Fish Physiology and Biochemistry

, Volume 33, Issue 3, pp 259–268 | Cite as

Biochemical and molecular differences in diploid and triploid ocean-type chinook salmon (Oncorhynchus tshawytscha) smolts

  • J. Mark Shrimpton
  • Aurora M. C. Sentlinger
  • John W. Heath
  • Robert H. Devlin
  • Daniel D. Heath
Article

Abstract

There is increasing evidence for complex dosage effects on gene expression, enzyme activity and phenotype resulting from induced ploidy change. In this study, ocean-type chinook salmon were bred using a 2 × 2 factorial mating design to create four families and test whether triploidization resulted in changes in growth performance and smolting. Eggs were pressure shocked after fertilization to create triploid fish from a subset of each family. In June, fish were sampled for size, plasma insulin-like growth factor 1 (IGF-1), gill Na+–K+-ATPase activity, and expression of two Na+–K+-ATPase α subunits in the gill. Diploids were significantly heavier than triploids, and there were significant differences due to family. Despite a significant positive correlation between plasma IGF-1 and fish size, plasma IGF-1 did not differ between diploid and triploid smolts. Diploids also had significantly greater gill Na+–K+-ATPase enzyme activities than triploids and there was a strong family effect. Gill Na+–K+-ATPase α1b isoform expression differed significantly by family, but not ploidy, and generally families with lower Na+–K+-ATPase enzyme activity had higher α1b isoform gene expression. Na+–K+-ATPase α1a isoform expression did not differ among any of the groups. Although diploids were larger and had higher specific activities of Na+–K+-ATPase in the gills, there was no difference in gene expression or circulating hormone levels. The strong family effect, however, suggests that strain selection may be useful in improving performance of triploids for aquaculture.

Keywords

Ploidy Enzyme activity Gene expression Gill IGF-1 Na+–K+-ATPase Salmonid 

References

  1. Agustsson T, Sundell K, Sakamoto T, Johansson V, Ando M, Björnsson BTh (2001) Growth hormone endocrinology of Atlantic salmon (Salmo salar): pituitary gene expression, hormone storage, secretion and plasma levels during parr-smolt transformation. J Endocrinol 170:227–234PubMedCrossRefGoogle Scholar
  2. Beckman BR, Larsen DA, Moriyama S, Lee-Pawlak B, Dickoff WW (1998) Insulin-like growth factor and environmental modulation of growth during smoltification of spring Chinook salmon (Oncorhynchus tshawytscha). Gen Comp Endocrinol 109:325–335PubMedCrossRefGoogle Scholar
  3. Beckman BR, Shearer KD, Cooper KA, Dickhoff WW (2001) Relationship of insulin-like growth factor-I and insulin to size and adiposity of under-yearling Chinook salmon. Comp Bioc Phys A 129:585–593CrossRefGoogle Scholar
  4. Benfey TJ (1999) The physiology and behaviour of triploid fishes. Rev Fish. Sci. 7:39–67CrossRefGoogle Scholar
  5. Benfey TJ (2001) Use of sterile triploid Atlantic salmon (Salmo salar L.) for aquaculture in New Brunswick, Canada. ICES J Mar Sci 58:525–529CrossRefGoogle Scholar
  6. Birchler JA, Bhadra U, Bhadra MP, Auger DL (2001) Dosage-dependent gene regulation in multicellular eukaryotes: implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev Biol 234:275–288PubMedCrossRefGoogle Scholar
  7. Bonnet S, Hafray P, Blanc JM, Vallée F, Vauchez C, Fauré A, Fauconneau B (1999) Genetic variation in growth parameters until commercial size in diploid and triploid freshwater rainbow trout (Oncorhynchus mykiss) and seawater brown trout (Salmo trutta). Aquaculture 173:359–375CrossRefGoogle Scholar
  8. Carter CG, McCarthy ID, Houlihan DF, Johnstone R, Walsingham MV, Mithcell AI (1994) Food-consumption, feeding-behavior, and growth of triploid and diploid Atlantic salmon, Salmo salar L., parr. Can J Zool 72:609–617CrossRefGoogle Scholar
  9. Cogswell AT, Benfey TJ, Sutterlin AM (2002) The hematology of diploid and triploid transgenic Atlantic salmon (Salmo salar). Fish Phys Bioc 24:271–277CrossRefGoogle Scholar
  10. Cotter D, O’Donnovan V, Drumm A, Roche N, Ling EN, Wilkins NP (2002) Comparison of freshwater and marine performance of all-female diploid and triploid Atlantic salmon (Salmo salar L.). Aquac Res 33:43–53CrossRefGoogle Scholar
  11. Davis KB, Peterson BC (2006) The effect of temperature, stress, and cortisol on plasma IGF-I and IGFBPs in sunshine bass. Gen Comp Endocrinol 149:219–225PubMedCrossRefGoogle Scholar
  12. D’Cotta H, Valotaire C, Le Gac F, Prunet P (2000) Synthesis of gill Na+-K+-ATPase in Atlantic salmon smolts: differences in α-protein levels. Am J Physiol – Reg Integ Comp Physiol 278:R101–R110Google Scholar
  13. Devlin RH, Biagi CA, Yesaki TY (2004) Growth, viability and genetic characteristics of GH transgenic coho salmon strains. Aquaculture 236:607–632CrossRefGoogle Scholar
  14. Devlin RH, Holm DG, Grigliatti TA (1988) The influence of whole-arm trisomy on gene expression in Drosophila. Genetics 138:87–101Google Scholar
  15. Duan CM (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128:306S–314SPubMedGoogle Scholar
  16. Friars GW, McMillan I, Quinton VM, O’Flynn FM, McGeachy SA, Benfey TJ (2001) Family differences in relative growth of diploid and triploid Atlantic salmon (Salmo salar). Aquaculture 192:23–29CrossRefGoogle Scholar
  17. Garnier-Gere PH, Naciri-Graven Y, Bougrier S, Magoulas A, Heral M, Kotoulas G, Hawkins A, Gerard A (2002) Influences of triploidy, parentage and genetic diversity on growth of the Pacific oyster Crassostrea gigas reared in contrasting natural environments. Mol Ecol 111:1499–1514CrossRefGoogle Scholar
  18. Gilmour KM, DiBattista JD, Thomas JB (2005) Physiological causes and consequences of social status in salmonid fish. Int Comp Biol 45:263–273CrossRefGoogle Scholar
  19. Guo M, Davis D, Birchler JA (1996) Dosage effects on gene expression in a maize ploidy series. Genetics 142:1349–1355PubMedGoogle Scholar
  20. Heath DD, Fox CW, Heath JW (1999) Maternal effects on offspring size: variation through early development in chinook salmon. Evolution 53:1605–1611CrossRefGoogle Scholar
  21. Johnson RM, Shrimpton JM, Heath JW, Heath DD (2004) Family, induction methodology and interaction effects on the performance of diploid and triploid Chinook salmon (Oncorhynchus tswawytscha). Aquaculture 234:123–142CrossRefGoogle Scholar
  22. Johnson RM, Shrimpton JM, Cho GK, Heath DD (2007) Dosage effects on heritability and maternal effects in diploid and triploid Chinook salmon (Oncorhynchus tshawytscha) early life traits. Heredity 98:303–310PubMedCrossRefGoogle Scholar
  23. Leary RF, Allendorf FW, Knudsen KL, Thorgaard GH (1985) Heterozygosity and developmental stability in gynogenetic diploid and triploid rainbow trout. Heredity 54:219–225PubMedGoogle Scholar
  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using Real-Time quantitative PCR and the 2-ΔΔC T method. Methods 25:402–408PubMedCrossRefGoogle Scholar
  25. Marie V, Gonzalez P, Baudrimont M, Boutet I, Moraga D, Bourdineaud JP, Boudou A (2006) Metallothionein gene expression and protein levels in triploid and diploid oysters Crassostrea gigas after exposure to cadmium and zinc. Environ Toxicol Chem 25:412–418PubMedCrossRefGoogle Scholar
  26. McCormick SD (1993) Methods for nonlethal gill biopsy and measurements of Na+–K+-ATPase activity. Can J Fish Aquat Sci 50:656–658Google Scholar
  27. McCormick SD, Kelley KM, Young G, Nishioka RS, Bern HA (1992) Stimulation of coho salmon growth by insulin-like growth factor I. Gen Comp Endocrinol 86:398–406PubMedCrossRefGoogle Scholar
  28. McCormick S D, Moriyama S, Björnsson BTh (2000) Low temperature limits photoperiod control of smolting in Atlantic salmon through endocrine mechanisms. Am J Physiol – Reg Integr Comp Physiol 278:R1352–R1361Google Scholar
  29. McCormick SD, Sakamoto T, Hasegawa S, Hirano T (1991) Osmoregulatory actions of insulin-like growth factor-I in rainbow trout (Oncorhynchus mykiss). J Endocrinol 130:87–92PubMedCrossRefGoogle Scholar
  30. McCormick SD, Shrimpton JM, Carey JB, O’Dea MF, Sloan KE, Moriyama S, Björnsson BTh (1998) Repeated acute stress reduces growth rate of Atlantic salmon parr and alters plasma levels of growth hormone, insulin-like growth factor I and cortisol. Aquaculture 168:221–235CrossRefGoogle Scholar
  31. McCormick SD, Shrimpton JM, Moriyama S, Björnsson BTh (2002) Effects of an advanced temperature cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for smolting in Atlantic salmon. J Exp Biol 205:3553–3560PubMedGoogle Scholar
  32. O’Keefe RA, Benfey TJ (1997) The feeding response of diploid and triploid Atlantic salmon and brook trout. J Fish Biol 51:989–997CrossRefGoogle Scholar
  33. O’Keefe RA, Benfey TJ (1999) Comparative growth and food consumption of diploid and triploid brook trout (Salvelinus fontinalis) monitored by radiography. Aquaculture 175:111–120CrossRefGoogle Scholar
  34. Pierce AL, Dickey JT, Larson DA, Fukuda H, Swanson P, Dickhoff WW (2004) A quantitative real-time RT-PCR assay for salmon IGF-I mRNA, and its application in the study of GH regulation of IGF-I gene expression in primary culture of salmon hepatocytes. Gen Comp Endocrinol 135:401–411PubMedCrossRefGoogle Scholar
  35. Richards JG, Semple JW, Bystriansky JS, Schulte PM (2003) Na+/K+-ATPase α-isoform switching in gills of rainbow trout (Oncorhynchus mykiss) during salinity transfer. J Exp Biol 206:4475–4486PubMedCrossRefGoogle Scholar
  36. Sapolsky RM, Spencer EM (1997) Insulin-like growth factor I is suppressed in socially subordinate male baboons. Am J Physiol 273:R1346–R1351PubMedGoogle Scholar
  37. Shimizu M, Swanson P, Fukada H, Hara A, Dickhoff WW (2000) Comparison of extraction methods and assay validation for salmon insulin-like factor I using commercially available components. Gen Comp Endocrinol 119:26–36PubMedCrossRefGoogle Scholar
  38. Shrimpton JM, Patterson DA, Richards JG, Cooke SJ, Schulte PM, Hinch SG, Farrell AP (2005) Ionoregulatory changes in different populations of maturing sockeye salmon (Oncorhynchus nerka) during ocean and river migration. J Exp Biol 208:4069–4078PubMedCrossRefGoogle Scholar
  39. Sloman KA, Metcalfe NB, Taylor AC, Gilmour KM (2001) Plasma cortisol concentrations before and after social stress in rainbow trout and brown trout. Phys Bioc Zool 74:383–389CrossRefGoogle Scholar
  40. Suzuki MG, Shimada T, Yokoyama T, Kobayashi M (1999) The influence of triploidy on gene expression in the silkworm, Bombyx mori. Heredity 82:661–667PubMedCrossRefGoogle Scholar
  41. Wagner EJ, Arndt RE, Routledge MD, Latremouille D, Mellenthin RF (2006) Comparison of hatchery performance, agonistic behavior, and poststocking survival between diploid and triploid trout of three different Utah strains. NA J Aquaculture 68:63–73CrossRefGoogle Scholar
  42. Wang S, Hard JJ, Utter F (2002) Genetic variation and fitness in salmonids. Conserv Genet 3:321–333CrossRefGoogle Scholar
  43. Withler RE, Beachem TD, Solar II, Donaldson EM (1995) Freshwater growth, smolting and marine survival and growth of diploid and triploid coho salmon (Oncorhynchus kisutch). Aquaculture 136:91–107CrossRefGoogle Scholar
  44. Withler RE, Clarke WC, Blackburn J, Baker I (1998) Effect of triploidy on growth and survival of pre-smolt and post-smolt coho salmon (Oncorrhynchus kisutch). Aquaculture 175:111–120Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • J. Mark Shrimpton
    • 1
  • Aurora M. C. Sentlinger
    • 1
  • John W. Heath
    • 2
  • Robert H. Devlin
    • 3
  • Daniel D. Heath
    • 4
  1. 1.Ecosystem Science & Management Program (Biology)University of Northern British ColumbiaPrince GeorgeCanada
  2. 2.Yellow Island Aquaculture LtdCampbell RiverCanada
  3. 3.Fisheries and Oceans CanadaWest VancouverCanada
  4. 4.Great Lakes Institute for Environmental Research and Department of Biological SciencesUniversity of WindsorWindsorCanada

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