Skip to main content

Evaluating the genetic structure of wild and commercial red cusk-eel (Genypterus chilensis) populations through the development of novel microsatellite markers from a reference transcriptome

Abstract

The red cusk-eel (Genypterus chilensis) is a native Chilean species with a high-value market, with the potential to diversify Chilean aquaculture. The objective of this study was to develop a set of microsatellite markers, estimate genetic parameters, determine population differentiation, and identify the population structure of wild and commercial populations of G. chilensis. We discovered 6427 microsatellites markers from RNA-seq data, of which 54.9%, 20.2% and 16.8% were di-, tri-, and tetranucleotides, respectively. We used 12 of these markers to genotype two sets of broodstock, one group from commercial fish, and one group from wild fish from the Coquimbo Region of G. chilensis. We estimate the genetic parameters of the markers, selecting ten polymorphic markers (PIC > 0.5). We observed differences in the inbreeding coefficient among populations, with high values of inbreeding in one broodstock set and lower values in the other groups. The evaluation of population differentiation using Fst showed small (0.0195) to large (0.1888) genetic differentiation between the groups. The structure analysis showed that commercial and wild groups were formed by three clusters, without relevant evidence of admixture process, suggesting that groups evaluated in this study are formed of at least three subpopulations of G. chilensis, which could be explained by the low or lack of migration suggested for this species. This is the first study that identifies a high number of molecular markers in G. chilensis, providing relevant information of the genetic structure of commercial and wild population of this species.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Nielsen JG, Cohen DM, Markle DF, Robins CR (1999) An annotated and illustrated catalogue of pearlfishes, cusk-eels, brotulas and other ophidiiform fishes known to date. In: FAO species catalogue, No. 125, vol 18. FAO Fisheries Synopsis, FAO, Rome, p 178

  2. Vega R, Pradenas M, Estrada JM, Ramirez D, Valdebenito I, Mardones A, Dantagnan P, Alfaro D, Encina F, Pichara C (2012) Evaluation and comparison of the efficiency of two incubation systems for Genypterus chilensis (Guichenot, 1848) eggs. Lat Am J Aquat Res 40(1):187–200. https://doi.org/10.3856/vol40-issue1-fulltext-18

    Article  Google Scholar 

  3. Vega R, Estrada JM, Ramirez D, Flores C, Zamorano J, Encina F, Mardones A, Valdebenito I, Dantagnan P (2015) Growth of cusk eel Genypterus chilensis juveniles in culture conditions. Lat Am J Aquat Res 43(2):344–350. https://doi.org/10.3856/vol43-issue2-fulltext-11

    Article  Google Scholar 

  4. Smith PJ (1979) Glucosephosphate isomerase and phosphoglucomutase polymorphisms in the New-Zealand ling Genypterus blacodes. Comp Biochem Phys B 62(4):573–577. https://doi.org/10.1016/0305-0491(79)90136-6

    Article  Google Scholar 

  5. Ward RD, Reilly A (2001) Development of microsatellite loci for population studies of the pink ling, Genypterus blacodes (Teleostei: Ophidiidae). Mol Ecol Notes 1(3):173–175. https://doi.org/10.1046/j.1471-8278.2001.00066.x

    CAS  Article  Google Scholar 

  6. Ward RD, Appleyard SA, Daley RK, Reilly A (2001) Population structure of pink ling (Genypterus blacodes) from south-eastern Australian water, inferred from allozyme and microsatellite analyses. Mar Freshw Res 52(7):965–973. https://doi.org/10.1071/Mf01014

    Article  Google Scholar 

  7. Canales-Aguirre CB, Ferrada S, Hernandez CE, Galleguillos R (2010) Usefulness of heterologous microsatellites obtained from Genypterus blacodes (Schneider 1801) in species Genypterus off the southeast Pacific. Gayana 74(1):74–77

    Google Scholar 

  8. Weber JL, May PE (1989) Abundant class of human DNA polymorphisms which can be typed using the polymerase chain-reaction. Am J Hum Genet 44(3):388–396

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Gui JF, Zhu ZY (2012) Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chinese Sci Bull 57(15):1751–1760. https://doi.org/10.1007/s11434-012-5213-0

    CAS  Article  Google Scholar 

  10. Wilke K, Jung M, Chen YZ, Geldermann H (1994) Porcine (Ct)(N) sequences—structure and association with dispersed and tandem repeats. Genomics 21(1):63–70. https://doi.org/10.1006/geno.1994.1225

    CAS  Article  PubMed  Google Scholar 

  11. Patel A, Dettleff P, Hernandez E, Martinez V (2016) A comprehensive transcriptome of early development in yellowtail kingfish (Seriola lalandi). Mol Ecol Res 16(1):364–376. https://doi.org/10.1111/1755-0998.12451

    CAS  Article  Google Scholar 

  12. Du M, Li N, Niu BZ, Liu YH, You DJ, Jiang DF, Ruan CQ, Qin ZQ, Song TW, Wang WT (2018) De novo transcriptome analysis of Bagarius yarrelli (Siluriformes: Sisoridae) and the search for potential SSR markers using RNA-Seq. PLoS ONE 13(2):e0190343. https://doi.org/10.1371/journal.pone.0190343

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  13. Ariede RB, Freitas MV, Hata ME, Matrochirico VA, Utsunomia R, Mendonca FF, Foresti F, Porto-Foresti F, Hashimoto DT (2018) Development of microsatellite markers using next-generation sequencing for the fish Colossoma macropomum. Mol Biol Rep 45(1):9–18. https://doi.org/10.1007/s11033-017-4134-z

    CAS  Article  PubMed  Google Scholar 

  14. Aedo JE, Maldonado J, Estrada JM, Fuentes EN, Silva H, Gallardo-Escarate C, Molina A, Valdes JA (2014) Sequencing and de novo assembly of the red cusk-eel (Genypterus chilensis) transcriptome. Mar Genom 18:105–107. https://doi.org/10.1016/j.margen.2014.08.001

    Article  Google Scholar 

  15. da Maia LC, Palmieri DA, de Souza VQ, Kopp MM, de Carvalho FI, Costa de Oliveira A (2008) SSR locator: tool for simple sequence repeat discovery integrated with primer design and PCR simulation. Int J Plant Genom 2008:412696. https://doi.org/10.1155/2008/412696

    CAS  Article  Google Scholar 

  16. Aedo JE, Maldonado J, Aballai V, Estrada JM, Bastias-Molina M, Meneses C, Gallardo-Escarate C, Silva H, Molina A, Valdes JA (2015) mRNA-seq reveals skeletal muscle atrophy in response to handling stress in a marine teleost, the red cusk-eel (Genypterus chilensis). BMC Genom 16:1024. https://doi.org/10.1186/s12864-015-2232-7

    CAS  Article  Google Scholar 

  17. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4(3):535–538. https://doi.org/10.1111/j.1471-8286.2004.00684.x

    CAS  Article  Google Scholar 

  18. Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6(1):288–295. https://doi.org/10.1111/j.1471-8286.2005.01155.x

    Article  Google Scholar 

  19. Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28(19):2537–2539. https://doi.org/10.1093/bioinformatics/bts460

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic-linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32(3):314–331

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Rousset F (2008) GENEPOP’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Res 8(1):103–106. https://doi.org/10.1111/j.1471-8286.2007.01931.x

    Article  Google Scholar 

  22. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14(8):2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x

    CAS  Article  PubMed  Google Scholar 

  24. Beaumont MA (2005) Adaptation and speciation: what can F(st) tell us? Trends Ecol Evol 20(8):435–440. https://doi.org/10.1016/j.tree.2005.05.017

    Article  PubMed  Google Scholar 

  25. Ward RD (2000) Genetics in fisheries management. Hydrobiologia 420:191–201. https://doi.org/10.1023/A:1003928327503

    CAS  Article  Google Scholar 

  26. Hauser L, Seeb JE (2008) Advances in molecular technology and their impact on fisheries genetics. Fish Fish 9(4):473–486. https://doi.org/10.1111/j.1467-2979.2008.00306.x

    Article  Google Scholar 

  27. Xu K, Duan W, Xiao J, Tao M, Zhang C, Liu Y, Liu S (2015) Development and application of biological technologies in fish genetic breeding. Sci China Life Sci 58(2):187–201. https://doi.org/10.1007/s11427-015-4798-3

    CAS  Article  PubMed  Google Scholar 

  28. Hulata G (2001) Genetic manipulations in aquaculture: a review of stock improvement by classical and modern technologies. Genetica 111(1–3):155–173

    CAS  Article  PubMed  Google Scholar 

  29. Canales-Aguirre CB, Ferrada S, Hernandez CE, Galleguillos R (2010) Population structure and demographic history of Genypterus blacodes using microsatellite loci. Fish Res 106(1):102–106. https://doi.org/10.1016/j.fishres.2010.06.010

    Article  Google Scholar 

  30. Fang DA, Zhou YF, Duan JR, Zhang MY, Xu DP, Liu K, Xu P, Wei Q (2015) Screening potential SSR markers of the anadromous fish Coilia nasus by de novo transcriptome analysis using Illumina sequencing. Genet Mol Res 14(4):14181–14188. https://doi.org/10.4238/2015.November.13.1

    CAS  Article  PubMed  Google Scholar 

  31. Luo W, Deng W, Yi SK, Wang WM, Gao ZX (2013) Characterization of 20 polymorphic microsatellites for Blunt snout bream (Megalobrama amblycephala) from EST sequences. Conserv Genet Resour 5(2):499–501. https://doi.org/10.1007/s12686-012-9837-9

    Article  Google Scholar 

  32. Basiita RK, Zenger KR, Mwanja MT, Jerry DR (2018) Gene flow and genetic structure in Nile perch, Lates niloticus, from African freshwater rivers and lakes. PLoS ONE 13(7):e0200001. https://doi.org/10.1371/journal.pone.0200001

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  33. DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater and anadromous fishes compared with other animals. J Fish Biol 56(3):461–473. https://doi.org/10.1111/j.1095-8649.2000.tb00748.x

    CAS  Article  Google Scholar 

  34. An HS, Kim EM, Kang HW, Han HS, Lee JW, Park JY, Myeong JI, An CM (2013) Comparative genetic diversity of wild and hatchery-produced populations of tongue sole (Cynoglossus semilaevis) using multiplex PCR assays with polymorphic microsatellite markers. Genet Mol Res 12(4):6331–6343. https://doi.org/10.4238/2013.December.4.20

    CAS  Article  PubMed  Google Scholar 

  35. Amos W, Wilmer JW, Fullard K, Burg TM, Croxall JP, Bloch D, Coulson T (2001) The influence of parental relatedness on reproductive success. Proc R Soc B 268(1480):2021–2027. https://doi.org/10.1098/rspb.2001.1751

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. An HS, Kim EM, Lee JH, Noh JK, An CM, Yoon SJ, Park KD, Myeong JI (2011) Population genetic structure of wild and hatchery black rockfish Sebastes inermis in Korea, assessed using cross-species microsatellite markers. Genet Mol Res 10(4):2492–2504. https://doi.org/10.4238/2011.October.13.6

    CAS  Article  PubMed  Google Scholar 

  37. Smith PJ, Francis RICC (1982) A glucosephosphate isomerase polymorphism in New-Zealand ling Genypterus blacodes. Comp Biochem Phys B 73(3):451–455. https://doi.org/10.1016/0305-0491(82)90057-8

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by CONICYT/FONDAP [Grant Number 15110027] awarded to Juan Antonio Valdés and Alfredo Molina, and CONICYT FONDECYT Postdoctorado [Grant Number 3180283] awarded to Phillip Dettleff.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alfredo Molina.

Ethics declarations

Conflict of interest

The authors declare that there are no financial or non-financial conflict of interest.

Ethical approval

The procedures with animals in this study were according to animal welfare procedures of the National Commission for Scientific and Technological Research (CONICYT) of the Chilean government and approved by the bioethical committees of the Universidad Andres Bello (Approbation Number 0072018).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

González, P., Dettleff, P., Valenzuela, C. et al. Evaluating the genetic structure of wild and commercial red cusk-eel (Genypterus chilensis) populations through the development of novel microsatellite markers from a reference transcriptome. Mol Biol Rep 46, 5875–5882 (2019). https://doi.org/10.1007/s11033-019-05021-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-019-05021-0

Keywords

  • Microsatellites
  • Transcriptome
  • Genypterus chilensis
  • Red cusk-eel
  • Genetic structure