An integrated linkage map reveals candidate genes underlying adaptive variation in Chinook salmon (Oncorhynchus tshawytscha)

Molecular Ecology Resources

Volumn 16, Issue 3, 2016, Pages 769-783

  Mckinney, G J ^a   Seeb, L W ^a   Larson, W A ^a   Gomez Uchida, D ^a,b   Limborg, M T ^a,c   Brieuc, M S O ^a   Everett, M V ^a,d   Naish, K A ^a   Waples, R K ^a   Seeb, J E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CONCEPCIÓN   (Chile)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d NORTHWEST FISHERIES SCIENCE CENTER   (United States)

Author keywords

Adaptation; Duplicated genome; Linkage mapping; Population differentiation; RAD sequence

Indexed keywords

ADAPTATION; ANIMAL; CHROMOSOMAL MAPPING; CLASSIFICATION; EXPRESSED SEQUENCE TAG; GENETIC VARIATION; GENETICS; MOLECULAR GENETICS; POPULATION GENETICS; SALMONINE; SINGLE NUCLEOTIDE POLYMORPHISM;

ADAPTATION, BIOLOGICAL; ANIMALS; CHROMOSOME MAPPING; EXPRESSED SEQUENCE TAGS; GENETIC VARIATION; GENETICS, POPULATION; MOLECULAR SEQUENCE ANNOTATION; POLYMORPHISM, SINGLE NUCLEOTIDE; SALMON;

EID: 84962886293     PISSN: 1755098X     EISSN: 17550998     Source Type: Journal    
DOI: 10.1111/1755-0998.12479     Document Type: Article

References (70)

1. Berthelot C, Brunet F, Chalopin D et al. (2014) The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nature Communications, 5, 3657.
2. de Boer JG, Yazawa R, Davidson WS, Koop BF (2007) Bursts and horizontal evolution of DNA transposons in the speciation of pseudotetraploid salmonids. BMC Genomics, 8, 422.
3. Bourret V, Kent MP, Primmer CR et al. (2013) SNP-array reveals genome-wide patterns of geographical and potential adaptive divergence across the natural range of Atlantic salmon (Salmo salar). Molecular Ecology, 22, 532-551.
4. Bradbury IR, Hubert S, Higgins B et al. (2013) Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish. Evolutionary Applications, 6, 450-461.
5. Brieuc MSO, Waters CD, Seeb JE, Naish KA (2014) A dense linkage map for Chinook salmon (Oncorhynchus tshawytscha) reveals variable chromosomal divergence following an ancestral whole genome duplication event. Genes Genomes Genetics, 4, 447-460.
6. Brieuc MS, Ono K, Drinan D, Naish KA (2015) Integration of Random Forest with population-based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchustshawytscha). Molecular Ecology, 24, 2729-2746.
7. Brown CA, Murray AW, Verstrepen KJ (2010) Rapid expansion and functional divergence of subtelomeric gene families in yeasts. Current Biology, 20, 895-903.
8. Catchen JM, Amores A, Hohenlohe P, Cresko W, Postlethwait JH (2011) Stacks: building and genotyping loci de novo from short-read sequences. Genes Genomes Genetics, 1, 171-182.
9. Corduan A, Lecomte S, Martin C, Michel D, Desmots F (2009) Sequential interplay between BAG6 and HSP70 upon heat shock. Cellular and Molecular Life Sciences, 66, 1998-2004.
10. Crete-Lafreniere A, Weir LK, Bernatchez L (2012) Framing the Salmonidae family phylogenetic portrait: a more complete picture from increased taxon sampling. PLoS ONE, 7, e46662.
11. Davidson WS, Koop BF, Jons SJM et al. (2010) Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biology, 11, 403.
12. Doerge RW (2002) Mapping and analysis of quantitative trait loci in experimental populations. Nature Reviews Genetics, 3, 43-52.
13. Dorion S, Landry J (2002) Activation of the mitogen-activated protein kinase pathways by heat shock. Cell Stress and Chaperones, 7, 200-206.
14. Dufresne F, Stift M, Vergilino R, Mable BK (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state-of-the-art molecular and statistical tools. Molecular Ecology, 23, 40-69.
15. Everett MV, Seeb JE (2014) Detection and mapping of QTL for temperature tolerance and body size in Chinook salmon (Oncorhynchus tshawytscha) using genotyping by sequencing. Evolutionary Applications, 7, 480-492.
16. Everett MV, Miller MR, Seeb JE (2012) Meiotic maps of sockeye salmon derived from massively parallel DNA sequencing. BMC Genomics, 13, 521.
17. Excoffier L, Lischer HE (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources, 10, 564-567.
18. Fedorova ND, Khaldi N, Joardar VS et al. (2008) Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PLoS Genetics, 4, e1000046.
19. Gagnaire P-A, Pavey SA, Normandeau E, Bernatchez L (2013) The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish species pairs assessed by RAD sequencing. Evolution, 67, 2483-2497.
20. Gomez-Uchida D, Seeb LW, Warheit KI, McKinney GJ, Seeb JE (2014) Deep sequencing of the transcriptome and mining of single nucleotide polymorphisms (SNPs) provide genomic resources for applied studies in Chinook salmon (Oncorhynchus tshawytscha). Conservation Genetics Resources, 6, 807-811.
21. Gonen S, Lowe NR, Cezard T et al. (2014) Linkage maps of the Atlantic salmon (Salmo salar) genome derived from RAD sequencing. BMC Genomics, 15, 166.
22. Goodier JL, Davidson WS (1994) Tc1 transposon-like sequences are widely distributed in Salmonids. Journal of Molecular Biology, 241, 26-34.
23. Hecht BC, Campbell NR, Holecek DE, Narum SR (2013) Genome-wide association reveals genetic basis for the propensity to migrate in wild populations of rainbow and steelhead trout. Molecular Ecology, 22, 3061-3076.
24. Hemmer-Hansen J, Nielsen EE, Therkildsen NO et al. (2013) A genomic island linked to ecotype divergence in Atlantic cod. Molecular Ecology, 22, 2653-2667.
25. 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. Molecular Ecology, 23, 5224-5240.
26. Hertz-Fowler C, Figueiredo LM, Quail MA et al. (2008) Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS ONE, 3, e3527.
27. Hohenlohe PA, Bassham S, Etter PD, et al. (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD Tags. PLoS Genetics, 6, e1000862.
28. Huang X (1999) CAP3: a DNA sequence assembly program. Genome Research, 9, 868-877.
29. Jeukens J, Renaut S, St-Cyr J, Nolte AW, Bernatchez L (2010) The transcriptomics of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis spp., Salmonidae) divergence as revealed by next-generation sequencing. Molecular Ecology, 19, 5389-5403.
30. King Y-T, Lin C-S, Lin J-H, Lee W-C (2002) Whole-body hyperthermia-induced thermotolerance is associated with the induction of Heat Shock Protein 70 in mice. The Journal of Experimental Biology, 205, 273-278.
31. Kodama M, Brieuc MS, 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. Genes Genomes Genetics, 4, 1717-1730.
32. Krasileva KV, Buffalo V, Bailey P et al. (2013) Separating homeologs by phasing in the tetraploid wheat transcriptome. Genome Biology, 14, R66.
33. Kruglyak L (1999) Prospects for whole-genome linkage disequilibrium mapping of common disease genes. Nature Genetics, 22, 139-144.
34. Kurtz S, Phillippy A, Delcher AL et al. (2004) Versatile and open software for comparing large genomes. Genome Biology, 5, R12.
35. Larson WA, Seeb LW, Everett MV et al. (2014) Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evolutionary Applications, 7, 355-369.
36. Lien S, Gidskehaug L, Moen T 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.
37. 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. Journal of Heredity, 105, 741-751.
38. Limborg MT, McKinney GJ, Seeb L, Seeb JE (2015) Recombination patterns reveal information about centromere location on linkage maps. Molecular Ecology Resources, doi:10.1111/1755-0998.12484.
39. MacQueen DJ, Johnston IA (2014) A well-constrained estimate for the timing of the salmonid whole genome duplication reveals major decoupling from species diversification. Proceedings. Biological Sciences/The Royal Society, 281, 20132881.
40. McCormick SD (2012) Smolt physiology and endocrinology. In: Euryhaline Fishes (eds McCormick SD, Farrell AP & Brauner CJ), pp. 199-251. Elsevier, Amsterdam.
41. McKinney GJ, Hale MC, Goetz G et al. (2015) Ontogenetic changes in embryonic and brain gene expression in progeny produced from migratory and resident Oncorhynchus mykiss. Molecular Ecology, 24, 1792-1809.
42. Miller MR, Brunelli JP, Wheeler PA et al. (2012) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Molecular Ecology, 21, 237-249.
43. Moen T, Hayes B, Baranski M et al. (2008) A linkage map of the Atlantic salmon (Salmo salar) based on EST-derived SNP markers. BMC Genomics, 9, 223.
44. Munoz NJ, Farrell AP, Heath JW, Neff BD (2015) Adaptive potential of a Pacific salmon challenged by climate change. Nature Climate Change, 5, 163-166.
45. Naish KA, Phillips RB, Brieuc MS, et al. (2013) Comparative genome mapping between Chinook salmon (Oncorhynchustshawytscha) and rainbow trout (O. mykiss) based on homologous microsatellite loci. Genes Genomes Genetics, 3, 2281-2288.
46. Narum SR, Campbell NR (2015) Transcriptomic response to heat stress among ecologically divergent populations of redband trout. BMC Genomics, 16, 103.
47. Nichols KM, Young WP, Danzmann RG et al. (2003) A consolidated linkage map for rainbow trout (Oncorhynchus mykiss). Animal Genetics, 34, 102-115.
48. Nollen EA, Kabakov AE, Brunsting JF et al. (2001) Modulation of in vivo HSP70 chaperone activity by Hip and Bag-1. Journal of Biological Chemistry, 276, 4677-4682.
49. Ojima N, Yamashita M, Watabe S (2005) Quantitative mRNA expression profiling of heat-shock protein families in rainbow trout cells. Biochemical and Biophysical Research Communications, 329, 51-57.
50. O'Malley KG, Ford MJ, Hard JJ (2010) Clock polymorphism in Pacific salmon: evidence for variable selection along a latitudinal gradient. Proceedings. Biological Sciences/The Royal Society, 277, 3703-3714.
51. O'Quin CT, Drilea AC, Conte MA, Kocher TD (2013) Mapping of pigmentation QTL on an anchored genome assembly of the cichlid fish, Metriaclima zebra. BMC Genomics, 14, 287.
52. Parisod C, Alix K, Just J et al. (2010) Impact of transposable elements on the organization and function of allopolyploid genomes. New Phytologist, 186, 37-45.
53. Phillips RB, Park LK, Naish KA (2013) Assignment of Chinook salmon (Oncorhynchus tshawytscha) linkage groups to specific chromosomes reveals a karyotype with multiple rearrangements of the chromosome arms of rainbow trout (Oncorhynchus mykiss). Genes Genomes Genetics, 3, 2289-2295.
54. Rastas P, Paulin L, Hanski I, Lehtonen R, Auvinen P (2013) Lep-MAP: fast and accurate linkage map construction for large SNP datasets. Bioinformatics, 29, 3128-3134.
55. Rebl A, Verleih M, Kobis JM et al. (2013) Transcriptome profiling of gill tissue in regionally bred and globally farmed rainbow trout strains reveals different strategies for coping with thermal stress. Marine Biotechnology, 15, 445-460.
56. Rexroad CE III, Palti Y, Gahr SA, Vallejo RL (2008) A second generation genetic map for rainbow trout (Oncorhynchus mykiss). BMC Genetics, 9, 74.
57. Rondeau EB, Minkley DR, Leong JS 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.
58. Safran M, Dalah I, Alexander J et al. (2010) GeneCards version 3: the human gene integrator. Database (Oxford), 2010, baq020.
59. Sakamoto T, Danzmann RG, Gharbi K 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.
60. Schindler DE, Hilborn R, Chasco B et al. (2010) Population diversity and the portfolio effect in an exploited species. Nature, 465, 609-612.
61. Seeb LW, Waples RK, Limborg MT et al. (2014) Parallel signatures of selection in temporally isolated lineages of pink salmon. Molecular Ecology, 23, 2473-2485.
62. Stinchcombe JR, Hoekstra HE (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158-170.
63. Takayama S, Bimston DN, Matsuzawa S-I et al. (1997) BAG-1 modulates the chaperone activity of Hsp70/Hsc70. EMBO Journal, 16, 4887-4896.
64. Thorgaard GH, Allendorf FW, Knudsen KL (1983) Gene-centromere mapping in rainbow trout: high interference over long map distances. Genetics, 103, 771-783.
65. Tomalty KM, Meek MH, Stephens MR et al. (2015) Transcriptional response to acute thermal exposure in Juvenile Chinook Salmon determined by RNAseq. Genes Genomes Genetics, 5, 1335-1349.
66. Van Rossom S, Op de Beeck K, Hristovska V, Winderickx J, Van Camp G (2015) The deafness gene DFNA5 induces programmed cell death through mitochondria and MAPK-related pathways. Frontiers in Cellular Neuroscience, 9, 231.
67. Waples RK, Seeb LW, Seeb JE (2015) Linkage mapping with paralogs exposes regions of residual tetrasomic inheritance in chum salmon (Oncorhynchus keta). Molecular Ecology Resources, doi:10.1111/1755-0998.12394.
68. Wu Y, Bhat PR, Close TJ, Lonardi S (2008) Efficient and accurate construction of genetic linkage maps from the minimum spanning tree of a graph. PLoS Genetics, 4, e1000212.
69. Wu Y, Timothy JC, Stefano L (2011) Accurate construction of consensus genetic maps via integer linear programming. IEEE/ACM Transactions on Computational Biology and Bioinformatics, 8, 381-394.
70. Zhang Y, Huang L, Zhang J, Moskophidis D, Mivechi NF (2002) Targeted disruption of hsf1 leads to lack of thermotolerance and defines tissue-specific regulation for stress-inducible Hsp molecular chaperones. Journal of Cellular Biochemistry, 86, 376-393.