.org/10.1007/s12686-020-01154-8
Ewers-Saucedo C, Zardus JD, Wares JP (2016) Microsatellite loci discovery from next-generation sequencing data and loci characterization in the epizoic barnacle Chelonibia testudinaria (Linnaeus, 1758). PeerJ. https://doi.org/10.7717/peerj.2019
Wei N, Bemmels JB, Dick CW (2014) The effects of read length, quality and quantity on microsatellite discovery and primer development: from Illumina to PacBio. Mol Ecol Resour 14:953–965
Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510
Zhou J, Zhou B, Li Q et al (2017) Isolation and characterization of 33 EST-SNP markers in Schizothorax prenanti. Conserv Genet Resour 10:205–207. https://doi.org/10.1007/s12686-017-0799-9
Yu L, Bai J, Cao T et al (2014) Genetic variability and relationships among six grass carp Ctenopharyngodon idella populations in China estimated using EST-SNP markers. Fish Sci 80:475–481. https://doi.org/10.1007/s12562-014-0709-y
Luo H, Ye H, Xiao S-J et al (2016) Development of SNP markers associated with immune-related genes of Schizothorax prenanti. Conserv Genet Resour 8:223–226. https://doi.org/10.1007/s12686-016-0539-6
Peng X, Zhao L, Liu J, Guo X (2018) Development of SNP markers for Xenocypris argentea based on transcriptomics. Conserv Genet Resour 10(4):679–684. https://doi.org/10.1007/s12686-017-0900-4
Nazari S, Jafari V, Pourkazemi M, Kolangi Miandare H, Abdolhay H (2016) Association between myostatin gene (MSTN-1) polymorphism and growth traits in domesticated rainbow trout (Oncorhynchus mykiss). Agri Gene 1:109–115
Khoshkholgh M, Nazari S (2019) The genetic diversity and differentiation of narrow-clawed crayfish Pontastacus leptodactylus (Eschscholtz, 1823) (Decapoda: Astacidea: Astacidae) in the Caspian Sea Basin, Iran as determined with mitochondrial and microsatellite DNA markers. J Crust Biol 39(2):112–120
Wang S, Liu P, Lv J, Li Y, Cheng T, Zhang L (2016) Serial sequencing of iso-length rad tags for cost-efficient genome-wide profiling of genetic and epigenetic variations. Nat Protoc 11(11):2189–2200. https://doi.org/10.1038/nprot.2016.133
Bian L, Liu C, Liu G, Chen S, Zhang L, Ge J, Li F, Tan J (2018) SNP discovery in spotted halibut (Verasper variegatus) using restriction site-associated DNA sequencing (RAD-seq). Conserv Genet Resour 10(3):409–413
Andrews S (2016) FastQC: a quality control tool for high throughput sequence data. Version 0.11.5. Babraham Institute, Cambridge, UK. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Martin M (2011) Sequencing reads. EMBnet J 17:10–12
Catchen JP, Hohenlohe SB, Amores A, Cresko W (2013) Stacks: an analysis tool set for population genomics. Mol Ecol 22(11):3124–3140
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. J Bioinform 22(13):1658–1659
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760
Miller MP (1997) Tools for population genetic analyses (TFPGA) v 1.3: a windows program for the analysis of allozyme and molecular genetic data. Northern Arizona University, Flagstaff
Nei M (1972) Genetic distance between populations. Am Nat 106:283–292
Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Resour 4(3):535–538
Chapuis MP, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research_an update. Bioinformatics 28:2537–2539
Excoffier L (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform. https://doi.org/10.1143/JJAP.34.L418
Rousset F (2008) Genepop’007: a complete re-implementation of the genepop software for windows and linux. Mol Ecol Resour 8:103–106
Ling LP, Adibah AB, Tan SG et al (2013) Isolation by the 5′ anchored PCR technique and characterization of eighteen microsatellite loci in horseshoe crab (Tachypleus gigas). J Genet 92:101–104. https://doi.org/10.1007/s12041-011-0115-5
Ariede RB, Freitas MV, Hata ME, Matrochirico-Filho VA, Utsunomia R, Mendonça FF et al (2018) Development of microsatellite markers using next-generation sequencing for the fish Colossoma macropomum. Mol Biol Rep 45:9–18. https://doi.org/10.1007/s11033-017-4134-z
Han Z, Xiao S, Li W, Ye K, Wang ZY (2018) The identification of growth, immune related genes and marker discovery through transcriptome in the yellow drum (Nibea albiflora). Genes Genomics 40:881–891. https://doi.org/10.1007/s13258-018-0697-x
Bazsalovicsová E, Koleniˇcová A, Králová-Hromadová I, Minárik G, Šoltys K, Kuchta R, Štefka J (2018) Development of microsatellite loci in zoonotic tapeworm Dibothriocephalus latus (Linnaeus, 1758), Lühe, 1899 (syn. Diphyllobothrium latum) using microsatellite library screening. Mol Biochem Parasitol 225:1–3
Gravley MC, Pierson BJ, Sage GK, Ramey AM, Talbot SL (2018) DNA microsatellite markers for northern fulmar (Fulmaris glacialis) and cross-species amplification in select seabird species, Alaska 2018. U.S. Geological Survey data release. https://doi.org/10.5066/P9KWA9VZ
Patel A, Das P, Barat A, Meher PK, Jayasankar P (2010) Utility of cross-species amplification of 34 rohu microsatellite loci in Labeo bata, and their transferability in six other species of the cyprinidae family. Aquac Res 41:590–593
Gao Z, Luo W, Liu H, Zeng C, Liu X, Yi S, Wang W (2012) Transcriptome analysis and SSR/SNP markers information of the blunt snout bream (Megalobrama amblycephala). PLoS ONE. https://doi.org/10.1371/journal.pone.0042637
Fitch AJ, Leeworthy G, Li X, Bowman W, Turner L, Gardner MG (2013) Isolation and characterisation of eighteen microsatellite markers from the sea cucumber Holothuria scabra (Echinodermata: Holothuriidae). Aust J Zool 60:368–371
Norrell AE, Crawley D, Jones KL, Saillant EA (2014) Development and characterization of eighty-four microsatellite markers for the red snapper (Lutjanus campechanus) using Illumina paired-end sequencing. Aquaculture 430:128–132
Fan S, Wang J, Huang G, Liu B, Yu D (2015) Identification of twenty novel polymorphic microsatellite DNA markers from transcripts of the pearl oyster Pinctada fucata using next-generation sequencing approach. J Genet 94:82–85
Rodrigues MDN, Moreira CGÁ, Gutierrez HJP, Almeida DB, Junoir D, Moreira HLM (2015) Development of microsatellite markers for use in breeding catfish, Rhamdia sp. Afr J Biotechnol 14:400–411
Yu JN, Kim SK, Sagong J, Ryu SH, Chae B (2019) Identification of microsatellite markers and their application in yellow catfish (Pseudobagrus fulvidraco Richardson, 1846) population genetics of Korea. J Genet 98:2–7
Nazari S, Pourkazemi M, Khoshkholgh MR (2019) Analysis of the genetic structure of the Persian sturgeon (Acipenser persicus) populations: comparison of control region sequencing and PCR-RFLP analysis of mitochondrial DNA. Iran J Fish Sci 19(6):3201–3220
Peyran C, Planes S, Tolou N, Iwankow G, Boissin E (2020) Development of 26 highly polymorphic microsatellite markers for the highly endangered fan mussel Pinna nobilis and cross-species amplification. Mol Biol Rep 4:2551–2559
Pathak RU, Mamillapalli A, Rangaraj N, Kumar RP, Vasanthi D, Mishra K, Mishra RK (2013) AAGAG repeat RNA is an essential component of nuclear matrix in Drosophila. RNA Biol 10(4):564–571
Guichoux E, Lagache L, Wagner S, Chaumeil P, Léger P, Lepais O, Lepoittevin C, Malausa T, Revardel E, Salin F, Petit RJ (2011) Current trends in microsatellite genotyping. Mol Ecol Resour 11:591–611
Ma H, Zou X, Ji X, Ma C, Lu J, Jiang W, Xia L, Li S, Liu Y, Gong Y, Ma L (2013) Discovery and characterization of a first set of polymorphic microsatellite markers in red crab (Charybdis feriatus). J Genet 92:e113–e115
Zalapa JE, Cuevas H, Zhu H, Steffan S, Senalik D, Zeldin E, McCown B, Harbut R, Simon P (2012) Using next-generation sequencing approaches to isolate simple sequence repeat (SSR) loci in the plant sciences. Am J Bot 99:193–208
Acknowledgements
This work was supported by the Research Fund for the department of Fisheries of the Islamic Azad University of Tehran, Iran.
Author information
Authors and Affiliations
Contributions
HG made the literature, sample collection, material preparation. SPHS has major contribution to the preliminary study design and interpretation of data. The first draft of the manuscript was written by HAA. SN designed the experiment, institutional support and supervision of the preliminary experiment and made the data analysis. MSM has significant contributions to the laboratory work and interpretation of the results. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
The main research project researcher of this work was approved for animal ethics by Iranian Fisheries Sciences Research Institute (IFSRI) for scientific purposes development, Iran. All applicable guidelines for the care and use of animals were followed by the authors. The experiment was approved for Animal Welfare by the Institutional Animal Welfare Committee of Agricultural Research, Education and Extension Organization (AREEO), Iran.
Informed consent
This research does not involve humans and therefore informed consents are not applicable.
Consent to participate (ethics)
Informed consent was obtained from all individual participants included in the study.
Consent to publish (ethics)
The participant has consented to the submission of the report to the journal.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gandomkar, H., Shekarabi, S.P.H., Abdolhay, H.A. et al. Characterization of novel genotyping-by-sequencing (GBS)-based simple sequence repeats (SSRs) and their application for population genomics of Capoeta aculeata (Valenciennes, 1844). Mol Biol Rep 48, 6471–6480 (2021). https://doi.org/10.1007/s11033-021-06653-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-021-06653-x