Isolation and characterization of new microsatellite markers for the Pacific geoduck (Panopea generosa ) using next generation sequencing
DOI:
https://doi.org/10.24275/uam/izt/dcbs/hidro/2018v28n1/RochaKeywords:
Microsatellite, Panopea generosa, Next-generation sequencing, genetic markersAbstract
Background. Panopea generosa is a large and long-lived infaunal clam with a considerable commercial value in Canada, United States and Mexico, in need of population genetic studies across its range of distribution. Goals. We set to develop new genetic markers (microsatellites) specific for P. generosa. Methods. We tested 30 microsatellite loci generated using next-generation genome sequencing (Illumina Hi-Seq 2500). Results. We identified eight as suitable polymorphic genetic markers. The number of alleles per locus ranged from 5 to 22 and heterozygosity from 0.429 to 0.818 (observed) and from 0.548 to 0.962 (expected). Deviation from Hardy-Weinberg equilibrium was found in three loci, after Dunn-Šidák correction, as a result of heterozygote deficiencies suggesting the presence of null alleles and linkage disequilibrium was found between two loci. Conclusions. These markers are highly informative and useful for population genetic studies aimed at informing management and conservation measures of this valuable resource.
Downloads
References
Abdelkrim, J., B. Robertson, J. A. Stanton & N. Gemmell. 2009. Fast, costeffective development of species-specific microsatellite markers by genomic sequencing. BioTechniques 46 (3):185-192. DOI:10.2144/000113084.
Ahanchede, A., J. E. F. Alfaya, L. W. Andersen, D. Azam, M. A. M. Bautista, A. L. Besnard, G. Bigatti, A. Bouetard, M. A. Coutellec, E. E. B. K. Ewedje, R. Fuseya, R. Garcia-Jimenez, M. Haratian, O. J. Hardy, L. E. Holm, C. W. Hoy, E. Koshimizu, V. Loeschcke, V. Lopez-Marquez, C. A. Machado, A. Machordom, C. Marchi, A. P. Michel, C. Micheneau, O. Mittapalli, T. Naga i, N. Okamoto, Y. Pan, F. Panitz, N. Safaie, T. Sakamoto, B. Sharifnabi, E. W. Tian, H. Yu & M. E. R. P. Dev. 2013. Permanent Genetic Resources added to Molecular Ecology Resources Database 1 August 2012-30 September 2012. Molecular Ecology Resources 13 (1):158-159. DOI:10.1111/1755-0998.12035.
Amos, W., J. I. Hoffman, A. Frodsham, L. Zhang, S. Best & A. V. S. Hill. 2007. Automated binning of microsatellite alleles: problems and solutions. Molecular Ecology Notes 7 (1):10-14. DOI:10.1111/j.1471-8286.2006.01560.x.
An, H. S. & J. W. Lee. 2012. Development of microsatellite markers for the Korean mussel, Mytilus coruscus (Mytilidae) using next-generation sequencing. International Journal of Molecular Sciences 13 (8):10583-10593. DOI:10.3390/ijms130810583.
Arag ón-Noriega, E. A., E. Alcántara-Razo, L. E. Calderón-Aguilera & R. Sánchez-Fourcade. 2012. Status of Geoduck clam fisheries in Mexico. Journal of Shellfish Research 31 (3):733-738. DOI:10.2983/035.031.0317.
Becquet, V., I. Lanneluc, B. Simon-Bouhet & P. García. 2009. Microsatellite markers for the Baltic clam, Macoma balthica (Linne, 1758), a key species concerned by changing southern limit, in exploited littoral ecosystems. Conservation Genetics Resources 1 (1): 265-267. DOI:10.1007/s12686-009-9065-0.
Bisbal-Pardo, C. I. 2014. Secuenciación masiva de Panopea generosa y Panopea globosa para el desarrollo de marcadores moleculares. Tesis de maestría, Centro de Investigación Científica y de Educación Superior de Ensenada, B.C., México.
Bisbal-Pardo, C. I., M. Á. Del Río-Portilla, A. Y. Castillo-Paéz & A. Rocha-Olivares. 2016. Isolation and characterization of new microsatellite markers for the cortés Geoduck (Panopea globosa). CICIMAR Oceánides 31 (1): 17-22.
Bureau, D., W. Hajas, N. Surry, C. Hand, G. Dovey & A. Campbell. 2002. Age, size structure and growth parameters of geoducks (Panopea abrupta, Conrad 1849) from 34 locations in British Columbia sampled between 1993 and 2000. Canadian Technical Report of Fisheries and Aquatic Sciences 2413:1-84.
Calderón-Aguilera, L. E., E. A. Arag ón-Noriega, C. M. Hand & V. M. Moreno-Rivera. 2010. Morphometric relationships, age, growth, and mortality of the geoduck clam, Panopea generosa, along the Pacific coast of Baja California, Mexico. Journal of Shellfish Research 29 (2): 319-326. DOI:10.2983/035.029.0206.
Castoe, T. A., A. W. Poole, A. P. J. de Koning, K. L. Jones, D. F. Tomback, S. J. Oyler-McCance, J. A. Fike, S. L. Lance, J. W. Streicher, E. N. Smith & D. D. Pollock. 2012. Rapid microsatellite identification from Illumina paired-end genomic sequencing in two birds and a snake. PLoS One 7 (2): e30953. DOI:10.1371/journal.pone.0030953.
Castoe, T. A., A. W. Poole, W. Gu, A. P. J. de Koning, J. M. Daza, E. N. Smith & D. D. Pollock. 2010. Rapid identification of thousands of copperhead snake (Agkistrodon contortrix) microsatellite loci from modest amounts of 454 shotgun genome sequence. Molecular Ecology Resources 10 (2): 341-347. DOI:10.1111/j.1755-0998.2009.02750.x.
Cruz-Hernández, P., A. Munguia-Vega, I. Leyva-Valencia, F. Lucero-Burquez & D. B. Lluch-Cota, 2014. Development of 24 tetra-nucleotide microsatellite markers in Cortes Geoduck Panopea globosa by next-generation sequencing. Conservation Genetics Resources 6 (3): 531-533. DOI:10.1007/s12686-014-0172-1.
Csencsics, D., S. Brodbeck & R. Holderegger . 2010. Cost-effective, speciesspecific microsatellite development for the endangered dwarf bulrush (Typha minima) using next-generation sequencing technology. Journal of Heredity 101 (6): 789-793. DOI:10.1093/Jhered/Esq069.
Ekblom, R. & J. Galindo. 2011. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity 107 (1):1. DOI:10.1038/hdy.2010.152.
Evans, S. R. & B. C. Sheldon. 2008. Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conservation Biology 22 (4): 1016-25. DOI:10.1111/j.1523-1739.2008.00972.x.
Excoffier, L., G. Lava l & S. Schneider. 2005. Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
Greenley, A. P., A. Muguía-Vega, A. Saenz-Arroyo & F. Micheli. 2012. New tetranucleotide microsatellite loci in pink abalone (Haliotis corrugata) isolated via 454 pyrosequencing. Conservation Genetics Resources 4 (2): 265-268. DOI:10.1007/s12686-011-9521-5.
Guichoux, E., L. Laga che, S. Wag ner, P. Chaumeil, P. Leger, O. Lepais, C. Lepoittevin, T. Malausa, E. Revardel, F. Salin & R. J. Petit. 2011. Current trends in microsatellite genotyping. Molecular Ecology Resources 11 (4): 591-611. DOI:10.1111/J.1755-0998.2011.03014.X.
Hedgecock, D., G. Li, S. Hubert, K. Bucklin & V. Ribes. 2004. Widespread null alleles and poor cross-species amplification of microsatellite DNA loci cloned from the Pacific oyster, Crassostrea gigas. Journal of Shellfish Research 23 (2): 379-385.
Huang, J., Y. Z. Li, L. M. Du, B. Yang, F. J. Shen, H. M. Zhang, Z. H. Zhang, X. Y. Zhang & B. S. Yue. 2015. Genome-wide survey and analysis of microsatellites in giant panda (Ailuropoda melanoleuca), with a focus on the applications of a novel microsatellite marker system. BMC Genomics 16: 61. DOI:10.1186/s12864-015-1268-z.
Inoue, K., B. K. Lang & D. J. Berg. 2013. Development and characterization of 20 polymorphic microsatellite markers for the Texas hornshell, Popenaias popeii (Bivalvia: Unionidae), through next-generation sequencing. Conservation Genetics Resources 5 (1): 195-198. DOI:10.1007/s12686-012-9766-7.
Jarne, P. & P. J. L. Lag oda. 1996. Microsatellites, from molecules to populations and back. Trends in Ecology & Evolution 11 (10): 424-429. DOI:10.1016/0169-5347(96)10049-5.
Kaukinen, K., K. Supernault & K. Miller. 2004. Enrichment of tetranucleotide microsatellite loci from invertebrate species. Journal of Shellfish Research 23 (2): 621-627.
Lance, S. L., C. N. Love, S. O. Nunziata, J. R. O’Bryhim, D. E. Scott, R. W. Flynn & K. L. Jones. 2013. 32 species validation of a new Illumina pairedend approach for the development of microsatellites. PLoS One 8 (11): e81853. DOI:10.1371/journal.pone.0081853.
McInerney, C. E., A. L. Allcock, M. P. Johnson, D. A. Bailie & P. A. Prodohl.2011. Comparative genomic analysis reveals species-dependent complexities that explain difficulties with microsatellite marker development in molluscs. Heredity 106 (1): 78-87. DOI:10.1038/hdy.2010.36.
Miller, K. M., K. J. Supernault, S. Li & R. E. Withler. 2006. Population Structure in Two Marine Invertebrate Species (Panopea abrupta and Strongylocentrotus franciscanus) Targeted for Aquaculture and Enhancement in British Columbia. Journal of Shellfish Research 25 (1): 33-42. DOI:10.2983/0730-8000(2006)25[33:psitmi]2.0.co;2.
Mira, Ó., J. G. Martínez, D. A. Daw son, A. Tinaut & C. Sánchez-Prieto. 2014. Twenty new microsatellite loci for population structure and parentage studies of Parnassius apollonevadensis (Lepidoptera; Papilionidae). Journal of insect conservation 18 (5): 771-779. DOI:10.1007/s10841-014-9683-z.
O’Bryhim, J., J. P. Chong, S. L. Lance, K. L. Jones & K. J. Roe. 2012. Development and characterization of sixteen microsatellite markers for the federally endangered species: Leptodea leptodon (Bivalvia: Unionidae) using paired-end Illumina shotgun sequencing. Conservation Genetics Resources 4 (3): 787-789. DOI:10.1007/s12686-012-9644-3.
Orensanz, J., C. M. Hand, A. M. Parma, J. Valero & R. Hilborn. 2004. Precaution in the harvest of Methuselah’s clams the difficulty of getting timely feedback from slow-paced dynamics. Canadian Journal of Fisheries and Aquatic Sciences 61 (8): 1355-1372. DOI:10.1139/F04-136.
Park, S. 2001. MStools v 3 (Excel spreadsheet toolkt for data conversion). Smurfit Institute of Genetics. Trinity College, Dublin.
Peñarrubia, L., N. Sanz, C. Pla, O. Vidal & J. Viñas. 2015. Using massive parallel sequencing for the development, validation, and application of population genetics markers in the invasive bivalve zebra mussel (Dreissena polymorpha). PLoS One 10 (3): e0120732. DOI:10.1371/journal.pone.0120732.
Selkoe, K. A. & R. J. Toonen. 2006. Microsatellites for ecologists: a practical
guide to using and evaluating microsatellite markers. Ecology Letters 9 (5): 615-629. DOI:10.1111/j.1461-0248.2006.00889.x.
Šidák, Z. K., 1967. Rectangular confidence regions for the means of multivariate normal distributions. Journal of the American Statistical Association 62 (318): 626-633. DOI:10.1080/01621459.1967.10482935.
Sloan, N. & S. Robinson. 1984. Age and gonadal development in the geoduck clam Panope abrupta (Conrad) from southern British Columbia, Canada. Journal of Shellfish Research 4:131-137.
Straus, K. M., L. M. Crosson & B. Vadopalas. 2008. Effects of Geoduck Aquaculture on the Environment: A Synthesis of Current Knowledge. School of Aquatic and Fishery Sciences, University of Washington, Washington, 67 p.
Suárez-Moo, P. J., E. A. Gilbert-Horvath, B. Vadopalas, L. E. Calderón-Aguilera, J. C. Garza & A. Rocha-Olivares. 2016. Genetic homogeneity of the geoduck clam Panopea generosa in the northeast Pacific. Biochemical
Systematics and Ecology 65: 66-71. DOI:10.1016/j.bse.2016.02.003.
Taberlet, P. & G. Luikart. 1999. Non-invasive genetic sampling and individual identification. Biological Journal of the Linnean Society 68 (1-2): 41-55. DOI:10.1111/j.1095-8312.1999.tb01157.x.
Vadopalas, B. & P. Bentzen. 2000. Isolation and characterization of diand tetranucleotide microsatellite loci in geoduck clams, Panopea abrupta. Molecular Ecology 9 (9): 1435-1436. DOI:10.1046/J.1365-294x.2000.01000-2.X.
Vadopalas, B., L. L. Leclair & P. Bentzen. 2004. Microsatellite and allozyme analyses reveal few genetic differences among spatially distinct aggregations of geoduck clams (Panopea abrupta, Conrad 1849). Journal of Shellfish Research 23 (3): 693-706.
Vadopalas, B., L. L. Leclair & P. Bentzen. 2012. Temporal Genetic Similarity Among Year-Classes of the Pacific Geoduck Clam (Panopea generosa Gould 1850): A Species Exhibiting Spatial Genetic Patchiness. Journal of Shellfish Research 31 (3): 697-709. DOI:10.2983/035.031.0314.
Vadopalas, B., T. W. Pietsch & C. S. Friedman. 2010. The proper name for the geoduck: resurrection of Panopea generosa Gould, 1850, from the synonymy of Panopea abrupta (Conrad, 1849) (Bivalvia: Myoida: Hiatellidae). Malacologia 52 (1): 169-173. DOI:10.4002/040.052.0111.
Van Oosterhout, C., W. F. Hutchinson, D. P. M. Wills & P. Shipley. 2004. MICROCHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4 (3): 535-538.
Xiao, Y. J., D. F. Cai, W. Yang, W. Ye, M. Younas, J. S. Wu & K. D. Liu. 2012. Genetic structure and linkage disequilibrium pattern of a rapeseed (Brassica napus L.) association mapping panel revealed by microsatellites. Theoretical and Applied Genetics 125 (3): 437-447. DOI:10.1007/s00122-012-1843-5.
Zane, L., L. Bargelloni & T. Patarnello. 2002. Strategies for microsatellite isolation: a review. Molecular Ecology 11 (1): 1-16. DOI:10.1046/j.0962-1083.2001.01418.x.
Downloads
Published
How to Cite
Issue
Section
License
Los autores/as que publiquen en esta revista aceptan las siguientes condiciones:
De acuerdo con la legislación de derechos de autor, HIDROBIOLÓGICA reconoce y respeta el derecho moral de los autores, así como la titularidad del derecho patrimonial, el cual será cedido a la revista para su difusión en acceso abierto.
Publicar en la revista HIDROBIOLÓGICA tiene un costo de recuperación de $500 pesos mexicanos por página en blanco y negro (aproximadamente 29 dólares americanos) y $1000 pesos por página a color (aproximadamente 58 dólares americanos).
Todos los textos publicados por HIDROBIOLÓGICA sin excepción se distribuyen amparados bajo la licencia Creative Commons 4.0Atribución-No Comercial (CC BY-NC 4.0 Internacional), que permite a terceros utilizar lo publicado siempre que mencionen la autoría del trabajo y a la primera publicación en esta revista.
Los autores/as pueden realizar otros acuerdos contractuales independientes y adicionales para la distribución no exclusiva de la versión del artículo publicado en HIDROBIOLÓGICA (por ejemplo incluirlo en un repositorio institucional o publicarlo en un libro) siempre que indiquen claramente que el trabajo se publicó por primera vez en HIDROBIOLÓGICA.
Para todo lo anterior, el o los autor(es) deben remitir el formato de Carta-Cesión de la Propiedad de los Derechos de la primera publicación debidamente requisitado y firmado por el autor(es). Este formato se puede enviar por correo electrónico en archivo pdf al correo: enlacerebvistahidrobiológica@gmail.com; rehb@xanum.uam.mx (Carta-Cesión de Propiedad de Derechos de Autor).
Esta obra está bajo una licencia de Creative Commons Reconocimiento-No Comercial 4.0 Internacional.