Genes & Genomics

, Volume 40, Issue 4, pp 447–454 | Cite as

Development of 21 polymorphic microsatellite markers for the black-banded sea krait, Laticauda semifasciata (Elapidae: Laticaudinae), and cross-species amplification for two other congeneric species

  • Young Se Hyun
  • Il-Hun Kim
  • Ha Yeun Song
  • Daesik Park
  • Mamoru Toda
  • Tein-Shun Tai
  • Hye Suck An
Research Article
  • 83 Downloads

Abstract

The genus Laticauda (Reptilia: Elapidae), commonly known as sea kraits, is venomous marine amphibious snakes distributed throughout the south and southeast Asian islands and mostly found in coastal waters. To facilitate genetic studies, we have developed microsatellite loci for L. semifasciata using the 454 GS-FLX pyrosequencing technique. A total of 65,680 sequences containing a minimum of five repeat motifs were identified from 451,659 reads. Among 80 loci containing more than nine repeat units, 34 primer sets (42.5%) produced strong PCR products, of which 21 were polymorphic among 36 samples of L. semifasciata. All loci exhibited high genetic variability, with an average of 7.38 alleles per locus, and the mean observed and expected heterozygosities were 0.73 and 0.76, respectively. The cross-species amplification of these loci in two laticaudine species, L. colubrina and L. laticaudata, revealed a high transferability (78.6%) and polymorphism (59.5%) of the loci. Our work demonstrated the utility of next-generation 454 sequencing as the rapid and cost-effective method for development of microsatellite markers. The high level of polymorphism in these microsatellite loci will be useful for the detection of population subdivision and the study of migration, gene flow, relatedness and philopatry of L. semifasciata and other laticaudine species.

Keywords

Laticauda semifasciata Microsatellite loci Pyrosequencing Genetic variability Cross-species amplification 

Notes

Acknowledgements

This work is funded by a grant from the National Marine Biodiversity Institute of Korea (MABIK) and is contribution number, 2017M01200, 2017M02000 and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (2014R1A1A4A01005302). Views expressed herein are those of the authors and do not necessarily reflect the views of MABIK.

Compliance with ethical standards

Conflict of interest

Young Se Hyun, Il-Hun Kim, Ha Yeun Song, Daesik Park, Mamoru Toda, Tein-Shun Tai and Hye Suck An declare that there is no conflict of interest.

Ethical approval

All animal experiments were performed in accordance with the ethical guidelines of National Marine Biodiversity Institute of Korea.

References

  1. Abdelkrim J, Robertson BC, Stanton JL, Gemmell NJ (2009) Fast, cost-effective development of species specific microsatellite markers by genomic sequencing. Biotechniques 46:185–192CrossRefPubMedGoogle Scholar
  2. An HS, Lee JW (2012) Development of microsatellite markers for the Korean mussel, Mytilus coruscus (Mytilidae) using next-generation sequencing. Int J Mol Sci 13:10583–10593CrossRefPubMedCentralPubMedGoogle Scholar
  3. An HS, Lee JW, Hong SW (2012) Application of novel polymorphic microsatellite loci identified in the Korean Pacific Abalone (Haliotis diversicolor supertexta (Haliotidae)) in the genetic characterization of wild and released populations. Int J Mol Sci 13:10750–10764CrossRefPubMedCentralPubMedGoogle Scholar
  4. An CM, An HS, Lee JW, Hong SW (2013) New polymorphic microsatellite loci of threadsail filefish, Stephanolepis cirrhifer (Teleostei, Monacanthidae), from Korean waters. Genet Mol Res 12:1679–1690CrossRefPubMedGoogle Scholar
  5. Austerlitz F, David O, Schaeffer B, Bleakley K, Olteanu M, Leblois R, Veuille M, Laredo C (2009) DNA barcode analysis: a comparison of phylogenetic and statistical classification methods. BMC Bioinformatics. doi: 10.1186/1471-2105-10-S14-S10 PubMedCentralPubMedGoogle Scholar
  6. Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW (2017) GenBank. Nucleic Acids Res 45:D37–D42. Accessed http://www.ncbi.nlm.nih.gov
  7. 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 32:314–331PubMedCentralPubMedGoogle Scholar
  8. Cogger H, Heatwole H, Ishikawa Y, McCoy M, Tamiya N, Teruuchi T (1987) The status and natural history of the Rennell Island sea krait, Laticauda crockery (Serpentes: Laticaudidae). J Herpetol 21:255–266CrossRefGoogle Scholar
  9. Heatwole H, Busack S, Cogger H (2005) Geographic variation in sea kraits of the Laticauda colubrine complex (Serpentes: Elapidae: Hydrophiinae: Laticaudini). Herpetol Monogr 19:1–136CrossRefGoogle Scholar
  10. Jun TH, Michel AP, Mian MA (2011) Development of soybean aphid genomic SSR markers using next generation sequencing. Genome 54:360–367CrossRefPubMedGoogle Scholar
  11. Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106CrossRefPubMedGoogle Scholar
  12. Kharin VE (2009) Redescription of a Russian finding of the Erabu sea krait Pseudolaticauda semifasciata (Reinwardt in Schlegel, 1837), with remarks about species composition of sea snakes (Serpentes: Laticaudidae, Hydrophiidae) in Russian and adjacent waters. Russ J Mar Biol 35:8–14CrossRefGoogle Scholar
  13. Kim IH, Park J, Kaplan RH, Lee JN, Park D (2016) Chinese sea snake (Laticauda semifasciata) misidentified as slender-necked sea snake in previous published account in Korea. J Ecol Environ 40:1. doi: 10.1186/s41610-016-0002-3 CrossRefGoogle Scholar
  14. Lai Y, Sun F (2003) The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol Biol Evol 20:2123–2131CrossRefPubMedGoogle Scholar
  15. Lane A, Shine R (2011) Phylogenetic relationships within laticaudine sea kraits (Elapidae). Mol Phylogenet Evol 59:567–577CrossRefPubMedGoogle Scholar
  16. Lane AM, Oldroyd BP, Shine R (2008) Microsatellite loci for laticaudine sea kraits. Mol Ecol Resour 8:1161–1163CrossRefPubMedGoogle Scholar
  17. Lee HJ, Lee DH, Yoon SJ, Kim DH, Kim SG, Hyun YS, Min GS, Chung KW (2013) Characterization of 20 microsatellite loci by multiplex PCR in swimming crab, Portunus trituberculatus. Genes Genom 35:77–85CrossRefGoogle Scholar
  18. Lindqvist AK, Magnusson PK, Balciuniene J, Wadelius C, Lindholm E, Alarcón-Riquelme ME, Gyllensten UB (1996) Chromosome-specific panels of tri- and tetranucleotide microsatellite markers for multiplex fluorescent detection and automated genotyping: evaluation of their utility in pathology and forensics. Genome Res 6:1170–1176CrossRefPubMedGoogle Scholar
  19. Lukoschek V, Avise JC (2011) Development of ten polymorphic microsatellite loci for the sea snake Hydrophis elegans (Elapidae: Hydrophiinae) and cross-species amplification for fifteen marine hydrophiine species. Cons Gen Res 3:497–501CrossRefGoogle Scholar
  20. Lukoschek V, Avise JC (2012) Development of eleven polymorphic microsatellite loci for the sea snake Emydocephalus annulatus (Elapidae: Hydrophiinae) and cross-species amplification for seven species in the sister genus Aipysurus. Cons Gen Res 4:11–14CrossRefGoogle Scholar
  21. Lukoschek V, Waycott M, Dunshea G (2005) Isolation and characterization of microsatellite loci from the Australasian sea snake, Aipysurus laevis. Mol Ecol Notes 5:875–881CrossRefGoogle Scholar
  22. Park J, Kim IH, Koo KS, Park D (2016) First record of Laticauda semifasciata (Reptilia: Squamata: Elapidae: Laticaudinae) from Korea. Anim Syst Evol Divers 32:148–152CrossRefGoogle Scholar
  23. Peakall R, Gilmore S, Keys W, Morgante M, Rafalski (1998) A Cross-species amplification of soybean (Glycine max) simple sequence repeats within the genus and other legume genera: Implications for the transferability of SSRs in plants. Mol Biol Evol 15:1275–1287CrossRefPubMedGoogle Scholar
  24. Perry JC, Rowe L (2011) Rapid microsatellite development for water striders by next-generation sequencing. J Hered 102:125–129CrossRefPubMedGoogle Scholar
  25. Rasmussen AR, Murphy JC, Ompi MG, Gibbons JW, Uetz P (2011) Marine Reptiles. PLoS ONE 6:e27373CrossRefPubMedCentralPubMedGoogle Scholar
  26. Rasmussen AR, Sanders KL, Guinea ML, Amey AP (2014) Sea snakes in Australian waters (Serpentes: subfamilies Hydrophiinae and Laticaudinae): a review with an updated identification key. Zootaxa 3869:351–371CrossRefPubMedGoogle Scholar
  27. Rice WR (1989) Analyzing tables of statistical tests. Evolution Int J org Evolution 43:223–225CrossRefGoogle Scholar
  28. Rousset F (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106CrossRefPubMedGoogle Scholar
  29. Sanders KL, Lee MSY, Leys R, Foster R, Keogh JS (2008) Molecular phylogeny and divergence dates for Australasian elapids and sea snakes (Hydrophiinae): evidence from seven genes for rapid evolutionary radiations. J Evol Biol 21:682–695CrossRefPubMedGoogle Scholar
  30. Santana Q, Coetze M, SteenKamp E, Mlonyeni O, Hammond G, Wingfield M, Wingfield B (2009) Microsatellite Discovery by deep sequencing of enriched genomic libraries. Biotechniques 46:217–223CrossRefPubMedGoogle Scholar
  31. Scanlon JD, Lee MSY (2004) Phylogeny of Australasian venomous snakes (Colubroidea, Elapidae, Hydrophiinae) based on phenotypic and molecular evidence. Zool Scr 33:335–366CrossRefGoogle Scholar
  32. Smith MA (1926) Monograph of the sea-snakes (Hydrophiidae). Oxford University Press, LondonGoogle Scholar
  33. Tandavanitj N, Mitani S, Toda M (2013) Origins of Laticauda laticaudata and Laticauda semifasciata (Elapidae: Laticaudinae) individuals collected from the main islands of Japan as inferred from molecular data. Curr Herpetol 32:135–141CrossRefGoogle Scholar
  34. 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 4:135Google Scholar
  35. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370Google Scholar
  36. Xu Q, Liu R (2011) Development and characterization of microsatellite markers for genetic analysis of the swimming crab, Portunus trituberculatus. Biochem Genet 49:202–212CrossRefPubMedGoogle Scholar

Copyright information

© The Genetics Society of Korea and Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Young Se Hyun
    • 1
  • Il-Hun Kim
    • 1
  • Ha Yeun Song
    • 1
  • Daesik Park
    • 2
  • Mamoru Toda
    • 3
  • Tein-Shun Tai
    • 4
  • Hye Suck An
    • 1
  1. 1.National Marine Biodiversity Institute of Korea (MABIK)SeochunSouth Korea
  2. 2.Division of Science EducationKangwon National UniversityChuncheonSouth Korea
  3. 3.Tropical Biosphere Research CenterUniversity of the RyukyusNishiharaJapan
  4. 4.Department of Biological Science and TechnologyNational Pingtung University of Science and TechnologyPingtung CountyTaiwan (Republic of China)

Personalised recommendations