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
Abstract
:1. Introduction
2. Results and Discussion
2.1. 454 Sequencing Results
2.2. Isolation of Microsatellite Loci
2.3. Genetic Variability within and between the Wild and Released Populations
2.4. Genetic Variability between the Wild and Released Populations
3. Experimental Section
3.1. Sample Collection and 454 Sequencing
3.2. Microsatellite Discovery and Primer Screening
3.3. DNA Amplification and Genotyping
3.4. Population Comparisons
4. Conclusions
Acknowledgments
References
- Geiger, D. A total evidence cladistic analysis of the Haliotidae (Gastropoda: Vetigastropoda). Ph.D. Thesis, University of Southern California, Los Angeles, CA, USA, 1999; p. 423. [Google Scholar]
- Lee, Y.C.; Kuo, H.H.; Chen, Y.G. Discrimination and abundance estimation of wild and released abalone Haliotis diversicolor using stable carbon and oxygen isotope analysis in north-eastern Taiwan. Fish. Sci 2002, 68, 1020–1028. [Google Scholar]
- Fisheries Information Service; Ministry for Food, Agriculture, Forestry and Fisheries: Gwacheon, Korea, 2009. Available online: http://www.fips.go.kr accessed on 10 July 2012.
- Ko, J.C.; Yoo, J.T.; Choi, Y.M.; Kim, J.W.; Im, Y.J. Fisheries management of an abalone Haliotis diversicolor in the eastern coastal waters of Jeju island using yield-per-recruit model (in Korean). Korean J. Malacol 2008, 24, 143–151. [Google Scholar]
- Allendorf, F.W.; Ryman, N. Genetic Management of Hatchery Stocks. In Population Genetics and Fishery Management; Ryman, N., Utter, F., Eds.; University of Washington Press: Seattle, WA, USA, 1987; pp. 141–159. [Google Scholar]
- Food and Agriculture Organization of the United Nations. Report of the expert consultation on utilization and conservation of aquatic genetic resources. FAO Fish Rep. 1993, 491, 1–58.
- Reiss, H.; Hoarau, G.; Dickey-Collas, M.; Wolff, W.J. Genetic population structure of marine fish: Mismatch between biological and fisheries management units. Fish and Fisheries 2009, 10, 361–395. [Google Scholar]
- Tauz, D. Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 1989, 17, 6463–6471. [Google Scholar]
- Holland, B.S. Invasion without a bottleneck: Microsatellite variation in natural and invasive populations of the brown mussel Perna perna (L). Mar. Biotechnol 2001, 3, 407–415. [Google Scholar]
- Lemay, M.A.; Boulding, E.G. Microsatellite pedigree analysis reveals high variance in reproductive success and reduced genetic diversity in hatchery-spawned northern abalone. Aquaculture 2009, 295, 22–29. [Google Scholar]
- Ren, P.; Wang, Z.; Tao, C.; Liu, Y.; Ke, C. Development of 11 polymorphic microsatellite loci in the small abalone (Haliotis diversicolor Reeve). Mol. Ecol. Res 2008, 8, 1390–1392. [Google Scholar]
- Zhan, X.; Hu, H.Y.; Ke, C.H.; Hu, S.N.; Wang, D.X.; Chen, F. Isolation and characterization of eleven microsatellite loci in small abalone, Haliotis diversicolor Reeve. Conserv. Genet 2009, 10, 1185–1187. [Google Scholar]
- Wang, Y.; Wang, F.; Shi, Y.H.; Gu, Z.F.; Wang, A.M. Development and characterization of 60 microsatellite markers in the abalone Haliotis diversicolor. Genet. Mol. Res 2011, 10, 860–866. [Google Scholar]
- Pompanon, F.; Bonin, A.; Bellemain, E.; Taberlet, P. Genotyping errors: Causes, consequences and solutions. Nat. Rev. Genet 2005, 6, 847–859. [Google Scholar]
- Deitz, K.C.; Reddy, V.P.; Reddy, M.R.; Satyanarayanah, N.; Lindsey, M.W.; Overgaard, H.J.; Jawara, M.; Caccone, A.; Slotman, M.A. Limited usefulness of microsatellite markers from the malaria vector Anopheles gambiae when applied to the closely related species Anopheles melas. J. Hered 2012, 103, 585–593. [Google Scholar]
- Zane, L.; Bargelloni, L.; Patarnello, T. Strategies for microsatellite isolation: A review. Mol. Ecol 2002, 11, 1–16. [Google Scholar]
- Gao, H.; Cai, S.; Yan, B.; Chen, B.; Yu, F. Discrepancy variation of dinucleotide microsatellite repeats in eukaryotic genomes. Biol. Res 2009, 42, 365–375. [Google Scholar]
- Schmuki, C.; Blacket, M.J.; Sunnucks, P. Anonymous single-copy nuclear DNA (scnDNA) markers for two endemic log-dwelling beetles: Apasis puncticeps and Adelium calosomoides (Tenebrionidae: Lagriinae: Adeliini). Mol. Ecol. Notes 2006, 6, 362–364. [Google Scholar]
- Arthofer, W.; Schlick-Steiner, B.C.; Steiner, F.M.; Avtzis, D.N.; Crozier, R.H.; Stauffer, C. Lessons from a beetle and an ant: Coping with taxon-dependent differences in microsatellite development success. J. Mol. Evol 2007, 65, 304–307. [Google Scholar]
- Santana, Q.; Coetze, M.; SteenKamp, E.; Mlonyeni, O.; Hammond, G.; Wingfield, M.; Wingfield, B. Microsatellite discovery by deep sequencing of enriched genomic libraries. Biotechniques 2009, 46, 217–223. [Google Scholar]
- Perry, J.C.; Rowe, L. Rapid microsatellite development for water striders by next generation sequencing. J. Hered 2010, 102, 125–129. [Google Scholar]
- Jun, T.H.; Michel, A.P.; Mian, M.A. Development of soybean aphid genomic SSR markers using next generation sequencing. Genome 2011, 54, 360–367. [Google Scholar]
- Wang, J.; Yu, X.; Zhao, K.; Zhang, Y.; Tong, J.; Peng, Z. Microsatellite development for an endangered bream Megalobrama pellegrini (Teleostei, Cyprinidae) using 454 sequencing. Int. J. Mol. Sci 2012, 13, 3009–3021. [Google Scholar]
- Greenley, A.P.; Muguia-Vega, A.; Saenz-Arroyo, A.; Micheli, F. New tetranucleotide microsatellite loci in pink abalone (Haliotis corrugata) isolated via 454 pyrosequencing. Conserv. Genet. Resour 2012, 4, 265–268. [Google Scholar]
- Guichoux, E.; Lagache, L.; Wagner, S.; Chaumeil, P.; Léger, P.; Lepais, O.; Lepoittevin, C.; Malausa, T.; Revardel, E.; Salin, F.; et al. Current trends in microsatellite genotyping. Mol. Ecol. Resour 2011, 211, 591–611. [Google Scholar]
- Castoe, T.A.; Poole, A.W.; Gu, W.; de Konig, A.P.J.; Daza, J.M.; Smith, E.N.; Pollock, D.D. Rapid identification of thousands of copperhead snake microsatellite loci from modest amounts of 454 shotgun genome sequence. Mol. Ecol. Resour 2010, 10, 341–347. [Google Scholar]
- Allentoft, M.E.; Schuster, S.C.; Holdaway, R.N.; Hale, M.L.; Mclat, E.; Oskam, C.; Gilbert, M.T.P.; Spencer, P.; Willerslev, E.; Bunce, M. Identification of microsatellites from an extinct moa species using highthroughput (454) sequence data. BioTechniques 2009, 46, 195–200. [Google Scholar]
- Lai, Y.; Sun, F. The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol. Biol. Evol 2003, 20, 2123–2131. [Google Scholar]
- Farrer, R.A.; Kemen, E.; Jones, J.D.; Studholme, D.J. De novo assembly of the Pseudomonas syringae pv. syringae B728a genome using Illumina/Solexa short sequence reads. FEMS Microbiol. Lett 2009, 291, 103–111. [Google Scholar]
- Peakall, R.; Gilmore, S.; Keys, W.; Morgante, M.; Rafalski, 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 1998, 15, 1275–1287. [Google Scholar]
- An, H.S.; Park, J.Y. Ten new highly polymorphic microsatellite loci in the blood clam Scapharca broughtonii. Mol. Ecol. Notes 2005, 5, 896–898. [Google Scholar]
- Kenchington, E.L.; Patwary, M.U.; Zouros, E.; Bird, C.J. Genetic differentiation in relation to marine landscape in a broadcast-spawning bivalve mollusc (Placopecten magellanicus). Mol. Ecol 2006, 15, 1781–1796. [Google Scholar]
- Launey, S.; Hedgecock, D. High genetic load in the Pacific oyster Crassostrea gigas. Genetics 2001, 159, 255–265. [Google Scholar]
- Evans, B.; Bartlett, J.; Sweijd, N.; Cook, P.; Elliott, N.G. Loss of genetic variation at microsatellite loci in hatchery produced abalone in Australia (Haliotis rubra) and South Africa (Haliotis midae). Aquaculture 2004, 233, 109–127. [Google Scholar]
- Li, Q.; Yu, H.; Yu, R.H. Genetic variability assessed by microsatellites in cultured populations of the Pacific oyster (Crassostrea gigas) in China. Aquaculture 2006, 259, 95–102. [Google Scholar]
- Callen, D.F.; Thompson, A.D.; Shen, Y.; Phillips, H.A.; Mulley, J.C.; Sutherland, G.R. Incidence and origin of “null” alleles in the (AC)n microsatellite markers. Am. J. Hum. Genet 1993, 52, 922–927. [Google Scholar]
- Zhan, A.B.; Bao, Z.M.; Hu, X.L.; Hui, M.; Wang, M.L.; Peng, W.; Zhao, H.B.; Hu, J.J. Isolation and characterization of 150 novel microsatellite markers for Zhikong scallop (Chlamys farreri). Mol. Ecol. Notes 2007, 7, 1015–1022. [Google Scholar]
- Li, Q.; Park, C.; Endo, T.; Kijima, A. Loss of genetic variation at microsatellite loci in hatchery strains of the Pacific abalone (Haliotis discus hannai). Aquaculture 2004, 235, 207–222. [Google Scholar]
- Hara, M.; Sekino, M. Genetic differences between hatchery stocks and natural populations in Pacific Abalone (Haliotis discus) estimated using microsatellite DNA markers. Mar. Biotechnol 2007, 9, 74–81. [Google Scholar]
- National Fisheries Research and Development Institute (NFRDI), Commercial Molluscs from the Freshwater and Continental Shelf in Korea: Order Archaeogastropoda; NFRDI: Busan, Korea, 1999; pp. 21–22.
- Asahida, T.; Kobayashi, T.; Saitoh, K.; Nakayama, I. Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentrations of urea. Fish. Sci. Tokyo 1996, 62, 727–730. [Google Scholar]
- NCBI BLAST. The basic local alignment search tool of the national center for biotechnology information. Available online http://ncbi.nlm.nih.gov/blast accessed on 1 June, 2012.
- Van Oosterhout, C.; Hutchinson, W.F.; Wills, D.P.M.; Shipley, P. MICRO-CHECKER: Software for identifying and correcting genotyping errors in microsatellite data. Mol. Ecol. Notes 2004, 4, 535–538. [Google Scholar]
- Tiago, A.; Ana, L.; Ricardo, J.L.; Albano, B.-P.; Luikart, G. LOSITAN: A workbench to detect molecular adaptation based on a Fst-outlier method. BMC Bioinfo 2008, 9, 323–327. [Google Scholar]
- Rousset, F. Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol. Ecol. Resour 2008, 8, 103–106. [Google Scholar]
- Goudet, J. FSTAT: a program to estimate and test gene diversities and fixation indices (version 2.9.3.2). Available online: http://www2.unil.ch/popgen/softwares/fstat.htm accessed on 20 June, 2012.
- Weir, B.S.; Cockerham, C.C. Estimating F-statistics for the analysis of population structure. Evolution 1984, 38, 1358–1370. [Google Scholar]
- Excoffier, L.; Smouse, P.E.; Quattro, J.M. Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 1992, 131, 479–491. [Google Scholar]
- Excoffier, L.; Laval, G.; Schneider, S. ARLEQUIN version 3.0: An integrated software package for population genetics data analysis. Evol. Bioinf. Online 2005, 1, 47–50. [Google Scholar]
- Slatkin, M.; Excoffier, L. Testing for linkage disequilibrium in genotypic data using the EM algorithm. Heredity 1996, 76, 377–383. [Google Scholar]
- Rice, W.R. Analyzing tables of statistical tests. Evolution 1989, 43, 223–225. [Google Scholar]
- Cornuet, J.M.; Luikart, G. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 1996, 144, 2001–2014. [Google Scholar]
Locus | Repeat motif | Primer sequence (5′-3′) | Ta (°C) | Cross-amplification in H. diversicolor diversicolor | GenBank Accession No. |
---|---|---|---|---|---|
KHds1 | (GCT)8 | F: HEX-CTCAAAGTCTTGAAAGGTTCT R: AGGTGTCAAGTAGTCCTGAAA | 54 | + | JQ678720 |
KHds2 | (CA)7(AT)5 | F: FAM-ACGCCCTGTTACTTCTGATCC R: GACTGAAGTAAGTACTCGTGT | 54 | + | JQ678721 |
KHds3 | (CTCA)8 | F: HEX-GTCTGTGATGAAATGTAGTCT R: GAGATTACAACAGGTGATTGC | 54 | + | JQ678722 |
KHds4 | (GTAA)10 | F: HEX-CACGACACACAAATGATCATT R: GTTTCTGACAAAGTACTCGAG | 54 | + | JQ678723 |
KHds5 | (CCGCA)19 | F: HEX-CTCCGCTCTCCGGGCGGACGC R: CCATATCAGACTTCACGCTGTAATC | 54 | + | JQ678724 |
KHds6 | (GATT)9 | F: HEX-GGACTGATCTGTGGTAGAGCT R: GGAGACTACTATTCTCATGGA | 54 | + | JQ678725 |
KHds7 | (CA)8 | F: FAM-GGTATAATTCTCACATGCACG R: ATCTCATCGACTGGAGGGACA | 54 | + | JQ678726 |
KHds8 | (GTGA)8 | F: HEX-GCAGGGACACCTGATTTGAAC R: GCCTTTGCATGGTATGATCTA | 54 | + | JQ678727 |
KHds9 | (GATA)9 | F: FAM-ACTAGCAGTAACTGCGACACC R: GATCTCGGCACATGACTATAT | 54 | + | JQ678728 |
KHds10 | (TCA)9 | F: HEX-TCGTTAACATTCCCCGGAAAT R: ATCGAGGAAAATACCAGCGCC | 54 | + | JQ678729 |
KHds11 | (TGAG)8 | F: FAM-CCTGCAATCAGCATATCAAAA R: CTTACAGTGATACTGCTGGAT | 54 | + | JQ678730 |
KHds12 | (CTA)11 | F: FAM-TGGTATTCGTTACTACTACTAC R: GACATGGACATAGATAGACAA | 54 | + | JQ678731 |
KHds13 | (CCTCA)10 | F: HEX-AGCTAAACATTCTCAAGCACG R: GGCTATACTTCATAACCGATG | 54 | + | JQ678732 |
KHds14 | (TTTA)14 | F: HEX-CTAATTTACCCAGACTGTAAC R: AGTTACACCTCACCTTACCAA | 54 | + | JQ678733 |
KHds15 | (CATT)9 | F: FAM-TTGGCCTAATTTGGAAGCTAG R: CAATATGAGTCAGGTTAGATC | 54 | + | JQ678734 |
KHds16 | (TA)8 | F: FAM-GCGCCCAAAAAACCTGTCCCA R: TCAGCTGCCTGTTCTATTCAC | 54 | + | JQ678735 |
KHds17 | (CA)8 | F: FAM-AACCTAACATCCACGCACACG R: CAGTCTCCGAAACCCTATAAT | 54 | + | JQ678736 |
KHds18 | (GTGGGT)8 | F: HEX-CGGTGGTTGACTGTGTGTTGG R: CACAAGGACATTTAGTGGTTGA | 54 | + | JQ678737 |
KHds19 | (AC)10 | F: FAM-CGAAATCACACTTCATGCATT R: TGAAGACCACATGTGTGTGTG | 54 | + | JQ678738 |
KHds20 | (CTGT)8 | F: HEX-GAGCTGATCAAATGTGTAGTA R: AGTCTGGACTATACAATCCAG | 54 | + | JQ678739 |
Microsatellite loci | FST | Population (No.) | |||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Wild (60) | Released (60) | ||||||||||||||||
NA | S | F | U | He | Ho | FIS | p | NA | S | F | U | He | Ho | FIS | p | ||
KHds1 | −0.0026 | 9 | 100–136 | 0.627 | 2 | 0.590 | 0.593 | −0.005 | 0.494 | 11 | 100–136 | 0.678 | 0 | 0.530 | 0.475 | 0.105 | 0.002 * |
KHds5 | 0.0055 | 26 | 114–249 | 0.186 | 6 | 0.919 | 0.898 | 0.023 | 0.369 | 25 | 117–243 | 0.110 | 7 | 0.936 | 0.847 | 0.095 | 0.000 * |
KHds6 | 0.0100 | 7 | 106–142 | 0.678 | 1 | 0.504 | 0.525 | −0.044 | 0.673 | 6 | 106–124 | 0.784 | 2 | 0.369 | 0.328 | 0.113 | 0.011 |
KHds7 | −0.0010 | 21 | 110–169 | 0.517 | 6 | 0.717 | 0.810 | −0.131 | 0.923 | 18 | 110–169 | 0.483 | 5 | 0.736 | 0.746 | −0.013 | 0.901 |
KHds10 | −0.0051 | 12 | 96–130 | 0.220 | 1 | 0.851 | 0.915 | −0.076 | 0.772 | 12 | 100–130 | 0.203 | 1 | 0.859 | 0.695 | 0.193 | 0.003 * |
KHds11 | 0.0032 | 19 | 118–202 | 0.164 | 3 | 0.916 | 0.845 | 0.078 | 0.004 | 17 | 118–191 | 0.161 | 5 | 0.907 | 0.831 | 0.085 | 0.000 * |
KHds12 | −0.0023 | 17 | 186–249 | 0.169 | 2 | 0.908 | 0.915 | −0.008 | 0.006 | 16 | 186–255 | 0.188 | 3 | 0.902 | 0.938 | −0.040 | 0.158 |
KHds13 | 0.0012 | 11 | 102–152 | 0.216 | 1 | 0.863 | 0.914 | −0.059 | 0.191 | 10 | 92–142 | 0.259 | 2 | 0.840 | 0.569 | 0.325 | 0.000 * |
KHds14 | 0.0078 | 32 | 100–222 | 0.229 | 7 | 0.911 | 0.864 | 0.052 | 0.140 | 31 | 100–218 | 0.129 | 8 | 0.955 | 0.466 | 0.515 | 0.000 * |
KHds15 | 0.0033 | 13 | 138–244 | 0.300 | 3 | 0.817 | 0.883 | −0.083 | 0.607 | 11 | 138–196 | 0.314 | 5 | 0.817 | 0.804 | 0.016 | 0.148 |
KHds16 | 0.0046 | 13 | 90–144 | 0.288 | 7 | 0.831 | 0.746 | 0.104 | 0.454 | 17 | 84–144 | 0.297 | 3 | 0.842 | 0.729 | 0.136 | 0.125 |
KHds17 | 0.0017 | 15 | 102–140 | 0.207 | 5 | 0.872 | 0.828 | 0.051 | 0.321 | 14 | 104–134 | 0.225 | 2 | 0.863 | 0.833 | 0.035 | 0.172 |
KHds19 | −0.0040 | 11 | 120–146 | 0.183 | 1 | 0.878 | 0.783 | 0.108 | 0.081 | 9 | 120–138 | 0.220 | 1 | 0.857 | 0.797 | 0.071 | 0.176 |
Mean | 0.0016 | 15.8 | 0.306 | 3.5 | 0.814 | 0.809 | 0.013 | 15.2 | 0.312 | 3.4 | 0.801 | 0.697 | 0.123 |
Source of Variation | Sum of Squares | Variance Components | Percentage Variation (%) | p-Value |
---|---|---|---|---|
Among populations | 6.60 | 0.009 | 0.2 | 0.960 |
Among individuals within a population | 640.5 | 0.35 | 6.74 | <0.001 |
Within individuals | 568.0007 | 4.90 | 93.1 | <0.001 |
Total | 1215.04 | 5.26 |
© 2012 by the authors; licensee Molecular Diversity Preservation International, Basel, Switzerland. This article is an open-access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
An, H.S.; Lee, J.W.; Hong, S.W. 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. 2012, 13, 10750-10764. https://doi.org/10.3390/ijms130910750
An HS, Lee JW, Hong SW. 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. International Journal of Molecular Sciences. 2012; 13(9):10750-10764. https://doi.org/10.3390/ijms130910750
Chicago/Turabian StyleAn, Hye Suck, Jang Wook Lee, and Seong Wan Hong. 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" International Journal of Molecular Sciences 13, no. 9: 10750-10764. https://doi.org/10.3390/ijms130910750