Molecular sexing and population genetic inference using a sex-linked microsatellite marker in the nine-spined stickleback (Pungitius pungitius)
Tóm tắt
Sex-specific DNA markers can serve as tools for molecular sex identification, as well as for population genetic inferences. We investigated the potential utility of a microsatellite marker located on sex chromosomes for molecular sexing of Fennoscandian nine-spined sticklebacks (Pungitius pungitius). In addition, we assessed the patterns of allelic differentiation between X and Y chromosomes across the populations to examine if the sex chromosomes had been highly differentiated prior to the postglacial recolonization of Fennoscandia. A clear and consistent sex difference in allele size distribution was observed at the Stn19 locus throughout the 15 populations investigated. Males were distinguishable by the presence of distinct male-specific alleles, which were lacking in all females. There was no indication of recombination between sex and the Stn19 locus in the 647 individuals tested. The degree of genetic differentiation between the X and Y chromosomes was much higher than that of interpopulation differentiation in the respective chromosomes. Our results indicate that the Stn19 locus can be used for molecular sex identification in Fennoscandian nine-spined sticklebacks. The consistent pattern of high allelic differentiation between the X and Y chromosomes in these populations suggests that the sex chromosomes were already highly differentiated prior to the postglacial recolonization of Fennoscandia.
Tài liệu tham khảo
Devlin RH, Nagahama Y: Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture. 2002, 208: 191-364. 10.1016/S0044-8486(02)00057-1.
Aida T: On the inheritance of colour in a fresh-water fish Aplocheilus latipes Temminck and Aclegel, with special reference to sex-linked inheritance. Genetics. 1921, 6: 554-573.
Wing O: One-sided masculine and sex-linked inheritance in Lebistes reticulates. J Genet. 1922, 12: 137-144. 10.1007/BF02983077.
Yamamoto T: Sex differentiation. Fish Physiology. Edited by: Hoar W, Randall D. 1969, New York: Academic Press, 117-175. full_text.
Fernando AA, Phang VPE: Colour pattern inheritance in three domesticated varieties of guppy, Poecilia reticulata. Genet Aquacult III. 1990, 85: 320-
Withler RE, McPhail JD, Devlin RH: Electrophoretic polymorphism and sexual dimorphism in the freshwater and anadromous threespine sticklebacks (Gasterosteus aculeatus) of the Little Campbell River, British Columbia. Biochem Genet. 1986, 24: 701-713. 10.1007/BF00499003.
Allendorf FW, Gellman WA, Thorgaard GH: Sex-linkage of two enzyme loci in Oncorhynchus mykiss (rainbow trout). Heredity. 1994, 72: 498-507. 10.1038/hdy.1994.67.
Liu Q, Goudie CA, Simco BA, Davis KB: Sex-linkage of glucose phosphate isomerase-B and mapping of the sex-determining gene in channel catfish. Cytogenet Cell Genet. 1996, 73: 282-285. 10.1159/000134356.
Devlin RH, NcNeil BK, Groves TDD, Donaldson EM: Isolation of a Y-chromosomal DNA probe capable of determining genetic sex in chinook salmon (Oncorhynchus tshawytscha). Can J Fish Aquat Sci. 1991, 48: 1606-1612. 10.1139/f91-190.
Matsuda M, Kusama T, Oshiro T, Kurihara Y, Hamaguchi S, Sakaizumi M: Isolation of a sex chromosome-specific DNA sequence in the medaka, Oryzias latipes. Genes Genet Syst. 1997, 72: 263-268. 10.1266/ggs.72.263.
Iturra P, Medrano JF, Bagley M, Lam N, Vergara N, Marin JC: Identification of sex chromosome molecular markers using RAPDs and fluorescent in situ hybridization in rainbow trout. Genetica. 1998, 101: 209-213. 10.1023/A:1018371623919.
Griffiths R, Orr KJ, Adam A, Barber I: DNA sex identification in the three-spined stickleback. J Fish Biol. 2000, 57: 1331-1334. 10.1111/j.1095-8649.2000.tb00490.x.
Brunelli JP, Wertzler KJ, Sundin K, Thorgaard GH: Y-specific sequences and polymorphisms in rainbow trout and Chinook salmon. Genome. 2008, 51: 739-748. 10.1139/G08-060.
Jobling MA, Tyler-Smith C: The human Y chromosome: an evolutionary marker comes of age. Nat Rev Genet. 2003, 4: 598-612. 10.1038/nrg1124.
Greminger MP, Krützen M, Schelling C, Pienkowska-Schelling A, Wandeler P: The quest for Y-chromosomal markers - methodological strategies for mammalian non-model organisms. Mol Ecol Res. 2010, 10: 409-420. 10.1111/j.1755-0998.2009.02798.x.
Wilder JA, Kingan SB, Mobasher Z, Pilkington MM, Hammer MF: Global patterns of human mitochondrial DNA and Y-chromosome structure are not influenced by higher migration rates of females versus males. Nat Genet. 2004, 36: 1122-1125. 10.1038/ng1428.
Underhill PA, Kivisild T: Use of Y chromosome and mitochondrial DNA population structure in tracing human migrations. Ann Rev Genet. 2007, 41: 539-564. 10.1146/annurev.genet.41.110306.130407.
Brunelli JP, Steele CA, Thorgaard GH: Deep divergence and apparent sex-biased dispersal revealed by a Y-linked marker in rainbow trout. Mol Phylogenet Evol. 2010, 56: 983-990. 10.1016/j.ympev.2010.05.016.
Wootton RJ: The Biology of the Sticklebacks. 1976, New York: Academic Press
Bell MA, Foster SA: Introduction to the evolutionary biology of the threespine stickleback. The Evolutionary Biology of the Threespine Stickleback. Edited by: Bell MA, Foster SA. 1994, Oxford: Oxford University Press, 1-27.
Östlund-Nilsson S, Mayer I: The Biology of Other Sticklebacks. Biology of the Three-Spined Stickleback. Edited by: Östlund-Nilsson S, Mayer I, Huntingford FA. 2007, Boca Raton, FL: CRC Press, 353-372.
Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL: Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet. 2009, 5: e1000391-10.1371/journal.pgen.1000391.
Shapiro MD, Summers BR, Balabhadra S, Aldenhoven JT, Miller AL, Cunningham C, Bell MA, Kingsley DM: The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr Biol. 2009, 19: 1140-1145. 10.1016/j.cub.2009.05.029.
Nanda I, Feichtinger W, Schmid M, Schröder JH, Zischler H, Epplen JT: Simple repetitive sequences are associated with differentiation of the sex chromosomes in the guppy fish. J Mol Evol. 1990, 30: 456-462. 10.1007/BF02101117.
Shikano T, Shimada Y, Herczeg G, Merilä J: History vs. habitat type: explaining the genetic structure of European nine-spined stickleback (Pungitius pungitius) populations. Mol Ecol. 2010, 19: 1147-1161. 10.1111/j.1365-294X.2010.04553.x.
Elphinstone MS, Hinten GN, Anderson MJ, Nock CJ: An inexpensive and high-throughput procedure to extract and purify total genomic DNA for population studies. Mol Ecol Notes. 2003, 3: 317-320. 10.1046/j.1471-8286.2003.00397.x.
Mäkinen HS, Välimäki K, Merilä J: Cross-species amplification of microsatellite loci for nine-spined stickleback Pungitius pungitius. Ann Zool Fennici. 2007, 44: 218-224.
Ensembl. [http://www.ensembl.org/Gasterosteus_aculeatus/Info/Index]
Peichel CL, Nereng KS, Ohgi KA, Cole BL, Colosimo PF, Buerkle CA, Schluter D, Kingsley DM: The genetic architecture of divergence between threespine stickleback species. Nature. 2001, 414: 901-905. 10.1038/414901a.
Brownstein MJ, Carpten JD, Smith JR: Modulation of non-templated nucleotide addition by Taq DNA polymerase: primer modifications that facilitate genotyping. BioTechniques. 1996, 20: 1004-1010.
Goudet J: FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered. 1995, 86: 485-486.
Rice WR: Analyzing tables of statistical tests. Evolution. 1989, 43: 223-225. 10.2307/2409177.
Goldstein DB, Ruíz-Linares A, Feldman M, Cavalli-Sforza LL: Genetic absolute dating based on microsatellites and the origin of modern humans. Proc Natl Acad Sci USA. 1995, 92: 6720-6727. 10.1073/pnas.92.15.6723.
Dieringer D, Schlötterer C: Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes. 2003, 3: 167-169. 10.1046/j.1471-8286.2003.00351.x.
Langella O: Populations 1.2.28. Logiciel de génétique des populations. Gif-sur-Yvette: CNRS UPR9034. 2002
Ocalewicz K, Fopp-Bayat D, Woznicki P, Jankun M: Heteromorphic sex chromosomes in the ninespine stickleback Pungitius pungitius. J Fish Biol. 2008, 73: 456-462. 10.1111/j.1095-8649.2008.01902.x.
Lahn BT, Page DC: Four evolutionary strata on the human X chromosome. Science. 1999, 286: 964-967. 10.1126/science.286.5441.964.
Malaspina P, Ciminelli BM, Viggiano L, Jodice C, Cruciani F, Santolamazza P, Sellitto D, Scozzari R, Terrenato L, Rocchi M, Novelletto A: Characterization of a small family (CAIII) of microsatellite-containing sequences with X-Y homology. J Mol Evol. 1997, 44: 652-659. 10.1007/PL00006189.
Kotliarova ES, Toda T, Takenaka O, Matsushita I, Hida A, Shinka T, Goto J, Tokunaga K, Nakagome Y, Nakahori Y: Novel (CA) n marker DXYS241 on the nonrecombinant part of the human Y chromosome. Hum Biol. 1999, 71: 261-275.
Carvalho-Silva DR, Pena SD: Molecular characterization and population study of an X chromosome homolog of the Y-linked microsatellite DYS391. Gene. 2000, 247: 233-240. 10.1016/S0378-1119(00)00085-8.
Balaresque P, Toupance B, Heyer E, Crouau-Roy B: Evolutionary dynamics of duplicated microsatellites shared by sex chromosomes. J Mol Evol. 2003, 57: S128-S137. 10.1007/s00239-003-0018-z.
Scozzari R, Cruciani F, Malaspina P, Santolamazza P, Ciminelli BM, Torroni A, Modiano D, Wallace DC, Kidd KK, Olckers A, Moral P, Terrenato L, Akar N, Qamar R, Mansoor A, Mehdi SQ, Meloni G, Vona G, Cole DE, Cai W, Novelletto A: Differential structuring of human populations for homologous X and Y microsatellite loci. Am J Hum Genet. 1997, 61: 719-733. 10.1086/515500.
Karafet T, de Knijff P, Wood E, Ragland J, Clark A, Hammer MF: Different patterns of variation at the X- and Y-chromosome-linked microsatellite loci DXYS156X and DXYS156Y in human populations. Hum Biol. 1998, 70: 979-992.
Balaresque P, Manni F, Dugoujon JM, Crouau-Roy B, Heyer E: Estimating sex-specific processes in human populations: Are XY-homologous markers an effective tool?. Heredity. 2006, 96: 214-221. 10.1038/sj.hdy.6800779.