BMC Genomics | |
A comparison of gene transcription profiles of domesticated and wild Atlantic salmon (Salmo salar L.) at early life stages, reared under controlled conditions | |
John B Taggart1  Kevin A Glover2  James E Bron1  Beatrix Bicskei1  | |
[1] Institute of Aquaculture, School of Natural Sciences, University of Stirling, Stirling FK9 4LA, UK;Institute of Marine Research, Population genetics, PO Box 1870, N-5817 Bergen, Norway | |
关键词: Maternal effects; Farm escapees; Gene expression; Atlantic salmon; Microarray; Domestication selection; | |
Others : 1128472 DOI : 10.1186/1471-2164-15-884 |
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received in 2014-05-17, accepted in 2014-09-29, 发布年份 2014 | |
【 摘 要 】
Background
Atlantic salmon have been subject to domestication for approximately ten generations, beginning in the early 1970s. This process of artificial selection will have created various genetic differences between wild and farmed stocks. Each year, hundreds of thousands of farmed fish escape into the wild. These escapees may interbreed with wild conspecifics raising concerns for both the fish-farming industry and fisheries managers. Thus, a better understanding of the interactions between domesticated and wild salmon is essential to the continued sustainability of the aquaculture industry and to the maintenance of healthy wild stocks.
Results
We compared the transcriptomes of a wild Norwegian Atlantic salmon population (Figgjo) and a Norwegian farmed strain (Mowi) at two life stages: yolk sac fry and post first-feeding fry. The analysis employed 44 k oligo-microarrays to analyse gene expression of 36 farmed, wild and hybrid (farmed dam x wild sire) individuals reared under identical hatchery conditions. Although some of the transcriptional differences detected overlapped between sampling points, our results highlighted the importance of studying various life stages. Compared to the wild population, the Mowi strain displayed up-regulation in mRNA translation-related and down regulation in nervous and immune system -related pathways in the sac fry, whereas up-regulation of digestive and endocrine activities, carbohydrate, energy, amino acid and lipid metabolism and down-regulation of environmental information processing and immune system pathways were evident in the feeding fry. Differentially regulated pathways that were common among life stages generally belonged to environmental information processing and immune system functional groups. In addition, we found indications of strong maternal effects, reinforcing the importance of including reciprocal hybrids in the analysis.
Conclusions
In agreement with previous studies we showed that domestication has caused changes in the transcriptome of wild Atlantic salmon and that many of the affected pathways are life-stage specific We highlighted the importance of reciprocal hybrids to the deconvolution of maternal/paternal effects and our data support the view that the genetic architecture of the strains studied highly influences the genes differentially expressed between wild and domesticated fish.
【 授权许可】
2014 Bicskei et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150223212001581.pdf | 1780KB | download | |
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Figure 1. | 58KB | Image | download |
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【 参考文献 】
- [1]Hindar K, Ryman N, Utter F: Genetic Effects of Cultured Fish on Natural Fish Populations. Can J Fish Aquat Sci 1991, 48:945-957.
- [2]Naylor R, Hindar K, Fleming I, Goldburg R, Williams S, Volpe J, Whoriskey F, Eagle J, Kelso D, Mangel M: Fugitive Salmon: Assessing the Risks of Escaped Fish from Net-Pen Aquaculture. Bioscience 2005, 55:427.
- [3]Ferguson A, Fleming IA, Hindar K, Skaala O, McGinnity P, Cross T, Prodohl P: Farm escapees. In Atl Salmon Genet Conserv Manag. Edited by Verspoor E, Stradmeyer L, Nielsen J. Oxford: Blackwell Publishing Ltd; 2007:357-398.
- [4]Glover KA, Skilbrei OT, Skaala Ø: Genetic assignment identifies farm of origin for Atlantic salmon Salmo salar escapees in a Norwegian fjord. ICES J Mar Sci 2008, 65(6):912-920.
- [5]Glover K: Forensic identification of fish farm escapees: the Norwegian experience. Aquac Environ Interact 2010, 1:1-10.
- [6]Zhang Z, Glover K, Wennevik V, Svåsand T, Sørvik GE, Fiske P, Karlsson S, Skaala Ø: Genetic analysis of Atlantic salmon captured in a netting station reveals multiple escapement events from commercial fish farms. Fish Manag Ecol 2013, 20:42-51.
- [7]Seagrov H, Urdal K: Escaped Farmed Salmon in the Sea and Rivers; Numbers and Origin. Bergen, Norway: Rådgivende Biologer AS; 2006. Report 947/06, 21
- [8]Skilbrei O: Reduced migratory performance of farmed Atlantic salmon post-smolts from a simulated escape during autumn. Aquac Environ Interact 2010, 1:117-125.
- [9]Skilbrei O: Adult recaptures of farmed Atlantic salmon post-smolts allowed to escape during summer. Aquac Environ Interact 2010, 1:147-153.
- [10]Gausen D, Moen V: Large-Scale Escapes of Farmed Atlantic Salmon (Salmo salar) into Norwegian Rivers Threaten Natural Populations. Can J Fish Aquat Sci 1991, 48:426-428.
- [11]Fiske P, Lund R, Hansen L: Relationships between the frequency of farmed Atlantic salmon, Salmo salar L., in wild salmon populations and fish farming activity in Norway, 1989–2004. ICES J Mar Sci 2006, 63:1182-1189.
- [12]Webb JH, Youngson AF, Thomson CE, Hay DW, Donaghy MJ, McLaren IS: Spawning of escaped farmed Atlantic salmon, Salmo salar L., in western and northern Scottish rivers: egg deposition by females. Aquac Res 1993, 24:663-670.
- [13]Youngson AF, Webb JH, Maclean JC, Whyte BM: Short communication Frequency of occurrence of reared Atlantic salmon in Scottish salmon fisheries. ICES J Mar Sci 1997, 54:1216-1220.
- [14]Walker A, Beveridge M, Crozier W, Omaoileidigh N, Milner N: Monitoring the incidence of escaped farmed Atlantic salmon, Salmo salar L., in rivers and fisheries of the United Kingdom and Ireland: current progress and recommendations for future programmes. ICES J Mar Sci 2006, 63:1201-1210.
- [15]Gudjonsson S: Occurrence of reared salmon in natural salmon rivers in Iceland. Aquaculture 1991, 98:133-142.
- [16]Volpe JP, Taylor EB, Rimmer DW, Glickman BW: Evidence of Natural Reproduction of in a Salmon Atlantic Aquaculture-Escaped British Columbia River Coastal. Conserv Biol 2014, 14:899-903.
- [17]Morris MRJ, Fraser DJ, Heggelin AJ, Whoriskey FG, Carr JW, O’Neil SF, Hutchings J: Prevalence and recurrence of escaped farmed Atlantic salmon (Salmo salar) in eastern North American rivers. Can J Fish Aquat Sci 2008, 65:2807-2826.
- [18]Fleming AIA, Jonsson B, Gross MR, Lamberg A, Fleming IA: An experimental study of the reproductive behaviour and success of farmed and wild Atlantic salmon (Salmo salar). J Appl Ecol 1996, 33:893-905.
- [19]Fleming I, Hindar K, Mjølnerød IB, Jonsson B, Balstad T, Lamberg A: Lifetime success and interactions of farm salmon invading a native population. Proc Biol Sci 2000, 267:1517-1523.
- [20]Webb JH, Hay DW, Cunningham PD, YAF: The spawning behaviour of escaped farmed and wild adult Atlantic salmon (& imo sakzr L .) in a northern Scottish river. Aquaculture 1991, 97-110.
- [21]Crozier WW: Evidence of genetic interaction between escaped farmed salmon and wild Atlantic salmon (Salmo salar L.) in a Northern Irish river. Aquaculture 1993, 113:19-29.
- [22]Clifford SL, McGinnity P, Ferguson A: Genetic changes in Atlantic salmon (Salmo salar) populations of Northwest Irish rivers resulting from escapes of adult farm salmon. Can J Fish Aquat Sci 1998, 55:358-363.
- [23]Skaala O, Wennevik V, Glover K: Evidence of temporal genetic change in wild Atlantic salmon, Salmo salar L., populations affected by farm escapees. ICES J Mar Sci 2006, 63:1224-1233.
- [24]Glover K, Quintela M, Wennevik V, Besnier F, Sørvik AGE, Skaala Ø: Three decades of farmed escapees in the wild: a spatio-temporal analysis of Atlantic salmon population genetic structure throughout Norway. PLoS One 2012, 7:e43129.
- [25]Glover KA, Pertoldi C, Besnier F, Wennevik V, Kent M, Skaala Ø: Atlantic salmon populations invaded by farmed escapees: quantifying genetic introgression with a Bayesian approach and SNPs. BMC Genet 2013, 14:74.
- [26]Taylor EB: A review of local adaptation in Salmonidae, with particular reference to Pacific and Atlantic salmon. Aquaculture 1991, 185-207.
- [27]McGinnity P, Prodohl P, Maoileidigh NO, Hynes R, Cotter D, Baker N, O’Hea B, Ferguson A: Differential lifetime success and performance of native and non-native Atlantic salmon examined under communal natural conditions. J Fish Biol 2004, 65(SUPPL. A):173-187.
- [28]Garcia de Leaniz C, Fleming I, Einum S, Verspoor E, Jordan WC, Consuegra S, Aubin-Horth N, Lajus D, Letcher BH, Youngson F, Webb JH, Vøllestad L, Villanueva B, Ferguson A, Quinn TP: A critical review of adaptive genetic variation in Atlantic salmon: implications for conservation. Biol Rev Camb Philos Soc 2007, 82:173-211.
- [29]Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB: Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity (Edinb) 2011, 106:404-420.
- [30]Gjedrem T, Gjoen HN, Gjerde B: Genetic origin of Norwegian farmed Atlantic salmon. Aquaculture 1991, 41-50.
- [31]Gjedrem T: Genetic improvement of cold-water fish species. Aquac Res 2000, 31(1):25-33.
- [32]Gjedrem T: The first family-based breeding program in aquaculture. Rev Aquac 2010, 2:2-15.
- [33]Thodesen J, Grisdale-Helland B, Helland SJ, Gjerde B: Feed intake, growth and feed utilization of offspring from wild and selected Atlantic salmon (Salmo salar). Aquaculture 1999, 180:237-246.
- [34]Glover K, Ottera H, Olsen R, Slinde E, Taranger G, Skaala O: A comparison of farmed, wild and hybrid Atlantic salmon (Salmo salar L.) reared under farming conditions. Aquaculture 2009, 286:203-210.
- [35]Solberg MF, Kvamme BO, Nilsen F, Glover K: Effects of environmental stress on mRNA expression levels of seven genes related to oxidative stress and growth in Atlantic salmon Salmo salar L. of farmed, hybrid and wild origin. BMC Res Notes 2012, 5:672. BioMed Central Full Text
- [36]Solberg MF, Skaala Ø, Nilsen F, Glover KA: Does domestication cause changes in growth reaction norms? A study of farmed, wild and hybrid Atlantic salmon families exposed to environmental stress. PLoS One 2013, 8:e54469.
- [37]Einum S, Fleming I: Genetic divergence and interactions in the wild among native, farmed and hybrid Atlantic salmon. J Fish Biol 1997, 50:634-651.
- [38]Norris AT, Bradley DG, Cunningham EP: Microsatellite genetic variation between and within farmed and wild Atlantic salmon (Salmo salar) populations. Aquaculture 1999, 180(3-4):247-264.
- [39]Skaala Ø, Høyheim B, Glover K, Dahle G: Microsatellite analysis in domesticated and wild Atlantic salmon (Salmo salar L.): allelic diversity and identification of individuals. Aquaculture 2004, 240:131-143.
- [40]Roberge C, Einum S, Guderley H, Bernatchez L: Rapid parallel evolutionary changes of gene transcription profiles in farmed Atlantic salmon. Mol Ecol 2006, 15:9-20.
- [41]Roberge C, Normandeau E, Einum S, Guderley H, Bernatchez L: Genetic consequences of interbreeding between farmed and wild Atlantic salmon: insights from the transcriptome. Mol Ecol 2008, 17:314-324.
- [42]Mcginnity P, Stone C, Taggart JB, Cooke D, Cotter D, Hynes R, Mccamley C, Cross T, Ferguson A: Genetic impact of escaped farmed Atlantic salmon (Salmo salar L .) on native populations: use of DNA profiling to assess freshwater performance of wild, farmed, and hybrid progeny in a natural river environment. ICES J Mar Sci 1997, 54(6):998-1008.
- [43]McGinnity P, Prodöhl P, Ferguson A, Hynes R, Maoiléidigh NO, Baker N, Cotter D, O’Hea B, Cooke D, Rogan G, Taggart J, Cross T: Fitness reduction and potential extinction of wild populations of Atlantic salmon, Salmo salar, as a result of interactions with escaped farm salmon. Proc Biol Sci 2003, 270:2443-2450.
- [44]Skaala Ø, Glover KA, Barlaup BT, Svåsand T, Besnier F, Hansen MM, Borgstrøm R, Fleming I: Performance of farmed, hybrid, and wild Atlantic salmon (Salmo salar) families in a natural river environment. Can J Fish Aquat Sci 2012, 69:1994-2006.
- [45]Araki H, Berejikian B, Ford MJ, Blouin MS: Fitness of hatchery-reared salmonids in the wild. Evol Appl 2008, 1:342-355.
- [46]Araki H, Schmid C: Is hatchery stocking a help or harm? Aquaculture 2010, 308:S2-S11.
- [47]King M, Wilson AC: Evolution at Two Levels in Humans and Chimpanzees. Science 1975, 188(4184):107-116.
- [48]Carroll SB: Evolution at two levels: on genes and form. PLoS Biol 2005, 3:e245.
- [49]Schalburg Von KR, Rise ML, Cooper G, Brown GD, Gibbs R, Nelson CC, Davidson WS, Koop BF: Fish and chips: various methodologies demonstrate utility of a 16,006-gene salmonid microarray. BMC Genomics 2005, 6:126. BioMed Central Full Text
- [50]Taggart JB, Bron JE, Martin S a M, Seear PJ, Høyheim B, Talbot R, Carmichael SN, Villeneuve LN, Sweeney GE, Houlihan DF, Secombes CJ, Tocher DR, Teale J: A description of the origins, design and performance of the TRAITS-SGP Atlantic salmon Salmo salar L. cDNA microarray. J Fish Biol 2008, 72:2071-2094.
- [51]White SL, Sakhrani D, Danzmann RG, Devlin RH: Influence of developmental stage and genotype on liver mRNA levels among wild, domesticated, and hybrid rainbow trout (Oncorhynchus mykiss). BMC Genomics 2013, 14:673. BioMed Central Full Text
- [52]Glover K, Skår C, Christie KE, Glette J, Rudra H, Skaala Ø: Size-dependent susceptibility to infectious salmon anemia virus (ISAV) in Atlantic salmon (Salmo salar L.) of farm, hybrid and wild parentage. Aquaculture 2006, 254:82-91.
- [53]LUND RA, HANSEL LP: Identification of wild and reared Atlantic salmon, Salmo salar L., using scale characters. Aquac Res 1991, 22:499-508.
- [54]Tacchi L, Bickerdike R, Douglas A, Secombes CJ, Martin S a M: Transcriptomic responses to functional feeds in Atlantic salmon (Salmo salar). Fish Shellfish Immunol 2011, 31:704-715.
- [55]Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ: GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics 2009, 10:161. BioMed Central Full Text
- [56]Warnes AGR, Bolker B, Bonebakker L, Huber W, Liaw A, Lumley T, Magnusson A, Moeller S, Schwartz M, Venables B, Warnes MGR: gplots: Various R programming tools for plotting data. 2014. http://cran.r-project.org/web/packages/gplots/index.html webcite
- [57]Wickham H: ggplot2: Elegant graphics for data analysis. New York: Springer; 2009.
- [58]Pfaffl MW, Horgan GW, Dempfle L: Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 2002, 30:e36.
- [59]Bougas B, Audet C, Bernatchez L: The influence of parental effects on transcriptomic landscape during early development in brook charr (Salvelinus fontinalis, Mitchill). Heredity (Edinb) 2013, 110:484-491.
- [60]Mennigen J, Skiba-Cassy S, Panserat S: Ontogenetic expression of metabolic genes and microRNAs in rainbow trout alevins during the transition from the endogenous to the exogenous feeding period. J Exp Biol 2013, 216(Pt 9):1597-1608.
- [61]Bernatchez L, Renaut S, Whiteley AR, Derome N, Jeukens J, Landry L, Lu G, Nolte AW, Ostbye K, Rogers SM, St-Cyr J: On the origin of species: insights from the ecological genomics of lake whitefish. Philos Trans R Soc Lond B Biol Sci 2010, 365:1783-1800.
- [62]Glover K a, Bergh Ø, Rudra H, Skaala Ø: Juvenile growth and susceptibility to Aeromonas salmonicida subsp. salmonicida in Atlantic salmon (Salmo salar L.) of farmed, hybrid and wild parentage. Aquaculture 2006, 254:72-81.
- [63]Fleming I, Agustsson T: Effects of domestication on growth physiology and endocrinology of Atlantic salmon (Salmo salar). J Fish 2002, 1330:1323-1330.
- [64]Tymchuk W, Sakhrani D, Devlin R: Domestication causes large-scale effects on gene expression in rainbow trout: analysis of muscle, liver and brain transcriptomes. Gen Comp Endocrinol 2009, 164:175-183.
- [65]Debes PV, Normandeau E, Fraser DJ, Bernatchez L, Hutchings JA: Differences in transcription levels among wild, domesticated, and hybrid Atlantic salmon (Salmo salar) from two environments. Mol Ecol 2012, 21:2574-2587.
- [66]Martinez V, Dettleff P, Lopez P, Fernandez G, Jedlicki A, Yañez JM, Davidson WS: Assessing footprints of selection in commercial Atlantic salmon populations using microsatellite data. Anim Genet 2013, 44:223-226.
- [67]Kawai T, Akira S: Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med 2007, 13:460-469.
- [68]Tort L: Stress and immune modulation in fish. Dev Comp Immunol 2011, 35:1366-1375.
- [69]Alejo A, Tafalla C: Chemokines in teleost fish species. Dev Comp Immunol 2011, 35:1215-1222.
- [70]Bougas B, Granier S, Audet C, Bernatchez L: The transcriptional landscape of cross-specific hybrids and its possible link with growth in brook charr (Salvelinus fontinalis Mitchill). Genetics 2010, 186:97-107.
- [71]Renaut S, Nolte W, Bernatchez L: Gene expression divergence and hybrid misexpression between lake whitefish species pairs (Coregonus spp. Salmonidae). Mol Biol Evol 2009, 26:925-936.
- [72]Fraser DJ, Houde ALS, Debes PV, O’Reilly P, Eddington JD, Hutchings J: Consequences of farmed-wild hybridization across divergent wild populations and multiple traits in salmon. Ecol Appl 2010, 20:935-953.
- [73]Bougas B, Normandeau E, Audet C, Bernatchez L: Linking transcriptomic and genomic variation to growth in brook charr hybrids (Salvelinus fontinalis, Mitchill). Heredity (Edinb) 2013, 110:492-500.
- [74]Normandeau E, Hutchings J, Fraser DJ, Bernatchez L: Population-specific gene expression responses to hybridization between farm and wild Atlantic salmon. Evol Appl 2009, 2:489-503.