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The Balance Between Coherence and Variation in Evolution by Jens Clausen and Wm

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The Balance Between Coherence and Variation in Evolution by Jens Clausen and Wm 494 BOTANY: CLAUSEN AND HIESEY PROC. N. A. S. to fresh medium, especially when small inocula are involved. increased formation of acetylorni- thine permease appears to take place (Vogel, H. J., unpublished data). 23 Magasanik, B., A. K. Magasanik, and F. C. Neidhardt, in Regulation of Cell Metabolism, ed. G. E. W. Wolstenholme and C. M. O'Connor (Boston: Little, Brown and Company, 1959), p. 334. THE BALANCE BETWEEN COHERENCE AND VARIATION IN EVOLUTION BY JENS CLAUSEN AND WM. M. HIESEY DEPARTMENT OF PLANT BIOLOGY, CARNEGIE INSTITUTION OF WASHINGTON, STANFORD, CALIFORNIA Read before the Academy, November 18, 1969 What are the mechanisms that cause living things to differentiate into recogniz- able species and subspecific entities rather than to evolve into a flow of continuous variation? This age-old question has puzzled evolutionists, and no adequate answer has been demonstrated. One of the reasons for our highly fragmentary understanding of evolutionary processes is that only scant information has been available about mechanisms governing variation in truly wild organisms. A recently concluded analysis of 20-year experiments on the hereditary mecha- nisms that separate ecological races of wild plants of western North America shows that coherence is as much a part of evolution as is variation. Even characters of evolutionary entities below the level of the species are held together by coherence mechanisms that are balanced against others producing variation. The fact that the forces of coherence are as integral a part of evolutionary mechanisms as are the forces of variation makes the process of speciation comprehensible. Studies on the mechanisms of inheritance in wild organisms have hitherto largely been avoided because their inheritance has been known to be relatively complex. For experimental purposes, organisms that have evolved within the protective environment created by human civilization have been selected because they fre- quently differ in rather spectacular characters whose modes of inheritance are simpler to study. Emphasis has also been placed on the effects of individual genes as they relate to the inheritance of one or a few traits, and on the effects of mutant genes having conspicuous effects, rather than on their wild-type alleles having many small but cumulative effects. Natural selection tends to discard the average mutant and does not directly operate on single genes, but rather upon combinations of characters regulated by constellations of genes. Races of wild plants are products of natural selection acting through geologic periods of time. They are adjusted to living in arrays of distinct environments and differ by many traits, both morphological and physiolog- ical. GENETIC STRUCTURE OF WILD RACES In an attempt to fill some of the gaps in our knowledge concerning mechanisms of natural evolution, our group has undertaken to analyze the hereditary structure Downloaded by guest on September 28, 2021 VOL. 46, 1960 BOTANY: CLAUSEN AND HIESEY 495 of ecological races of selected species of wild plants. Some of these are on record ,9"' 13-16. 20-22 and others are still unpublished. These investigations have shown that nearly every character distinguishing one ecological race from another is controlled by a small system of genes. The com- bined effects of all the genes of such a system can be easily noticed, but each com- ponent gene induces much less effect than genes commonly- studied in the laboratory as mutants. The physiological effects of genes in wild races tend to counterbalance each other so that their expression is buffered. About 35 years ago Erwin Baur2 3 demonstrated that in crossings between wild and cultivated snapdragons (Antir- rhinum), segregation for many small differences occurred, but no actual genetic analysis was then attempted. The Coherence Mechanism.-The basic mechanism by which coherence is achieved is provided through the chromosomes. The several genes that regulate the pheno- typic expression of a character, such as petal shape or anthocyanin coloration of stems and leaves, are usually located on separate chromosomes, but each chromo- some carries genes that contribute to the control of many other characters as well. Some of the genes that regulate two distinct characters may thus be linked, whereas other genes governing these characters recombine freely. The hereditary mecha- nism that regulates the phenotypic expression of the characters operates, therefore, like a loose, partly disengaging network. If natural selection favors a particular trait of an organism, its effect is transmitted to the progeny through the chromo- somes that carry the genes controlling that trait, and through these it will also be partially-linked with several other distinct characters regulated by genes carried by the same chromosomes. Potentials of Variation.-Natural races carry much greater potentials of vari- ability than has previously been assumed. Crossings between wild races greatly increase the expression of variability. Epistatic (covering) effects of certain genes are frequent; likewise, genes of separate races may complement each other so that much hitherto unexpressed variability becomes released and subject to selection. Genes having additive, subtractive, and complementary effects on a character are frequently carried by separate races of the species and cause transgressive segre- gations in interracial crosses. In the case of physiological differences, such segre- gations may far exceed the limits found in the parental races. Number of Genes per Character.-From evidence thus far obtained, each morpho- logical difference has been found to be regulated by a system composed of a rela- tively small number of genes. In Potentilla and the Madiinae of western North America, the parental expressions of segregating individual characters have been approached, attained, or exceeded in F2 populations consisting of 500 to 1,000 individuals under circumstances suggesting that systems on the order of three to six pairs of genes govern such characters."' 1' These findings are supported by other data previously obtained in diallel intercrossings between forms of the two wild pansy species of northwestern Europe, Viola tricolor and V. arvensis.6-8 15 The highly variable floral colors of wild pansies can be accounted for by assuming interactions between 11 pairs of genes, three of which also concern the development of anthocyanin in stems and leaves. The occurrence of an inconspicuous honey spot on the front of the pistil is regulated by the complementary and oppositional interactions of four pairs of genes. Downloaded by guest on September 28, 2021 496 BOTANY: CLAUSEN AND HIESEY PROC. N. A. S. The genetic regulation of certain physiological characters, such as date of flower- ing in Potentilla, is more complex, however; the F2 segregation with regard to this trait greatly exceeded the limits of the parents. Considering the dates of flowering of the cloned F2 individuals in three contrasting environments, it was estimated that a minimum of 20 pairs of genes regulate this character in the interracial crosses. In contrast, other physiological characters, such as winter-dormancy and frost re- sistance, appeared to be governed by three or four pairs of genes. Combining data from crosses between several agricultural races of barley (Hor- deum), Wexelsen32 33 found that 6 pairs of genes, having somewhat unequal effects, control the length of the internodes between spikelets of the ear. His conclusions were based on detailed genetic analyses of segregating F2's, F3's, and F4's resulting from selfing, and were supported by the fact that two of the multiple genes were linked with two groups of genes governing other morphological characters located on separate chromosomes. The estimates above refer to the minimal number of gene differences in organisms where it has been possible to conduct a careful and fairly representative analysis of interracial crosses. These estimates are far below the 100 to 200 genes per character that were suggested by J. Rasmusson28 without substantiating data, but have been repeatedly quoted.1 26 The high estimates were based on statistical deductions rather than directly on observed segregations, and they assumed small, linearly ad- ditive differences. A moderate number of gene differences can, however, produce great diversity in segregation when the system contains complementary and op- positional genes, or when both parents carry a different set of genes having additive or subtractive effects. Correlation in Inheritance.-Only few studies on correlations between segre- gating characters are on record, although there are many on linkages between individual genes. The calculation of correlation becomes a major operation when many segregating characters within a species are studied. The extensive study of correlations in progenies of interracial Potentilla hybrids16 were facilitated through the use of punched card techniques. Supporting evidence on correlations between characters is available from inter- racial hybrids within Layia and Madia;9' 14, 15 and from subspecific hybrids of the Solidago sempervirens complex,4 and Gilia capitata.19 It was also reported in the subspecific hybrid of the lowland Antirrhinum majus X alpine A. molle.3 Strong correlations were observed between 8 segregating characters in a cross between two agricultural races of barley, one race developed in California and the other in Sweden.32' 33 The segregations of 5 of these characters were widely trans- gressive.
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