Is salmon smoltification an example of vertebrate metamorphosis? Lessons learnt from work on flatfish larval development

Aquaculture

Volumn 362-363, Issue , 2012, Pages 264-272

  Björnsson, Björn Thrandur ^a   Einarsdottir, Ingibjörg Eir ^a   Power, Deborah ^b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Development; Flatfish; Metamorphosis; Parr smolt transformation; Salmonids; Smoltification

Indexed keywords

ENDOCRINE DISRUPTOR; FLATFISH; GENE EXPRESSION; LARVAL DEVELOPMENT; METAMORPHOSIS; MORPHOLOGY; SALMONID; SMOLT; VERTEBRATE;

PLEURONECTIFORMES; SALMONIDAE; VERTEBRATA;

EID: 84866854918     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2011.03.002     Document Type: Article

References (63)

1. Adzhubei A.A., Vlasova A.V., Hagen-Larsen H., Ruden T.A., Laerdahl J.K., Høyheim B. Annotated expressed sequence tags (ESTs) from pre-smolt Atlantic salmon (Salmo salar) in a searchable data resource. BMC Genomics 2007, 8:209.
2. Arnesen A.M., Toften H., Agustsson T., Stefansson S.O., Handeland S.O., Björnsson B.Th. Osmoregulation, feed intake, growth and growth hormone levels in 0+ Atlantic salmon (Salmo salar L.) transferred to seawater at different stages of smolt development. Aquaculture 2003, 222:167-187.
3. Aroua S., Schmitz M., Baloche S., Vidal B., Rousseau K., Dufour S. Endocrine evidence that silvering, a secondary metamorphosis in the eel, is a pubertal rather than a metamorphic event. Neuroendocrinology 2005, 82:221-232.
4. Aubin-Horth N., Landry C.R., Letcher B.H., Hofmann H.A. Alternative life histories shape brain gene expression profiles in males of the same population. Proc. Biol. Sci. 2005, 272:1655-1662.
5. Aubin-Horth N., Letcher B.H., Hofman H.A. Gene-expression signatures of Atlantic salmon's plastic life cycle. Gen. Comp. Endocrinol. 2009, 163:278-284.
6. Barrington E.J.W. Metamorphic processes in fish and lampreys. Am. Zool. 1961, 1:97-106.
7. Bern H.A. Endocrinological studies on normal and abnormal salmon smoltification. Comparative Endocrinology, Elsevier 1978, 97-100. P.J. Gaillard, H.H. Boer (Eds.).
8. Bishop C.D., Erezyilmaz D.F., Flatt T., Georgiou C.D., Hadfield M.G., Heyland A., Hodin J., Jacobs M.W., Maslakova S.A., Pires A., Reitzel A.M., Santagata S., Tanakay K., Youson J.H. What is metamorphosis?. Integr. Comp. Biol. 2006, 46:655-661.
9. Björnsson B.Th., Ogasawara T., Hirano T., Bolton J.P., Bern H.A. Elevated growth hormone levels in stunted Atlantic salmon, Salmo salar. Aquaculture 1988, 73:275-281.
10. Björnsson B.Th., Young G., Lin R.J., Deftos L.J., Bern H.A. Smoltification and seawater adaptation in coho salmon (Oncorhynchus kisutch): Plasma calcium regulation, osmoregulation, and calcitonin. Gen. Comp. Endocrinol. 1989, 74:346-354.
11. Cheng C.L., Gan K.J., Flamarique I.N. Thyroid hormone induces a time-dependent opsin switch in the retina of salmonid fishes. Gen. Comp. Endocrinol. 2009, 50:3024-3032.
12. de Jesus E.G., Inui Y., Hirano T. Cortisol enhances the stimulating action of thyroid hormones on dorsal fin-ray resorption of flounder larvae in vitro. Gen. Comp. Endocrinol. 1990, 79:167-173.
13. de Jesus E.G., Hirano T., Inui Y. Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. Gen. Comp. Endocrinol. 1991, 82:369-376.
14. de Jesus E.G., Hirano T., Inui Y. Flounder metamorphosis: Its regulation by various hormones. Fish Physiol. Biochem. 1993, 11:323-328.
15. Dickhoff W.W., Folmar L.C., Gorbman A. Changes in plasma thyroxine during smoltification of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 1978, 36:229-232.
16. Dickhoff W.W., Brown C.L., Sullivan C.V., Bern H.A. Fish and amphibian models for developmental endocrinology. J. Exp. Zool. Suppl. 1990, 4:90-97.
17. Einarsdóttir I.E., Silva N., Power D.M., Smáradóttir H., Björnsson B.Th. Thyroid and pituitary gland development from hatching through metamorphosis of a teleost flatfish, the Atlantic halibut. Anat. Embryol. 2006, 211:47-60.
18. Fleming I.A. Reproductive strategies of Atlantic salmon: ecology and evolution. Rev. Fish Biol. Fish. 1996, 6:379-416.
19. Folmar L.C., Dickhoff W.W. The parr-smolt transformation (smoltification) and seawater adaptation in salmonids: a review of selected literature. Aquaculture 1980, 21:1-37.
20. Folmar L.C., Dickhoff W.W., Mahnken C.V.W., Waknitz F.W. Stunting and parr-reversion during smoltification of coho salmon (Oncorhynchus kisutch). Aquaculture 1982, 28:91-104.
21. Galay-Burgos M., Power D.M., Llewellyn L., Sweeney G.E. Thyroid hormone receptor expression during metamorphosis of Atlantic halibut (Hippoglossus hippoglossus). Mol. Cell. Endocrinol. 2008, 281:56-63.
22. Gorbman A., Dickhoff W.W., Migell J.L., Prentice E.F., Waknitz F.W. Morphological indices of developmental progress in the parr-smolt coho salmon, Oncorhynchus kisutch. Aquaculture 1982, 28:1-19.
23. Hagen-Larsen H., Laerdahl J.K., Panitz F., Adzhubei A., Høyheim B. An EST-based approach for identifying genes expressed in the intestine and gills of pre-smolt Atlantic salmon (Salmo salar). BMC Genomics 2005, 6:171.
24. Harada M., Yoshinaga T., Ojima O., Iwata M. cDNA cloning and expression analysis of thyroid hormone receptor in the coho salmon Oncorhynchus kisutch during smoltification. Gen. Comp. Endocrinol. 2008, 155:658-667.
25. Hildahl, J., 2007. Endocrine Regulation of Flatfish Metamorphosis: Growth Hormone, Insulin-Like Growth Factor-I and their Receptors in Atlantic Halibut. Ph.D.-thesis, Göteborg University.
26. Hildahl J., Sweeny G.E., Galay-Burgos M., Einarsdottir I.E., Björnsson B.Th. Cloning of Atlantic halibut growth hormone receptor genes and quantitative gene expression during metamorphosis. Gen. Comp. Endocrinol. 2007, 151:143-152.
27. Hildahl J., Sweeney G.E., Galay-Burgos M., Einarsdottir I.E., Björnsson B.Th. Identification of two isoforms of Atlantic halibut insulin-like growth factor-I receptor genes and quantitative gene expression during metamorphosis. Comp. Biochem. Physiol. B 2007, 147:395-401.
28. Hildahl J., Power D.M., Björnsson B.Th., Einarsdottir I.E. The growth hormone-insulin-like growth factor I system is involved in cranial remodeling during halibut metamorphosis as indicated by tissue- and stage-specific receptor gene expression and the presence of growth hormone receptor protein. Cell Tissue Res. 2008, 332:211-225.
29. Hoar W.S. Smolt transformation-evolution, behavior, and physiology. J. Fish. Res. Board Can. 1976, 33:1233-1252.
30. Hoar W.S. The physiology of smolting salmonids. Fish Physiology, Vol. XIB 1988, 275-343. Academic Press, New York. W.S. Hoar, D.J. Randall (Eds.).
31. Hutchison M.J., Iwata M. Decreased aggressive behavior in masu salmon (Oncorhynchus masou) during the parr-smolt transformation. Mem. Fac. Fish. Hokkaido Univ 1997, 44:22-25.
32. Isorna E., Obregon M.J., Calvo R.M., Vazquez R., Pendon C., Falcon J., Munoz-Cueto J.A. Iodothyronine deiodinases and thyroid hormone receptors regulation during flatfish (Solea senegalensis) metamorphosis. J. Exp. Zool. 2009, 312B:231-246.
33. Iwata M., Komatsu S., Hasegawa S., Ogasawara T., Hirano T. Inconsistent effect of thyroid hormone alteration on seawater adaptability of fry of the chum salmon Oncorhynchus keta. Nippon Suisan Gakkaishi 1987, 53:1969-1973.
34. Iwata M., Tsuboi H., Yamashita T., Amemiya A., Yamada H., Chiba H. Function and trigger of thyroxine surge in migrating chum salmon Oncorhynchus keta fry. Aquaculture 2003, 222:315-329.
35. Johnston C.E., Eales J.G. Purines in the integument of Atlantic salmon (Salmo salar) during parr-smolt transformation. J. Fish. Res. Board Can. 1967, 24:955-964.
36. Just, J.J., Kraus-Just, J., Check, D.A., 1981. Survey of chordate metamorphosis. In: Gilbert, L.I., Frieden, E. (eds.), Metamorphosis: A Problem in Developmental Biology, 2nd ed., Plenum Press, New York, pp. 265-326.
37. Kubo T. Notes on the phase differentiation and smolt transformation of juvenile masu salmon (Oncorhynchus masou). Sci. Rep. Hokkaido Salmon Hatchery 1974, 28:9-26.
38. McCormick S.D. Evolution of the hormonal control of animal performance: insights from the seaward migration of salmon. Integr. Comp. Biol. 2009, 49:408-422.
39. McCormick S.D., Saunders R.L. Preparatory physiological adaptations for marine life of salmonids: osmoregulation, growth, and metabolism. Am. Fish. Soc. Symp. 1987, 1:211-229.
40. McCormick S.D., Lerner D.T., Monette M.Y., Nieves-Puigdoller K., Kelly J.T., Björnsson B.Th. Taking it with you when you go: how perturbations to the freshwater environment, including temperature, dams, and contaminants, affect marine survival of salmon. Am. Fish. Soc. Symp. 2009, 69:195-214.
41. Miwa S., Tagawa M., Inui Y., Hirano T. Thyroxine surge in metamorphosing flounder larvae. Gen. Comp. Endocrinol. 1988, 70:158-163.
42. Ojima D., Iwata M. Seasonal changes in plasma thyroxine kinetics in coho salmon Oncorhynchus kisutch during smoltification. Aquaculture 2007, 273:329-336.
43. Paris M., Laudet V. The history of a developmental stage: Metamorphosis in chordates. Genesis 2008, 46:657-672.
44. Plisetskaya E., Swanson P., Bernard M.G., Dickhoff W.W. Insulin in coho salmon (Oncorhynchus kisutch) during the parr-smolt transformation. Aquaculture 1988, 72:151-164.
45. Power D.M., Llewellyn L., Faustino M., Nowell M.A., Björnsson B.Th., Einarsdóttir I.E., Canario A.V.M., Sweeney G.E. Thyroid hormones in growth and development of fish. Comp. Biochem. Physiol. C 2001, 130:447-459.
46. Power D.M., Campinho M.A., Silva N. Metamorphosis. Fish Larval Physiology 2008, 607-638. Science Publishers, Enfield. R.N. Finn, B.G. Kapoor (Eds.).
47. Power D.M., Einarsdottir I.E., Pittman K., Sweeney G.E., Hildahl J., Campinho M.A., Silva N., Sæle Ø., Galay-Burgos M., Smáradóttir H., Björnsson B.Th. The molecular and endocrine basis of flatfish metamorphosis. Rev. Fish. Sci. 2008, 16(S1):93-109.
48. Richman N.H.I.I.I., Tai de Diaz S., Nishioka R.S., Prunet P., Bern H.A. Osmoregulatory and endocrine relationships with chloride cell morphology and density during smoltification in coho salmon (Oncorhynchus kisutch). Aquaculture 1987, 60:265-285.
49. Saele O., Solbakken J.S., Watanabe K., Hamre K., Power D., Pittman K. Staging of Atlantic halibut (Hippoglossus hippoglossus L.) from first feeding through metamorphosis, including cranial ossification independent of eye migration. Aquaculture 2004, 239:445-465.
50. Seear P.J., Carmichael S.N., Talbot R., Taggart J.B., Bron J.E., Sweeney G.E. Differential gene expression during smoltification of Atlantic salmon (Salmo salar L.): a first large-scale microarray study. Mar. Biotechnol. 2010, 12:126-140.
51. Shrimpton J.M., Björnsson B.Th., McCormick S.D. Can Atlantic salmon smolt twice? Endocrine and biochemical changes during smolting. Can. J. Fish. Aquat. Sci. 2000, 57:1969-1976.
52. Specker J.L., Schreck C.B. Changes in plasma corticosteroids during smoltification of coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 1982, 46:53-58.
53. Staley K.B., Ewing R.D. Purine levels in the skin of juvenile coho salmon (Oncorhynchus kisutch) during parr-smolt transformation and adaptation to seawater. Comp. Biochem. Physiol. B 1992, 447-452.
54. Stefansson S.O., Björnsson B.Th., Ebbesson L.O.E., McCormick S.D. Smoltification. Fish Larval Physiology 2008, 639-681. Science Publishers, Enfield. R.N. Finn, B.G. Kapoor (Eds.).
55. Sweeting R.M., Wagner G.F., McKeown B.A. Changes in plasma glucose, amino acid nitrogen and growth hormone during smoltification and seawater adaptation in coho salmon, Oncorhynchus kisutch. Aquaculture 1985, 45:185-197.
56. Taranger G.L., Carrillo M., Schulz R.W., Fontaine P., Zanuy S., Felip A., Weltzien F.A., Dufour S., Karlsen O., Norberg B., Andersson E., Hansen T. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 2010, 165:483-515.
57. Temple S.E., Ramsden S.D., Haimberger T.J., Veldhoen K.M., Veldhoen N.J., Carter N.L., Roth W.M., Hawryshyn C.W. Ontogenetic changes in photoreceptor opsin gene expression in coho salmon (Oncorhynchus kisutch, Walbaum). J. Exp. Biol. 2008, 211:3879-3888.
58. Wald, G., 1981. Metamorphosis: an overview. In Gilbert, L.I., Frieden, E., (eds). Metamorphosis, a Problem in Developmental Biology, ed 2. New York, Plenum Press, pp 1-39.
59. Winans G.A., Nishioka R.S. A multivariate description of change in body shape of coho salmon (Oncorhynchus kisutch) during smoltification. Aquaculture 1987, 66:235-245.
60. Yamano K. The role of thyroid hormone in fish development with reference to aquaculture. JARQ 2005, 39:161-168.
61. Yamano K., Miwa S. Differential gene expression of thyroid hormone receptor alpha and beta in fish development. Gen. Comp. Endocrinol. 1998, 109:75-85.
62. Young G., Björnsson B.Th., Lin R.J., Bolton J.P., Prunet P., Bern H.A. Smoltification and seawater adaptation in coho salmon, Oncorhynchus kisutch: Plasma prolactin, growth hormone, thyroid hormones and cortisol. Gen. Comp. Endocrinol. 1989, 74:335-345.
63. Youson J.H. First metamorphosis. Fish Physiology, Volume XI The Physiology of Developing Fish 1988, 135-196. Academic Press, San Diego. W.S. Hoar, D.J. Randall (Eds.).