Salmonid chromosome evolution as revealed by a novel method for comparing radseq linkagemaps

Genome Biology and Evolution

Volumn 8, Issue 12, 2016, Pages 3600-3617

  Sutherland, Ben J G ^a   Gosselin, Thierry ^a   Normandeau, Eric ^a   Lamothe, Manuel ^b   Isabel, Nathalie ^b   Audet, Céline ^c   Bernatchez, Louis ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b LAURENTIAN FORESTRY CENTRE   (Canada)

^c INSTITUT DES SCIENCES DE LA MER DE RIMOUSKI   (Canada)

Author keywords

Comparative genomics; Linkage map; RADseq; Salmon; Whole genome duplication

Indexed keywords

ANIMAL; CHROMOSOMAL MAPPING; CHROMOSOME; GENE DUPLICATION; GENETIC LINKAGE; GENETICS; GENOME; MOLECULAR EVOLUTION; PHYLOGENY; SALMONID; SYNTENY;

ANIMALS; CHROMOSOME MAPPING; CHROMOSOMES; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENETIC LINKAGE; GENOME; PHYLOGENY; SALMONIDAE; SYNTENY;

EID: 85014366721     PISSN: None     EISSN: 17596653     Source Type: Journal    
DOI: 10.1093/gbe/evw262     Document Type: Article

References (77)

1. Aljanabi SM, Martinez I. 1997. Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Res. 25:4692-4693.
2. Allendorf FW, et al. 2015. Effects of crossovers between homeologs on inheritance and population genomics in polyploid-derived salmonid fishes. J Hered. 106:217-227.
3. Allendorf FW, Thorgaard GH. 1984. Tetraploidy and the evolution of salmonid fishes. In: Turner BJ, editors. Evolutionary genetics of fishes. New York: Plenum Publishing Corporation. 1-53.
4. Amores A, et al. 2014. A RAD-tag genetic map for the Platyfish (Xiphophorus maculatus) reveals mechanisms of karyotype evolution among teleost fish. Genetics 197:625-641.
5. Amores A, Catchen J, Ferrara A, Fontenot Q, Postlethwait JH. 2011. Genome evolution and meiotic maps by massively parallel DNA sequencing: spotted Gar, an outgroup for the teleost genome duplication. Genetics 188:799-808.
6. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. 2016. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet. 17:81-92.
7. Baird NA, et al. 2008. Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376.
8. Berthelot C, et al. 2014. The Rainbow Trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun. 5:3657.
9. Brelsford A, Dufresnes C, Perrin N. 2016. High-density sex-specific linkage maps of a European tree frog (Hyla arborea) identify the sex chromosome without information on offspring sex. Heredity 116:177-181.
10. Brieuc MSO, et al. 2014. A dense linkage map for Chinook Salmon (Oncorhynchus tshawytscha) reveals variable chromosomal divergence after an ancestral whole genome duplication event. G3 Genes Genomes Genet. 4:447-460.
11. Brunet FG, et al. 2006. Gene loss and evolutionary rates following wholegenome duplication in teleost fishes. Mol Biol Evol. 23:1808-1816.
12. Cariou M, Duret L, Charlat S. 2013. Is RAD-seq suitable for phylogenetic inference? An in silico assessment and optimization. Ecol Evol. 3:846-852.
13. Catchen J, Hohenlohe PA, Bassham S, Amores A, Cresko WA. 2013. Stacks: an analysis tool set for population genomics. Mol Ecol. 22:3124-3140.
14. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH. 2011. Stacks: building and genotyping loci de novo from short-read sequences. G3 Genes Genomes Genet. 1:171-182.
15. Crête-Lafrenière A, Weir LK, Bernatchez L. 2012. Framing the Salmonidae Family phylogenetic portrait: a more complete picture from increased taxon sampling Fontaneto, D, editor. PLoS One 7:e46662.
16. Danzmann RG, et al. 2005. A comparative analysis of the rainbow trout genome with 2 other species of fish (Arctic charr and Atlantic salmon) within the tetraploid derivative Salmonidae family (subfamily: Salmoninae). Genome 48:1037-1051.
17. Danzmann RG, et al. 2008. Distribution of ancestral proto-Actinopterygian chromosome arms within the genomes of 4R-derivative salmonid fishes (Rainbow Trout and Atlantic Salmon). BMC Genomics 9:557.
18. Davidson WS, et al. 2010. Sequencing the genome of the Atlantic Salmon (Salmo salar). Genome Biol. 11:403.
19. Elshire RJ, et al. 2011. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379.
20. Everett MV, Miller MR, Seeb JE. 2012. Meiotic maps of Sockeye Salmon derived frommassively parallel DNA sequencing. BMCGenomics 13:521.
21. Fang Z, et al. 2003. cMap: the comparative genetic map viewer. Bioinformatics 19:416-417.
22. Fierst JL. 2015. Using linkage maps to correct and scaffold de novo genome assemblies: methods, challenges, and computational tools. Front Genet. 6:220.
23. Force A, et al. 1999. Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
24. Gagnaire P-A, Normandeau E, Pavey SA, Bernatchez L. 2013. Mapping phenotypic, expression and transmission ratio distortion QTL using RAD markers in the Lake Whitefish (Coregonus clupeaformis). Mol Ecol. 22:3036-3048.
25. Gonen S, et al. 2014. Linkage maps of the Atlantic Salmon (Salmo salar) genome derived from RAD sequencing. BMC Genomics 15:166.
26. Gonen S, Bishop SC, Houston RD. 2015. Exploring the utility of crosslaboratory RAD-sequencing datasets for phylogenetic analysis. BMC Res Notes 8:299.
27. Gosselin T, Bernatchez L. 2016. stackr: GBS/RAD Data Exploration, Manipulation and Visualization using R. Available from: https://github.com/thierrygosselin/stackr.
28. Grattapaglia D, Sederoff R. 1994. Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121-1137.
29. Gregory TR. 2016. Animal genome size database. Available from: http://www.genomesize.com.
30. Henning F, Lee HJ, Franchini P, Meyer A. 2014. Genetic mapping of horizontal stripes in Lake Victoria cichlid fishes: benefits and pitfalls of using RAD markers for dense linkage mapping. Mol Ecol. 23:5224-5240.
31. Ilut DC, Nydam ML, Hare MP. 2014. Defining loci in restriction-based reduced representation genomic data from nonmodel species: sources of bias and diagnostics for optimal clustering. Biomed Res Int. 2014:675158.
32. Kinnison MT, Hendry AP. 2004. From macro-to micro-evolution. In: Hendry AP, Stearns SC, editors. Evolution illuminated: salmon and their relatives. Oxford: Oxford University Press. p. 208-231.
33. Kirkpatrick M. 2010. How and why chromosome inversions evolve. PLoS Biol. 8:e1000501.
34. Kirubakaran TG, et al. 2016. Two adjacent inversions maintain genomic differentiation between migratory and stationary ecotypes of Atlantic cod. Mol Ecol. 25:2130-2143.
35. Kodama M, Brieuc MSO, Devlin RH, Hard JJ, Naish KA. 2014. Comparative mapping between Coho Salmon (Oncorhynchus kisutch) and three other salmonids suggests a role for chromosomal rearrangements in the retention of duplicated regions following a whole genome duplication event. G3 Genes Genomes Genet. 4:1717-1730.
36. Larson WA, et al. 2016. Identification of multiple QTL hotspots in Sockeye Salmon (Oncorhynchus nerka) using genotyping-by-sequencing and a dense linkage map. J Hered. 107:122-133.
37. Lee GM, Wright JE. 1981. Mitotic and meiotic analyses of Brook Trout, Salvelinus fontinalis. J Hered. 72:321-327.
38. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760.
39. Lien S, et al. 2011. A dense SNP-based linkage map for Atlantic Salmon (Salmo salar) reveals extended chromosome homeologies and striking differences in sex-specific recombination patterns. BMC Genomics 12:615.
40. Lien S, et al. 2016. The Atlantic salmon genome provides insights into rediploidization. Nature 553:200-205. doi: 10.1038/nature17164.
41. LimborgMT, Seeb LW, Seeb JE. 2016. Sorting duplicated loci disentangles complexities of polyploid genomes masked by genotyping by sequencing. Mol Ecol. 25:2117-2129. doi: 10.1111/mec.13600.
42. Limborg MT, Waples RK, Allendorf FW, Seeb JE. 2015. Linkage mapping reveals strong chiasma interference in Sockeye Salmon: implications for interpreting genomic data. G3 Genes Genomes Genet. 5:2463-2473.
43. Limborg MT, Waples RK, Seeb JE, Seeb LW. 2014 Temporally isolated lineages of pink salmon reveal unique signatures of selection on distinct pools of standing genetic variation. J Hered. 105:741-751.
44. Macqueen DJ, Johnston IA. 2014. A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proc R Soc B Biol Sci. 281:20132881-20132881.
45. Martin M. 2011. Cutadapt removes adapter sequences from highthroughput sequencing reads. EMBnet J. 17:10.
46. Mascher M, Stein N. 2014 Genetic anchoring of whole-genome shotgun assemblies. Front Genet. 5:208.
47. May B, Delany ME. 2015. Meiotic models to explain classical linkage, pseudolinkage, and chromosomal pairing in tetraploid derivative salmonid genomes: II. Wright is still right. J Hered. 106:762-766.
48. McKinney GJ, et al. 2016. An integrated linkage map reveals candidate genes underlying adaptive variation in Chinook Salmon (Oncorhynchus tshawytscha). 16:769-783.
49. Miller MR, et al. 2012. A conserved haplotype controls parallel adaptation in geographically distant salmonid populations.Mol Ecol. 21:237-249.
50. Ming R, Man Wai C. 2015. Assembling allopolyploid genomes: no longer formidable. Genome Biol. 16:27.
51. Naish KA, et al. 2013. Comparative genome mapping between Chinook Salmon (Oncorhynchus tshawytscha) and Rainbow Trout (O. mykiss) based on homologous microsatellite loci. G3 Genes Genomes Genet. 3:2281-2288.
52. Noor MA, Grams KL, Bertucci LA, Almendarez Y, et al. 2001. The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution 55:512-521.
53. Noor MA, Grams KL, Bertucci LA, Reiland J. 2001. Chromosomal inversions and the reproductive isolation of species. Proc Natl Acad Sci. 98:12084-12088.
54. Ohno S. 1970. Evolution by gene duplication. Berlin, Heidelberg: Springer Berlin Heidelberg.
55. Ostberg CO, Hauser L, Pritchard VL, Garza JC, Naish KA. 2013. Chromosome rearrangements, recombination suppression, and limited segregation distortion in hybrids between Yellowstone Cutthroat Trout (Oncorhynchus clarkii bouvieri) and Rainbow Trout (O. mykiss). BMC Genomics 14:570.
56. Palti Y, et al. 2015. Detection and validation of QTL affecting bacterial cold water disease resistance in Rainbow Trout using restriction-site associated DNA sequencing Wang, H, editor. PLoS One 10:e0138435.
57. Pante E, et al. 2014. Use of RAD sequencing for delimiting species. Heredity 114:450-459.
58. Phillips R, Ráb P. 2001. Chromosome evolution in the Salmonidae (Pisces): an update. Biol Rev Camb Philos Soc. 76:1-25.
59. Phillips RB, et al. 2009. Assignment of Atlantic Salmon (Salmo salar) linkage groups to specific chromosomes: conservation of large syntenic blocks corresponding to whole chromosome arms in Rainbow Trout (Oncorhynchus mykiss). BMC Genet. 10:46.
60. Phillips RB, et al. 2006. Assignment of Rainbow Trout linkage groups to specific chromosomes. Genetics 174:1661-1670.
61. Poland JA, Brown PJ, Sorrells ME, Jannink J-L. 2012. Development of highdensity genetic maps for barley and wheat using a novel two-enzyme Genotyping-by-Sequencing approach Yin, T, editor. PLoS One 7:e32253.
62. Rieseberg LH. 2001. Chromosomal rearrangements and speciation. Trends Ecol Evol. 16:351-358.
63. Rondeau EB, et al. 2014. The genome and linkage map of the Northern Pike (Esox lucius): conserved synteny revealed between the salmonid sister group and the Neoteleostei. PLoS One 9: e102089.
64. Sakamoto T, et al. 2000. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155:1331-1345.
65. Sankoff D, Zheng C, Zhu Q. 2010. The collapse of gene complement following whole genome duplication. BMC Genomics 11(1):313.
66. Sarropoulou E, Nousdili D, Magoulas A, Kotoulas G. 2008 Linking the genomes of nonmodel teleosts through comparative genomics. Mar Biotechnol. 10:227-233.
67. Sauvage C, Vagner M, Derôme N, Audet C, Bernatchez L. 2012. Coding gene single nucleotide polymorphism mapping and quantitative trait loci detection for physiological reproductive traits in Brook Charr, Salvelinus fontinalis. G3 Genes Genomes Genet. 2:379-392.
68. Sauvage C, Vagner M, Derôme N, Audet C, Bernatchez L. 2012. Coding gene SNPmapping reveals QTL linked to growth and stress response in Brook Charr (Salvelinus fontinalis). G3 Genes Genomes Genet. 2:707-720.
69. Stearley RF, Smith GR. 1993. Phylogeny of the Pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae. Trans Am Fisheries Soc. 122:1-33.
70. Timusk ER, et al. 2011. Genome evolution in the fish family salmonidae: generation of a Brook Charr genetic map and comparisons among charrs (Arctic Charr and Brook Charr) with Rainbow Trout. BMC Genet. 12:68.
71. van Ooijen JW. 2006. JoinMap4: software for the calculation of genetic linkage maps in experimental populations. Available from: https://www.kyazma.nl/docs/JM4manual.pdf.
72. van Ooijen JW. 2011. Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res (Camb). 93:343-349.
73. van Ooijen JW, Jansen J. 2013. Genetic mapping in experimental populations. Cambridge: Cambridge University Press.
74. Waples RK, Seeb LW, Seeb JE. 2016. Linkage mapping with paralogs exposes regions of residual tetrasomic inheritance in Chum Salmon (Oncorhynchus keta). Mol Ecol Resour. 16:17-28.
75. Woram RA, et al. 2004. A genetic linkage map for Arctic Char (Salvelinus alpinus): evidence for higher recombination rates and segregation distortion in hybrid versus pure strainmapping parents. Genome 47:304-315.
76. Wright JE, Johnson K, Hollister A, May B. 1983. Meiotic models to explain classical linkage, pseudolinkage, and chromosome pairing in tetraploid derivative salmonid genomes. Isozymes Curr Top Biol Med Res. 10:239-260.
77. Wu R, Ma C-X, Painter I, Zeng Z-B. 2002. Simultaneous maximum likelihood estimation of linkage and linkage phases in outcrossing species. Theor Popul Biol. 61:349-363.