Abstract
DNA sequence data was collected for the C and D introns in the duplicate growth hormone loci (GH1 and GH2) from Brachmystax lenok, two subspecies of Hucho hucho, Hucho (Parahucho) perryi, Salmo salar, Salmo trutta, Acantholingua ohridana (Salmothymus), six species of Salvelinus, eight species of Oncorhynchus including O. masou, and three outgroups including Thymallus thymallus, Coregonus artedi, and Coregonus clupeaformis. Phylogenetic analyses were performed using maximum parsimony and maximum likelihood (PAUP, version 4.08beta) with gaps as missing data and as a fifth base. B. lenok was basal in all of the trees and all of the other genera were monophyletic with the exception that A. ohridana always placed within Salmo, and H. hucho sp. often placed with B. lenok. The GH1 introns supported a sister relationship between Oncorhynchus and Salvelinus, while the combined GH2 introns were ambiguous at this node. This result contrasts with trees based on morphology and the ribosomal ITS1 sequences that support a sister relationship between Salmo and Oncorhynchus. The only estrogen response element (ERE) in the gene is found in the C intron and has mutated in GH2 in all of the species except B. lenok. The ERE element in GH1 has undergone another mutation in all of the species except for B. lenok, and members of the two genera Salvelinus and Oncorhynchus. Thus these latter two genera are the only ones with a difference in expression of GH1 and GH2 in the presence of estrogen. Differences in selective pressure on the introns in the duplicate genes in different taxa could account for the conflicting results obtained in the phylogenetic analysis.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allendorf, F.W. & G.H. Thorgaard. 1984. Tetraploidy and the evolution of salmonid fishes. pp. 1–53. In: B.J. Turner (ed.) Evolutionary Biology of Fishes, Plenum Publishing Co., New York.
Behnke, R.J. 1968. A new subgenus and species of trout: Platysalmo platycephalus from southcentral Turkey with comments on the classification of the subfamily Salmoninae. Mitteilungen Hamburgischen Zool. Mus. Instit. 66: 1–15.
Blackhall, W.J. 1994. A molecular study of introgression between westslope cutthroat trout and rainbow trout. MS Thesis. University of Alberta, Edmonton, Canada. 80 pp.
Devlin, R.H. 1993. Sequence of sockeye type 1 and type 2 growth hormone genes and the relationships of rainbow trout with Atlantic and Pacific salmon. Can. J. Fish. Aquat. Sci. 50: 1738–1748.
Felsenstein, J. 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evol. 39: 783–791.
Force, A., M. Lynch, F.B. Pickett, A. Amores, Y.L. Yan & J. Postlethwait. 1999. Preservation of duplicate genes by complementary degenerative mutations. Genetics 151: 1531–45.
Hadzisce, S. 1961. Zur Kenntnis des Salmothymus orhidanus (Steindachner) (Pisces, Salmonidae). Intl Vereinigung theoretische angewandte Limnol. Verhandlungen 14: 785–791.
Johansen, B., O.C. Johnsen & S. Valla. 1989. The complete nucleotide sequence of the growth-hormone gene from Atlantic salmon (Salmo salar). Gene (Amsterdam) 77: 317–324.
McKay, S.J. 1997. Evolutionary Genetic Analysis of Pacific Salmon and Trout, PhD. Thesis, Simon Fraser University, Burnaby, Canada. 140 pp.
McKay, S.J., R.H. Devlin & M.J. Smith. 1996. Phylogeny of Pacific salmon and trout based on growth hormone type-2 (GH2) and mitochondrial NADH dehydrogenase subunit 3 (ND3) DNA sequences. Can. J. Fish. Aquat. Sci. 53: 1165–1176.
McKay, S.J., M.J. Smith & R.H. Devlin. 1997. Polymerase chain reaction-based species identification of salmon and coastal trout in British Columbia. Mol. Mar. Biol. Biotech. 6: 131–140.
Oakley, T.H. & R.B. Phillips. 1999. Phylogeny of salmonine fish based on growth hormone introns: Atlantic (Salmo) and Pacific (Oncorhynchus) salmon are not sister taxa. Mol. Phylogen. Evol. 11: 381–393.
Phillips, R.B. & T.H. Oakley. 1997. Evolutionary relationships among salmonid fishes inferred from nuclear and mitochondrial sequences. Chapter 10 pp. 145–162. In: T. Kocher & C. Stepien (ed.) Molecular Systematics of Fishes, Academic Press, New York.
Phillips, R.B., M.P. Matsuoka, I. Konon & K.M. Reed. 2000. Phylogenetic analysis of mitochondrial and nuclear sequences supports inclusion of Acantholingua ohridana in Salmo. Copeia 2000: 546–550.
Prince, V.E. & F.B. Pickett. 2002. Splitting pairs: The diverging fates of duplicated genes. Nat. Rev. Genet. 3: 827–837.
Snoj, A.E. Melkic, S. Susnik, S. Muhamedagic & P. Dovc. DNA phylogeny supports revised classification of Salmothymus obtusirostris. 2002. Biol. J. Linn. Soc. 77: 399–411.
Stearley, R.F. & G.R. Smith. 1993. Phylogeny of the Pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae. Trans. Amer. Fish. Soc. 122: 1–33.
Svetovidov, A. 1975. Comparative osteological study of the Balkan endemic genus Salmothymus in relation to its classification. Zool. Zhurnal 54: 1174–1190.
Swofford, D. 2001. PAUP: Phylogenetic analysis using parsimony (beta ver. 4.08b). Illinois Natural History Association, Champaign, Illinois.
Westrich, K.M., N.R. Konkol, M.P. Matsuoka & R.B. Phillips. 2002. Interspecific relationships among charrs based on phylogenetic analysis of nuclear growth hormone introns. Environ. Biol. Fish. 64: 217–222.
Yang, B.-Y., K-M Chan, C.-M. Lin & Chen, T.T. 1997. Characterization of rainbow trout (Oncorhynchus mykiss) growth hormone 1 gene and the promoter region of growth hormone 2 gene. Arch. Biochem. Biophy. 340: 359–368.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Phillips, R.B., Matsuoka, M.P., Konkol, N.R. et al. Molecular Systematics and Evolution of the Growth Hormone Introns in the Salmoninae. Environmental Biology of Fishes 69, 433–440 (2004). https://doi.org/10.1023/B:EBFI.0000022873.32682.3f
Issue Date:
DOI: https://doi.org/10.1023/B:EBFI.0000022873.32682.3f