Physiological differences between lean and siscowet lake trout morphotypes: Are these metabolotypes?

Canadian Journal of Fisheries and Aquatic Sciences

Volumn 71, Issue 3, 2014, Pages 427-435

  Goetz, Frederick ^a,b   Jasonowicz, Andrew ^a,f   Johnson, Ronald ^b   Biga, Peggy ^c   Fischer, Greg ^d   Sitar, Shawn ^e  

^a UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

^b NORTHWEST FISHERIES SCIENCE CENTER   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^d UNIVERSITY OF WISCONSIN STEVENS POINT   (United States)

^e MICHIGAN DEPARTMENT OF NATURAL RESOURCES   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENETIC ANALYSIS; LIFE HISTORY; LIPID; MORPHOMETRY; MORPHOTYPE; PHYSIOLOGY; REPRODUCTION; SALMONID;

EID: 84896877611     PISSN: 0706652X     EISSN: 12057533     Source Type: Journal    
DOI: 10.1139/cjfas-2013-0463     Document Type: Article

References (67)

1. Adams, C.E., and Huntingford, F.A. 2004. Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of arctic charr. Biol. J. Linn. Soc. 81(4): 611-618. doi:10.1111/j.1095-8312.2004.00314.x.
2. AOAC International 2000. Official method 920.39. Official methods of analysis of AOAC International. W. Horwitz, Arlington, Va., USA. AOAC.
3. Babin, P.J., and Vernier, J.-M. 1989. Plasma lipoproteins in fish. J. Lipid Res. 30: 467-489. PMID:2666541.
4. Biga, P.R., Cain, K.D., Hardy, R.W., Schelling, G.T., Overturf, K., Roberts, S.B., Goetz, F.W., and Ott, T.L. 2004. Growth hormone differentially regulates muscle myostatin1 and-2 and increases circulating cortisol in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocr. 138(1): 32-41. doi:10.1016/j.ygcen. 2004.05.001. PMID:15242749.
5. Blackie, C.T., Weese, D.J., and Noakes, D.L.G. 2003. Evidence for resource polymorphism in the lake charr (Salvelinus namaycush) population of Great Bear Lake, Northwest Territories, Canada. Ecoscience, 10(4): 509-514.
6. Bligh, E.G., and Dyer, W.J. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37(8): 911-917. doi:10.1139/o59-099.
7. Bronte, C.R., Ebener, M.P., Schreiner, D.R., DeVault, D.S., Petzold, M.M., Jensen, D.A., Richards, C., and Lozano, S.J. 2003. Fish community change in Lake Superior, 1970-2000. Can. J. Fish. Aquat. Sci. 60(12): 1552-1574. doi:10. 1139/f03-136.
8. Childress, J.J., Cowles, D.L., Favuzzi, J.A., and Mickel, T.J. 1990a. Metabolic rates of benthic deep-sea decapod crustaceans decline with increasing depth primarily due to the decline in temperature. Deep-Sea Res. 37(6): 929-949. doi: 10.1016/0198-0149(90)90104-4.
9. Childress, J.J., Price, M.H., Favuzzi, J., and Cowles, D. 1990b. Chemical composition of midwater fishes as a function of depth of occurrence off the Hawaiian Islands: food availability as a selective factor? Mar. Biol. 105(2): 235-246. doi:10.1007/BF01344292.
10. Clarke, A., Doherty, N., DeVries, A.L., and Eastman, J.T. 1984. Lipid content and composition of 3 species of antarctic fish in relation to buoyancy. Polar Biol. 3(2): 77-83. doi:10.1007/BF00258151.
11. Derome, N., and Bernatchez, L. 2006. The transcriptomics of ecological convergence between 2 limnetic coregonine fishes (Salmonidae). Mol. Biol. Evol. 23(12): 2370-2378. doi:10.1093/molbev/msl110. PMID:16963516.
12. Derome, N., Duchesne, P., and Bernatchez, L. 2006. Parallelism in gene transcription among sympatric lake whitefish (Coregonus clupeaformis Mitchill) ecotypes. Mol. Ecol. 15(5): 1239-1249. doi:10.1111/j.1365-294X.2005.02968.x. PMID:16626451.
13. de Souza, N.E., Matsushita, M., de Oliveira, C.C., Franco, M.R.B., and Visentainer, J.V. 2007. Manipulation of fatty acid composition of Nile tilapia (Oreochromis niloticus) fillets with flaxseed oil. J. Sci. Food Agric. 87(9): 1677-1681. doi:10.1002/jsfa.2877.
14. Drazen, J.C., and Seibel, B.A. 2007. Depth-related trends in metabolism of benthic and benthopelagic deep-sea fishes. Limnol. Oceanogr. 52(5): 2306-2316. doi:10.4319/lo.2007.52.5.2306.
15. Eames, S.C., Philipson, L.H., Prince, V.E., and Kinkel, M.D. 2010. Blood sugar measurement in zebrafish reveals dynamics of glucose homeostasis. Zebrafish, 7(2): 205-213. doi:10.1089/zeb.2009.0640. PMID:20515318.
16. Eschmeyer, P.H., and Phillips, A.M. 1965. Fat content of the flesh of siscowets and lake trout from Lake Superior. Trans. Am. Fish. Soc. 94: 62-74. doi:10.1577/ 1548-8659(1965)94[62:FCOTFO]2.0.CO;2.
17. Eshenroder, R.L., and Burnham-Curtis, M.K. 1999. Species succession and sustainability of the great lakes fish community. In Great Lakes fisheries policy and management. Edited by W.W. Taylor and C.P. Ferreri. Michigan State University Press, East Lansing, Mich.
18. Evans, M.L., and Bernatchez, L. 2012. Oxidative phosphorylation gene transcription in whitefish species pairs reveals patterns of parallel and nonparallel physiological divergence. J. Evol. Biol. 25(9): 1823-1834. doi:10.1111/j.1420-9101. 2012.02570.x.
19. Evans, M.L., Chapman, L.J., Mitrofanov, I., and Bernatchez, L. 2013. Variable extent of parallelism in respiratory, circulatory, and neurological traits across lake whitefish species pairs. Ecol. Evol. 3(3): 546-557. doi:10.1002/ece3. 469. PMID:23532362.
20. Folch, J., Lees, M., and Sloane Stanley, G.H. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226(1): 497-509. PMID:13428781.
21. Freeman, N.K., Lindgren, F.T., and Nichols, A.V. 1963. The chemistry of serum lipoproteins. In Progress in the chemistry of fats and other lipids. Edited by R.T. Holman, W.O. Lundberg, and T. Malkin. The MacMillan Company, New York. pp. 215-250.
22. Garikipati, D.K., Gahr, S.A., and Rodgers, B.D. 2006. Identification, characterization, and quantitative expression analysis of rainbow trout myostatin-1a and myostatin-1b genes. J. Endocrinol. 190(3): 879-888. doi:10.1677/joe.1.06866.
23. Garikipati, D.K., Gahr, S.A., Roalson, E.H., and Rodgers, B.D. 2007. Characterization of rainbow trout myostatin-2 genes (rtmstn-2a and-2b): genomic organization, differential expression, and pseudogenization. Endocrinology, 148(5): 2106-2115. doi:10.1210/en.2006-1299. PMID:17289851.
24. Goetz, F., and MacKenzie, S. 2008. Functional genomics with microarrays in fish biology and fisheries. Fish Fish. 9: 378-395. doi:10.1111/j.1467-2979.2008. 00301.x.
25. Goetz, F., Rosauer, D., Sitar, S., Goetz, G., Simchick, C., Roberts, S., Johnson, R., Murphy, C., Bronte, C.R., and MacKenzie, S. 2010. A genetic basis for the phenotypic differentiation between siscowet and lean lake trout (Salvelinus namaycush). Mol. Ecol. 19(Suppl. 1): 176-196. doi:10.1111/j.1365-294X.2009. 04481.x.
26. Goetz, F.W., Sitar, S., Rosauer, D., Swanson, P., Bronte, C.R., Dickey, J., and Simchick, P. 2011. The reproductive biology of siscowet and lean lake trout (Salvelinus namaycush) in southern Lake Superior. Trans. Am. Fish. Soc. 140: 1472-1491. doi:10.1080/00028487.2011.630276.
27. Helterline, D.L., Garikipati, D., Stenkamp, D.L., and Rodgers, B.D. 2007. Embryonic and tissue-specific regulation of myostatin-1 and-2 gene expression in zebrafish. Gen. Comp. Endocr. 151(1): 90-97. doi:10.1016/j.ygcen.2006.12.023. PMID:17289047.
28. Henderson, B.A., and Anderson, D.M. 2002. Phenotypic differences in buoyancy and energetics of lean and siscowet lake charr in lake superior. Environ. Biol. Fishes, 64(1-3): 203-209. doi:10.1023/A:1016023027437.
29. Hrabik, T.R., Jensen, O.P., Martell, S.J.D., Walters, C.J., and Kitchell, J.F. 2006. Diel vertical migration in the Lake Superior pelagic community. I. Changes in vertical migration of coregonids in response to varying predation risk. Can. J. Fish. Aquat. Sci. 63(10): 2286-2295. doi:10.1139/f06-124.
30. Iijima, N., Gotou, T., and Kayama, M. 1995. Isolation and characterization of serum-lipoproteins in red-sea bream. Fish. Sci. 61(2): 297-303.
31. Jeukens, J., Renaut, S., St-Cyr, J., Nolte, A.W., and Bernatchez, L. 2010. The transcriptomics of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis spp., Salmonidae) divergence as revealed by next-generation sequencing. Mol. Ecol. 19(24): 5389-5403. doi:10.1111/j.1365-294X.2010.04934.x. PMID:21087448.
32. Jobling, M., and Bendiksen, E.A. 2003. Dietary lipids and temperature interact to influence tissue fatty acid compositions of Atlantic salmon, Salmo salar L., parr. Aquac. Res. 34(15): 1423-1441. doi:10.1111/j.1365-2109.2003.00970.x.
33. Johnson, R., Kroeger, E., Reichert, W., Deavila, D., and Rust, M. 2013. Abundance and origins of plasma lipids in sexually maturing female coho salmon Oncorhynchus kisutch (Walbaum) in culture. Aquac. Res. [In press.]: doi:10. 1111/are.12122.
34. Jonsson, B., and Jonsson, N. 2001. Polymorphism and speciation in arctic charr. J. Fish. Biol. 58(3): 605-638. doi:10.1111/j.1095-8649.2001.tb00518.x.
35. Kjaer, M.A., Vegusdal, A., Berge, G.M., Galloway, T.F., Hillestad, M., Krogdahl, A., Holm, H., and Ruyter, B. 2009. Characterisation of lipid transport in Atlantic cod (Gadus morhua) when fasted and fed high or low fat diets. Aquaculture, 288(3-4): 325-336. doi:10.1016/j.aquaculture.2008.12.022.
36. Kolditz, C., Borthaire, M., Richard, N., Corraze, G., Panserat, S., Vachot, C., Lefevre, F., and Medale, F. 2008a. Liver and muscle metabolic changes induced by dietary energy content and genetic selection in rainbow trout (Oncorhynchus mykiss). Am. J. Physiol. Regul. Integr. Comp. Physiol. 294(4): R1154-R1164. doi:10.1152/ajpregu.00766.2007. PMID:18234747.
37. Kolditz, C.I., Paboeuf, G., Borthaire, M., Esquerre, D., SanCristobal, M., Lefevre, F., and Medale, F. 2008b. Changes induced by dietary energy intake and divergent selection for muscle fat content in rainbow trout (Oncorhynchus mykiss), assessed by transcriptome and proteome analysis of the liver. BMC Genomics, 9: 506. doi:10.1186/1471-2164-9-506. PMID:18959775.
38. Kolditz, C.I., Plagnes-Juan, E., Quillet, E., Lefevre, F., and Medale, F. 2010. Changes in white muscle transcriptome induced by dietary energy levels in two lines of rainbow trout (Oncorhynchus mykiss) selected for muscle fat content. Br. J. Nutr. 103(5): 629-642. doi:10.1017/S0007114509992340. PMID: 19874644.
39. Kozlova, T.A., and Khotimchenko, S.V. 2000. Lipids and fatty acids of two pelagic cottoid fishes (Comephorus spp.) endemic to Lake Baikal. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 126(4): 477-485. doi:10.1016/S0305-0491(00) 00207-8.
40. Lin, J., Arnold, H.B., Della-Fera, M.A., Azain, M.J., Hartzell, D.L., and Baile, C.A. 2002. Myostatin knockout in mice increases myogenesis and decreases adipogenesis. Biochem. Biophys. Res. Comm. 291(3): 701-706. doi:10.1006/bbrc. 2002.6500.
41. Lu, G., and Bernatchez, L. 1999. Correlated trophic specialization and genetic divergence in sympatric lake whitefish ecotypes (Coregonus clupeaformis): support for the ecological speciation hypothesis. Evolution, 53(5): 1491-1505. doi:10.2307/2640895.
42. MacFarlane, R.B., Harvey, H.R., Bowers, M.J., and Patton, J.S. 1990. Serum lipoproteins in striped bass (Morone saxatilis): effects of starvation. Can. J. Fish. Aquat. Sci. 47(4): 739-745. doi:10.1139/f90-084.
43. McKay, M.C., Lee, R.F., and Smith, M.A.K. 1985. The characterization of the plasma-lipoproteins of the channel catfish Ictalurus punctatus. Physiol. Zool. 58(6): 693-704.
44. McPherron, A.C. 2010. Metabolic functions of myostatin and gdf11. Immunol. Endocr. Metab. Agents Med. Chem. 10(4): 217-231. doi:10.2174/187152210793663810.
45. McPherron, A.C., and Lee, S.-J. 2002. Suppression of body fat accumulation in myostatin-deficient mice. J. Clin. Invest. 109(5): 595-601. doi:10.1172/JCI200213562. PMID:11877467.
46. Moore, S.A., and Bronte, C.R. 2001. Delineation of sympatric morphotypes of lake trout in Lake Superior. Trans. Am. Fish. Soc. 130(6): 1233-1240. doi:10. 1577/1548-8659(2001)130<1233:DOSMOL>2.0.CO;2.
47. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29(9): e45. doi:10.1093/nar/29.9.e45. PMID:11328886.
48. Quillet, E., Le Guillou, S., Aubin, J., and Fauconneau, B. 2005. Two-way selection for muscle lipid content in pan-size rainbow trout (Oncorhynchus mykiss). Aquaculture, 245(1-4): 49-61. doi:10.1016/j.aquaculture.2004.12.014.
49. Rescan, P.Y., Jutel, I., and Ralliere, C. 2001. Two myostatin genes are differentially expressed in myotomal muscles of the trout (Oncorhynchus mykiss). J. Exp. Biol. 204 (Pt 20): 3523-3529.
50. Roberts, S.B., and Goetz, F.W. 2003. Myostatin protein and RNA transcript levels in adult and developing brook trout. Mol. Cell. Endocrinol. 210(1-2): 9-20. doi:10.1016/j.mce.2003.09.002.
51. Robinson, B.W., and Wilson, D.S. 1994. Character release and displacement in fishes: a neglected literature. Am. Nat. 144(4): 596-627. doi:10.1086/285696.
52. Rosauer, D.R., Biga, P.R., Lindell, S.R., Binkowski, F.P., Shepherd, B.S., Palmquist, D.E., Simchick, C.A., and Goetz, F.W. 2011. Development of yellow perch (Perca flavescens) broodstocks: initial characterization of growth and quality traits following grow-out of different stocks. Aquaculture, 317(1-4): 58-66. doi:10.1016/j.aquaculture.2011.03.037.
53. Sitar, S.P. 2013. Assessment of lake trout stocks in Michigan waters of Lake Superior, 1998 to 2007. Michigan Department of Natural Resources Fisheries Research Report. [In press.]
54. Skjaeraasen, J.E., Nash, R.D., Korsbrekke, K., Fonn, M., Nilsen, T., Kennedy, J., Nedreaas, K.H., Thorsen, A., Witthames, P.R., Geffen, A.J., Hoie, H., and Kjesbu, O.S. 2012. Frequent skipped spawning in the world's largest cod population. Proc. Natl. Acad. Sci. U.S.A. 109(23): 8995-8999. doi:10.1073/pnas. 1200223109. PMID:22615381.
55. Skulason, S., and Smith, T.B. 1995. Resource polymorphisms in vertebrates. Trends Ecol. Evol. 10(9): 366-370. doi:10.1016/S0169-5347(00)89135-1.
56. Skulason, S., Snorrason, S.S., Noakes, D.L.G., and Ferguson, M.M. 1996. Genetic basis of life history variations among sympatric morphs of Arctic char, Salvelinus alpinus. Can. J. Fish. Aquat. Sci. 53(8): 1807-1813. doi:10.1139/f96-098.
57. St-Cyr, J., Derome, N., and Bernatchez, L. 2008. The transcriptomics of lifehistory trade-offs in whitefish species pairs (Coregonus sp.). Mol. Ecol. 17(7): 1850-1870. doi:10.1111/j.1365-294X.2008.03696.x. PMID:18312278.
58. Stockwell, J.D., Hrabik, T.R., Jensen, O.P., Yule, D.L., and Balge, M. 2010. Empirical evaluation of predator-driven diel vertical migration in Lake Superior. Can. J. Fish. Aquat. Sci. 67(3): 473-485. doi:10.1139/F09-198.
59. Svedang, H. 1990. Genetic basis of life-history variation of dwarf and normal arctic charr, Salvelinus alpinus (L.), in Stora Rosjon, central Sweden. J. Fish. Biol. 36(6): 917-932. doi:10.1111/j.1095-8649.1990.tb05638.x.
60. Tait, J.S. 1959. Swimbladder studies in salmonids relating to problems of depth. Ph.D. thesis, University of Toronto, Toronto, Ont.
61. Templeton, M.C. 1961. Microdetermination of glycogen with anthrone reagent. Northwestern University, Dept. Medical Anatomy, Publication No. 658: 670-672.
62. Tocher, D.R. 2003. Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fish. Sci. 11(2): 107-184. doi:10.1080/713610925.
63. Wallaert, C., and Babin, P.J. 1994. Age-related, sex-related, and seasonal-changes of plasma-lipoprotein concentrations in trout. J. Lipid Res. 35(9): 1619-1633. PMID:7806976.
64. Wang, Y.J., Miller, L.A., Perren, M., and Addis, P.B. 1990. Omega-3 fatty acids in Lake Superior fish. J. Food Sci. 55: 71-76. doi:10.1111/j.1365-2621.1990. tb06018.x.
65. Wilkes, J.J., Lloyd, D.J., and Gekakis, N. 2009. Loss-of-function mutation in myostatin reduces tumor necrosis factor αproduction and protects liver against obesity-induced insulin resistance. Diabetes, 58(5): 1133-1143. doi:10.2337/ db08-0245. PMID:19208906.
66. Yang, X., Sheng, W., Sun, G.Y., and Lee, J.C. 2011. Effects of fatty acid unsaturation numbers on membrane fluidity and α-secretase-dependent amyloid precursorproteinprocessing. Neurochem. Int.58(3):321-329. doi:10.1016/j.neuint. 2010.12.004. PMID:21184792.
67. Zimmerman, M.S., Krueger, C.C., and Eshenroder, R.L. 2006. Phenotypic diversity of lake trout in Great Slave Lake: differences in morphology, buoyancy, and habitat depth. Trans. Am. Fish. Soc. 135(4): 1056-1067. doi:10.1577/T05-237.1.