HETEROZYGOSITY-FITNESS CORRELATIONS IN RAINBOW TROUT: EFFECTS OF ALLOZYME LOCI OR ASSOCIATIVE OVERDOMINANCE?
G. C. Thelen
Division of Biological Sciences, University of Montana, Missoula, Montana 59812
Search for more papers by this authorF. W. Allendorf
Division of Biological Sciences, University of Montana, Missoula, Montana 59812. E-mail: [email protected]
Search for more papers by this authorG. C. Thelen
Division of Biological Sciences, University of Montana, Missoula, Montana 59812
Search for more papers by this authorF. W. Allendorf
Division of Biological Sciences, University of Montana, Missoula, Montana 59812. E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract.— Previous studies with rainbow trout (Oncorhynchus mykiss) have shown that increased heterozygosity at allozyme loci is correlated with several phenotypic traits associated with fitness. We expected to find a similar effect of heterozygosity at other nuclear loci if these associations are due to loci in linkage disequilibrium with the allozyme loci (i.e., associative overdominance), rather than the allozymes themselves. We examined the association between multiple locus heterozygosity and condition factor at 10 allozyme and 10 microsatellite loci. Individuals that were more heterozygous at allozyme loci had significantly greater condition factor in two hatchery cohorts of rainbow trout (1996 P= 0.006; 1997 P < 0.001). In contrast, there was no evidence at microsatellite loci that increased heterozygosity was associated with greater condition factor. Our results suggest that the observed relationship between heterozygosity at allozyme loci and condition factor in rainbow trout appears to be due to the allozyme loci themselves, rather than associative overdominance. We cannot, however, rule out that differences in the mutation process between allozymes and microsatellites may be responsible for these observations. Regardless of the underlying mechanism, these results support the view that allozymes and microsatellites are differentially affected by natural selection.
Literature Cited
- Allendorf, F. W., and R. G. Danzmann. 1997. Secondary tetrasomic segregation of MDH-B and preferential pairing of homeologues in rainbow trout. Genetics 145: 1083–1092.
- Allendorf, F. W., and L. W. Seeb. 2000. Concordance of genetic divergence among sockeye salmon populations at allozyme, nuclear DNA, and mtDNA markers. Evolution 54: 640–651.
-
Allendorf, F. W., and
G. Thorgaard. 1984. Polyploidy and the evolution of salmonid fishes. Pp.
1–53
in
B. J. Turner, ed.
The evolutionary genetics of fishes. Plenum Press,
New York
.
10.1007/978-1-4684-4652-4_1 Google Scholar
- Allendorf, F. W., K. L. Knudsen, and S. R. Phelps. 1982. Identification of a gene regulating the tissue expression of a phosphoglucomutase locus in rainbow trout. Genetics 102: 259–268.
- Allendorf, F. W., K. L. Knudsen, and R. F. Leary. 1983. Adaptive significance of differences in the tissue-specific expression of a phosphoglucomutase gene in rainbow trout. Proc. Natl. Acad. Sci., USA 80: 1397–1400.
- Allendorf, F. W., G. Ståhl, and N. Ryman. 1984. Silencing of duplicate genes: a null allele polymorphism for lactate dehydrogenase in brown trout (Salmo trutta). Mol. Biol. Evol. 1: 238–248.
- Allendorf, F. W., W. A. Gellman, and G. H. Thorgaard. 1994. Sex-linkage of two enzyme loci in Oncorhynchus mykiss (rainbow trout). Heredity 72: 498–507.
-
Banks, M. A.,
M. S. Blouin,
B. A. Baldwin,
V. K. Rashbrook,
H. A. Fitzgerald,
S. M. Blankenship, and
D. Hedgecock. 1999. Isolation and inheritance of novel microsatellites in chinook salmon (Oncorhynchus tshawytscha).
J. Hered.
90: 281–288.
10.1093/jhered/90.2.281 Google Scholar
- Bierne, N., A. Tsitrone, and P. David. 2000. An inbreeding model of associative overdominance during a population bottleneck. Genetics 155: 1981–1990.
- Britten, H. B. 1996. Meta-analysis of the association between multilocus heterozygosity and fitness. Evolution 50: 2158–2164.
- Brookfield, J. F. 1996. A simple new method for estimating null allele frequency from heterozygote deficiency. Mol. Ecol. 5: 453–455.
-
Brookfield, J. F.
1999. Allozymes again.
Evolution
53: 632–634.
10.1111/j.1558-5646.1999.tb03799.x Google Scholar
-
Brown, M. E.
1957. Experimental studies on growth. Pp.
361–400
in
M. E. Brown, ed.
The physiology of fishes. Academic Press,
New York
.
10.1016/B978-1-4832-2817-4.50015-9 Google Scholar
- Burton, R. S., and M. W. Feldman. 1983. Physiological effects of an allozyme polymorphism: glutamate-pyruvate transaminase and response to hyperosmotic stress in the copepod Tigriopus californicus. Biochem. Genet. 21: 239–251.
- Coltman, D. W., W. D. Bowen, J. M. Wright. 1998. Birth weight and neonatal survival of harbour seal pups are positively correlated with genetic variation measured by microsatellites. Proc. R. Soc. Lond. B. 265: 803–809.
- Coulson, T. N., J. M. Pemberton, S. D. Albon, M. Beaumont, T. C. Marshall, J. Slate, F. E. Guinness, and T. H. Clutton-Brock. 1998. Microsatellites reveal heterosis in red deer. Proc. R. Soc. Lond. B. 265: 489–495.
- Crow, J. F., and M. J. Simmons. 1983. The mutation load in Drosophila. Pp. 1–35 in M. Ashburner, H. L. Carson, and J. N. Thompson, eds. The genetics and biology of Drosophila. Vol. 3c. Academic Press, London .
- Danzmann, R. G., M. F. Ferguson, and F. W. Allendorf. 1985. Allelic differences in initial expression of paternal alleles at an isocitrate dehydrogenase locus in rainbow trout (Salmo gairdneri). Dev. Genet. 5: 117–127.
- Danzmann, R. G., M. F. Ferguson, and F. W. Allendorf. 1986a. Does enzyme heterozygosity influence developmental rate in rainbow trout Heredity 56: 417–425.
- Danzmann, R. G., M. M. Ferguson, F. W. Allendorf, and K. L. Knudsen. 1986b. Heterozygosity and developmental rate in a strain of rainbow trout (Salmo gairdneri). Evolution 40: 86–93.
- Danzmann, R. G., M. F. Ferguson, and F. W. Allendorf. 1987. Heterozygosity and oxygen-consumption rate as predictors of growth and developmental rate in rainbow trout. Physiol. Zool 60: 211–220.
- Danzmann, R. G., M. F. Ferguson, and F. W. Allendorf. 1988. Heterozygosity and components of fitness of rainbow trout. Biol. J. Linn. Soc. 33: 285–304.
- David, P. 1997. Modeling the genetic basis of heterosis: tests of alternative hypotheses. Evolution 51: 1049–1057.
- David, P. 1998. Heterozygosity-fitness correlations: new perspectives on old problems. Heredity 80: 531–537.
-
Dempster, A. P.,
N. M. Laird, and
D. B. Rubin. 1977. Maximum likelihood from incomplete data via the EM algorithm.
J. R. Stat. Soc. B
39: 1–38.
10.1111/j.2517-6161.1977.tb01600.x Google Scholar
- Estoup, A., and B. Angers. 1998. Microsatellites and minisatellites for molecular ecology: theoretical and empirical considerations. Pp. 55–86 in G. R. Carvalho, ed. Advances in molecular ecology. IOS Press, Amsterdam , The Netherlands .
- Goldstein, D. B., A. R. Linares, L. L. Cavalli-Sforza, and M. W. Feldman. 1995. An evaluation of genetic distances for use with microsatellite loci. Genetics 139: 463–471.
- Jackson, D. A., H. H. Harvey, and K. M. Somers. 1990. Ratios in aquatic sciences: statistical shortcomings with mean depth and the morphometric index. Can. J. Fish. Aquat. Sci. 47: 1788–1795.
- Johnson, K. R., J. E. Wright Jr., and B. May. 1987. Linkage relationships reflecting ancestral tetraploidy in salmonid fish. Genetics 116: 579–591.
- Karl, S. A., and J. C. Avise. 1992. Balancing selection at allozyme loci in oysters: implications from nuclear RFLPs. Science 256: 100–102.
- Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1983. Developmental stability and enzyme heterozygosity in rainbow trout. Nature 301: 71–72.
- Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1984a. Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes. Am. Nat. 124: 540–551.
- Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1984b. Major morphological effects of a regulatory gene: Pgml-t in rainbow trout. Mol. Biol. Evol. 1: 183–194.
- Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1987. Differences in inbreeding coefficients do not explain the associations between heterozygosity at allozyme loci and developmental stability in rainbow trout. Evolution 41: 1413–1415.
- Leary, R. F., F. W. Allendorf, and K. L. Knudsen. 1993. Null alleles at two lactate dehydrogenase loci in rainbow trout are associated with decreased developmental stability. Genetica 89: 3–13.
- Ledig, F. T., R. P. Guries, and B. A. Bonefeld. 1983. The relation of growth to heterozygotes in pitch pine. Evolution 37: 1227–1238.
- Lindner, K. R., J. E. Seeb, C. Habicht, K. L. Knudsen, E. Kretschmer, D. J. Reedy, P. Spruell, and F. W. Allendorf. 2000. Genecentromere mapping of 312 marker loci in pink salmon by halftetrad analysis. Genome 43: 1–12.
- McConnell, S. K., P. O'Reilly, L. Hamilton, J. M. Wright, and P. Bentzen. 1995. Polymorphic microsatellite loci from Atlantic salmon (Salmo salar): genetic differentiation of North American and European populations. Can. J. Fish. Aquat. Sci. 52: 1863–1872.
- McDonald, J. H., B. C. Verrelli, and L. B. Geyer. 1996. Lack of geographic variation in anonymous nuclear polymorphisms in the American oyster, Crassostrea virginica. Mol. Biol. Evol. 13: 1114–1118.
-
Mitton, J. B.
1997. Selection in natural populations. Oxford Univ. Press,
New York
.
10.1093/oso/9780195063523.001.0001 Google Scholar
- Morris, D. B., K. R. Richard, and J. M. Wright. 1996. Microsatellites from rainbow trout (Oncorhynchus mykiss) and their use for genetic study of salmonids. Can. J. Fish. Aquat. Sci. 53: 120–126.
- Ohta, T. 1971. Associative overdominance caused by linked detrimental mutations. Genet. Res. 18: 277–286.
- Olsen, J. B., P. Bentzen, and J. Seeb. 1998. Characterization of seven microsatellite loci derived from pink salmon. Mol. Ecol. 7: 1083–1090.
- O'Reilly, P. T., L. C. Hamilton, S. K. McConnell, and J. M. Wright. 1996. Rapid detection of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Can. J. Fish. Aquat. Sci. 53: 2292–2298.
- Pamilo, P., and S. Pálsson. 1998. Associative overdominance, heterozygosity and fitness. Heredity 81: 381–389.
- Pogson, H. G., and E. Zouros. 1994. Allozyme and RFLP heterozygotes as correlates of growth rate in the scallop Placopecten magellanicus: a test of the associative overdominance hypothesis. Genetics 137: 221–231.
- Raymond, M., and F. Rousset. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86: 248–249.
- Sakamoto, T., N. Okamoto, and Y. Ikeda. 1994. Rapid communication: dinucleotide repeat polymorphism of rainbow trout, FGT3. J. Anim. Sci. 72: 2766.
- Sakamoto, T., R. G. Danzmann, K. Gharbi, P. Howard, A. Ozaki, S. K. Khoo, R. A. Woram, N. Okamoto, M. M. Ferguson, L. E. Holm, R. Guyomard, and B. Hoyheim. 2000. A microsatellite linkage map of rainbow trout (Oncorhynchus mykiss) characterized by large sex-specific differences in recombination rates. Genetics 155: 1331–1345.
- Savolainen, O., and P. Hedrick. 1995. Heterozygosity and fitness: no association in Scots pine. Genetics 140: 755–766.
- Schulte, P. M., M. Gomezchiarri, and D. A. Powers. 1997. Structural and functional differences in the promoter and 5′ flanking region of Ldh-B within and between populations of the teleost Fundulus heteroclitus. Genetics 145: 759–769.
- Scribner, K. T., J. R. Gust, and R. L. Fields. 1996. Isolation and characterization of novel salmon microsatellite loci: cross-species amplification and population genetic applications. Can. J. Fish. Aquat. Sci. 53: 833–841.
- Shaklee, J. B., F. W. Allendorf, D. C. Morizot, and G. S. Whitt. 1990. Gene nomenclature for protein-coding loci in fish. Trans. Am. Fish. Soc. 119: 2–15.
- Smouse, P. E. 1986. The fitness consequences of multiple-locus heterozygosity under the multiplicative overdominance and inbreeding depression models. Evolution 40: 946–957.
- Watt, W. B. 1994. Allozymes in evolutionary genetics: self-imposed burden or extraordinary tool Genetics 136: 11–16.
- Weir, B. S., and C. C. Cockerham. 1984. Estimating F-statistics for the analysis of population structure. Evolution 38: 1358–1370.
- Williams, R. F., Y. Pekarsky, S. Cheng, and K. Gardiner. 1994. YAC clones targeting gene-rich regions of human chromosome 3. Mamm. Genome 5: 380–383.
- Zouros, E. 1993. Associative overdominance: evaluating the effects of inbreeding and linkage disequilibrium. Genetica 89: 35–46.