OVERDOMINANCE, EPISTASIS AND MASS SELECTION IN CORN. Dr. Gordon F. Sprague
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1 OVERDOMINANCE, EPISTASIS AND MASS SELECTION IN CORN Dr. Gordon F. Sprague Research Agronomist in Charge Corn and Sorghums Crops Research Div. Agricultural Research Service, U. S. Dept. of Agriculture, Beltsville, Maryland
2 -?5 - Overdominance, Epistasis and Mass in Corn Selection The normal function of a discussant is to evaluate the major items covered and to reconcile any differences in viewpoint if this is neceasary. In ths present case little information has been presented which deals directly with poultry. It appears, therefore, that a departure from the normal function of a discussant may be justified. Rather than reivew specific information presented I shall attempt to present information from corn which has some baaring on the various topics which have received consideration at these meetings Little can be added to the excellent reviews presented by Professor L. A. Snyder other than a word of caution as to the immediate usefulness of such information to quantitative genetics. There has been a tremsmdous advance in biochemical g_etics in recent years. Some of the high lights have been the one gene-one enzyme theory of Beadle and Tatum, the Watson. Crick hypothesis for the structure of DNA, the genetic code involving nucleotide combination and sequence for the production of the various aminoacids, the three types of RNA and the distinction between structural and operator genes_ It is understandable that much of this development has come in bacteria, phage or virus, and fungi as it is only in such forms that we have the combination of information on fine gene structure and biochemical activity. reviewed by If the situation represented by the three genes O, x and _t Professor Snyder, had been detected in a higher organism, where information on fine gone structure and correlated information on biochemical function were lacking, it is doubtful if the investigator could have done
3 more than conclude that he had identified a possible multiple allelic series which was in some way involved in the metabolism of beta-galactoside. I should hasten to add, however, that any developments which increase our basic knowledge concerning mutations, and how genes produce their characteristic effects will_ in the long run_ be stimulating even though it is not immediately reflected in new models or modified breeding Overdominance procedures. Professor Crow has presented evidence indicating a lack of overdominance associated with lethals in Drosophila Three lines of evidence are available in corn bearing on the importance of overdominance. The first of these utilizes North Carolina Design III in which random F2 plants from an F1 single cross are mated to the homozygous parental inbreds. The statistical model is presented and discussed in (1) (7). In the North Carolina (13) and in one of the Nebraska (8) reports the average degree of dominance estimate (E) for yield was significantly greater than 1.O indicating either overdominance or repulsion linkage bias. Estimates for most other traits studied fell within the partial dominance range. The hybrid population was advanced by random mating and new tests conducted in the F8 and F13 generations. The results obtained were as follows (13): Generation a estimate F2 i 68 F FI3 i 09 Neither the F8 nor FI3 estimate of _ was significantly greater than 1.0 ) indicating the importance of linkage bias and suggesting that overdominance was of little, if any, importance
4 The second line of evidence on overdominance comes from studies on specific combining ability (18). Recurrent selection was conducted in two populations A and B, using a long-time inbred parent as a common tester. If dominant or partially dominant genes are of major importance then successive repetitions of the selection process will change gene frehuency with q = 1 as a limit. If overdominance is of major importance and the gene frequency of the tester parent is q then gene frequencies in populations A and B will approach 1-q as a limit. A test of the relative importance of these two types of gene action is provided by inter-population performance after successive cycles of selection. Comparisons between the original population and the derived populations after one and two generations of selection are shown below: Hybrid Yield A x B (original) 70.6 k1 x B1 (after 1st cycle of selection) 7ho8 A2 x B2 (after 2nd cycle of selection) 81.7 The results of the Design III and specific combining studies are compatible with the assumption that overdominance is of limited importance. Such studies cannot, however, completely rule out overdominance as a possibility. In both instances the average effect over all loci is under measurement and an average effect of 1.O or less could involve some loci where effects were significantly greater than 1.Oo ) Preliminary information is available from a third approach which _ay,_eventually provide more precise information on the occurrence of loci exhibiting
5 overdominance effects. The technique is very simple. Mutations are induced in a long-time inbred line. Seed and seedling mutations ha_'e been studied because of space limitations o Progenies which exhibit a mono-hybrid segregation in F2 are grovm in the field on an extensive scale. Each F2 plant is self-pollinated end the following day the ear-bag removed to permit a full seed sib. Each F2 plant, following harvest, can be classified as to genotype (AA and Aa) and corresponding grain weights t determined. A simple analysis of variance is used to determine whether there is a significant difference between mean yield of genotypes. The mutant studied represent the usual chlorophyll deficiencies characteristically found in open-pollinated varieties. There is no reason to suppose this class of mutations would be any more or less likely to be associated with overdominance effects than other classes of mutants. Seed and seedling mutants are used solely because of ease in handling large populations. Among the mutants studied thus far complete dominance appears to be the usual condition. A few cases of partial dominance have been found but so far these have always been associated with some seed defect such as shrunken seeds, premature germination or other trait which would have a direct influence on grain yield. One case of heterozygote superiority has been found. This case involved a virescent seedling. Further work is necessary for verification. Data currently available suggest that the frequency of loci having overdominance effects is low but this is to be expected on theoretical grounds.
6 I should like to give one additional illustration, not because it demonstrates overdominance but because it provides a conceptual illustratioh of one type of behavior which would be expected mt loci exhibiting overdominance. Schwartz (19) has identified three alleles in corn affecting an otherwise unidentified esterace. These alleles are distinguishable by migration rates under starch gel electrophoresis. The alleles haye been designated as Es (slow)j En (normal)and Ef (fast). Any hybrid involving two of the alleles exhibits a complex electrophoretic pattern. Three bands are detectable; two characteristic of the two parents and a third (the heterozygote) which is unique for each hybrid. In other words a new hybrid enzyme is produced which is different from either parent. The hybrid enzyme migrates at an intermediate rate so there is no overdominance with respect to migration. However this enzyme must have some function other than migration, and in this other function the unique hybrid enzyme could conceivably perform in a manner or at a rate quite different from the two parental enzymes. Epistasis Some of the illustrations used by Professor Snyder indicate epistasis at the biochemical functional level. Evidence from quantitative genetic studies is less convincing. Eberhart (4) has conducted studies with two openpollinated varieties of corn and has found that epistasis is of little or no importance for yield. Other approaches (5, 6) indicate that epistasis may be of importance for some traits in specific combinations. The most direct _ evidence for the importance of epistasis on corn yields _is provided by contrasts between single and three-way cross means (l?). In sets involving
7 three lines_ as illustrated below_ the means of the two groups are in complete balance with respect to all intra-allelic interactions. Single crosses Three-way crosses AxB (AxB) xc AxC (AxC) xb B x C (B x C) x A x They are not balanced_ however, if inter-allelic interactions occur and are of importance. In comparisons involving 20 such sets a significant difference was found between the corresponding sets of means in about 25 percent of the cases. The lines used were of different varietal origin and had been subjected to intense screening on the basis of single-cross performance. It was speculated that the past history of selection may have been responsible for isolating types in which epistasis was of importance. Similar tests are being conducted with a group of unselected lines derived from a single variety to test this assumption. Data for a single year (unpublished) are now available and exhibit a similar response pattern. Thus prior selection appears not to be the factor of major importance. Our current speculation is that epistasis may be of importance in open-pollinated varieties but due to the averaging process involved in estimating, estimates of zero or near zero are obtained If this assumption is correct any restriction on heterogeniety of the test material would lead to a more favorable milieu for measurement of epistatic differences. Selection Professor L. N_ Hazel has considered some of the selection experiments
8 with insects and small animals. Selection in corn populations has had a somewhat varied history. Mass selection was almost the sole method of breeding until about 19OO. Selection must ha ve been effective to account for the wide diversity of ear and plant types and differences in maturity which n_ exist. For over twenty years very close ear selection was practiced for show card standards. Varieties and strains became widely disseminated on the basis of corn show winnings. No controls were utilized and hence no measure is available of the effectiveness of the selection practiced. The op_uion became general, about 1920_ that this selection was ineffective which set the stage for a complete shift to the inbreeding and hybridization approach. Results from the utilization of this method are common knowledge and need not concern us. Beginning in the late 1940's evidence began to accumulate indicating that additive genetic variance was important in open-pollinated varieties. When a sufficient body of such evidence accumulated it became imperative to re-examine the question of the effectiveness of mass selection since this should be the most effective method for manipulating additive effects. This re-examination was undoubtedly delayed for a period due to some reluctance to return to a previously discredited technique. The first reports of the effectiveness of mass selectionj under the new philosophy, were presented by Gardner (9). He utilized a sub-plot or grid system to minimize environmental effects. Remnant seed was also saved to provide a direct measure of progress. The results obtained with the variety
9 Golden Republic are listed below: Generation Yield (Bu.per A) original 79.3 Ist generation nd " rd " 89._ hth " 97.4 These studies are being continued and Professor Gardner informs me that additional progress has been made_ Even more striking improvements have been reported by Dr. E. C. Johnson (ii) of the Rockefeller Foundation working in Mexico. Generation Yield (Kgs. _er plot) Original 5.61 ist cycle nd cycle rd cycle 7.47 Thus the indicated importance of additive genetic variance has been amply verified by the effectiveness of mass selection. The classical selection experiments in corn are the high and low oil and high and low protein studies conducted at lllinois. The results from these studies are in sharp contrast to the small animal selection experiments reviewed. In the lllinois experiments divergence i s still proceeding after some 60 generations of selection. After 48 generations of continuous selection reverse selection was initiated in each of the four types: High oil, low oil, high protein and low protein. After 13 generations of reverse selection changes have been made in each population (12). The long term _ experiments with continuous selection and the shorter term experiments _ involving reverse selection provide convincing evidence for the continued
10 existance of additive genetic variability. These results then are in direct contrast to the results with small animals reviewed by Dr. Hazel. Professor Hazel has mentioned the possible bias in evaluation of differing genotypes housed in the same pen because of social order. possible counterpart in plants has been designated as competition. A The literature bearing on this topic is voluminous and I shall illustrate with two examples o The first example involves the subsequent history of a mixture of four adapted barley varieties reported by Suneson (20). In pure stands the yields of the varieties were in the order V&ughan, Hero, Atlas and Club Mariout. The varietal make-up of the mixture was determined each year and a partial tabulation of the results follows : Percentage of the population made up of: Year Vaughan Hero Atlas Club Mariout o _ , Oo4 Oo7 88.O IO.5 Thus natural selection, in a 16 year period had practically eliminated the types having the highest yields under pure stand conditions of culture. The variety which ultimately dominated had the poorest leaf disease record and a mean yield below the median for the component varieties. Other sets of comparisons possibly have a more direct bearing on the situation in poultry New mixtures were prepared each year so any advantages arising from competition are not cumulative. The data given below are taken from Zavitz (22)_
11 Combination Average yield in pounds per acre Grown Grown in singly combination Oats and barley ,261 Oats, barley and peas ,101 Oats, barley and wheat ,067 Oats and peas ,988 Oats and wheat ,921 Barley and wheat ,558 Peas and wheat ,322 Only one generalization based on these and similar data involving mixture appears permissable: that competition is a function of the genotypes involved and each new assemblage of genotypes may lead to a different ne t pr oduc t.
12 BIBLIOGRAPHY 1. Comstcck, R o E., and Robinson, H. F The components of genetic variance in populations of biparental progenies and their use in estimating the average degree of dominance. Biometrics 4: ,, and Harvey, P. H A breeding procedure designed to make maximum use of both general specific combining ability, Agrono Jouro 41: and 3. j and Experiments for estimation of the average degree of dominance of genes affecting quantitative traits Heterosis, lowa State College Press, Ames, Iowa. 4. Eberhart, S. A., Moll, R. H. and Robinson, H. F Estimates of epistatic and other genetic variances in maize. Agron. Abstr. Amer. Soc. 5. Gamble, E. E. 1962o Gene effects in corn (Zea mays L.). I. Separation and relative importance of gene effects for yield. Canad.,our. Plant Science 42: , Gene effects in Corn (Zea mays L.). II. Relative importance of gene effects for plant height and certain component attributes of yields. Canad.,our. Plant Sci. 42: Gardner, C. 0., Harvey, P. H., Comstock, R. E. and Robinson, H. F. 1953o Dominance of genes controlling quantitative characters in maize. Agron._,our. 45: , and Lonnquist, J.H Linkage and the degree of dominance of genes controlling quantitative characters in maize. Agron.,ouro 51: o _ An evaluation of effects of mass selection snd seed irradiation with thermal neutrons on yield of corn Crop Science 1: lo. Homer, T. W., Comstock, R. E., and Robinson, H. F Non-allelic gene interactions and the interpretation of quantitative genetic data. North Carolina Agr. Expt. Sta. Tech. Bul. ll8. ll. Johnson, E. C Effects of mass selection for yield in a tropical corn variety. Amer. J Soc. Agron. Abstracts, p. 82
13 12. Laug, E. Ro Selection reversal in strains of corn previously long-term selected for chemical composition Crop Sci. 2: Moll, R. H_, Lindsey, M. F. and Robinson, H. F Estimates of genetic variances and level of dominance in maize. Genetics 49: o 14. Robinson, H. F., Comstock, Ro E_ and Harvey_ P. H. 1949o Estimates of heritability and degree of dominance in corn. Agron. Jour. 41: o Robinson, H. F o, Comstock, Rc E. and Harvey, P. H Analysis of genetic variability in corn with reference to probable effects of selection. Cold Spring Harbor Symposia on Quant. Biol. 20: Sakai, Ken-lchi. 1955, " Competition in plants and its relation to selection. Cold Spring Harbor Symposia on Quantitative Biology 20: Sprague, G. Fo, Russell, Wo A_, Penny, L. H., Hornet, T.W. and Hanson, W. D. 1959o Effect of epistasis on grain yield in maize. Crop Science 2: Sprague, G. F., Russell, W. k. and Penny, L. H Recurrent selection for specific combining ability and type of gene action involved in yield heterosis in corn. Agron. Jour. 51: Schwartz, Drew Genetic studies on mutant enzymes in maize: Synthesis of hybrid enzymes by heterozygotes. PNAS 46: Suneson, C.A Survival of four barley varieties in a mixture. Agron. Jour. 41: Woodworth, C. Mo, Leng, E. R. and Jugenheimer, R. W Fiftygenerations of selection for protein and oil in corn. Agron. Jour. 44: Zavitz, Co A o Forty years experiments with grain. Ontario Agr. College Bul \ ) i J /
14 - 8? - Dro G. F. Sprague "SYNTHESIS AND DISCUSSION" W. E. BRILES: Of the some thirty mutants you tested for overdominance, only one exhibited overdominance. _ould you describe the particular nature of the mutant? SPRAGUE: This one case involved a virescent seedling. Other virescents tested did not exhibit overdominance so virescent seedling types in general are not implicated This one virescent type will be studied further obtaining information on plant size, leaf area, ear length and weight, etc., to try and find some explanation for the observed heterosis. At the moment, however, such information is not available. M. L. HOGSETT: Regarding your mutogenic technique, did you say that out of 30 mutant genes studied one was overdominant and two expressed negative dominance? SPRAGUE: There were some cases of partial dominance, where the heterozygote was inferior to the homozygous dominant. Many of the mutants studied could not express negative dominance as the mutant type was lethal. L. H. BAKER: Did the Nebraska group select for more than one trait in their mass selection experiments? SPRAGUE: In their initial experiments, yield only. In their selection for yield, one of the ways in which the population changed rather rapidly was from a primarily single-eared the selection was not for number condition to a two-eared condition, but of ears but rather for total grain yield per plant.
15 88 - L. H. BAKER: Has there been any attempt to select for several traits at one time using mass selection? SPRAGUE: I don't know of any such work under way at the present time. DR. CROW: This is a comment rather than a question but I think it is in order I have been interested in the kind of experiment that Comstock, Robinson, and Gardner and the others are doing that you have been talking about rand I have been interested for some time whether this decrease as you go from F1 to F13, presumably through the breaking up of specific combinations, demands that the genes that are interacting be more closely linked than if they were randomly dispersed along the chromosome. During the past year we have tried two or three different methods. Using the simplest model_ just assuming that the genes are randomly distributed along the chromosome.and assuming a standard interference function, it turns out it doesn,t make very much difference what formula you use. The predictions are roughly in accordance with what Gardner has found. I haventt seen the particular set of data that you are looking at, but I think he is taking it purely at face value It is not necessary to assume that the particular link combinations are especially close_ I think perhaps just random dispersion along the chromosome is pretty satisfactory -- for these results. J. L. LUSH: I would like to make another comment along that very line. This Z-coefficient they get assumes independence between the degree iof dominance and the size of the effect_ whereas there is every theoretical reason to think that ccrrelation is negative_ that is,_your high degree of _i _ overdominance couldn,t occur when the two homozygot_s are far apart but
16 could occur when they are very close together. If that is right, I think the numerator of the coefficient that they call A has a lot of negative component in it. I believe it doesn't beginto tell how much overdominance there is. That's theoretical but it ought to be brought out here before too much is said about this _-coefficient. SPRAGUE: I would not care to comment on that The Nebraska and the North Carolina experimants involved different populations and the results from each exhibit the same general pattern. The estimate of _ decreased with generations of sib-pollination. DR. LUSH: This might _ean the same bias. DR. SPRAGUE: Yes, if any bias were involved it might obtain equally in the two cases.
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