Elements of Genetics pp. 246-248 (1950)
Darlington and Mathers


With suitable breeding experiments the linkage of this gene, S, as it is called, with other genes can be established and its mutations recorded. Of course in a fully operative system the number of allelomorphs of the S gene can never be less then three and is always in fact much more numerous. In the small species Oenothera organensis, with a total wild population of perhaps no more than 500 plants, 35 allelomorphs have been identified. In the larger species of Red Clover, Trifolium pratense, one group of 24 plants had 41 different allelomorphs and another group of 20 plants had 37 allelomorphs. And, although closely related, the 60 cultivated varieties of Sweet Cherry examined must have over 20 allelomorphs.

The S gene tells us many things of importance. Its large number of allelomorphs is without parallel. The specificity of their action in the style is nearly always complete, since Sx pollen fails on a style carrying Sx no matter what the other allelomorph may be. In some cases this specificity extends to the strength of action, for some allelomorphs are stronger than others whatever others are present, though in other cases the allelomorphs can strengthen one another's action. Moreover the properties of the pollen itself are determined by the single allelomorph carried in its own nuclei after segregation: there is no delayed effect from the other allelomorph present in its diploid parent (and in its sister pollen). The rapid and specific action puts one in mind of the relation between gene and antigen in the determination of blood groups. The analogy is still more evident from the effect of a rise of temperature which, so Lewis found, speeds up the growth of compatible pollen, yet slows down the growth of the incompatible. Incompatibility is thus due to a positive blocking reaction.

pp. 255-256

Ordinary incompatibility is controlled in the same way: it has the same genetic structure as heterostyly. For example, Petunia violacea has the usual multiple allelomorph system of pollen-style relationships: self-pollination rarely succeeds. P. axillaris, on the other hand, shows no trace of incompatibility: selfing and crossing succeed equally well. In the F1 different S allelomorphs from violacea vary in effectiveness and plants differ in the degree of self-compatibility. By crossing together F1 plants with different S allelomorphs, or by backcrossing them to their violacea parent, we can get plants with the same S constitution as violacea but with other genes, half in the F2 and a quarter, or nearly a quarter, in the backcross, from axillaris. Although alike in regard to S these three types of plants show incompatibility relations differing in two ways (Fig. 64).

First, the amount of seed set on self-fertilization increases with the proportion of axillaris genes. These genes must therefore be undermining the operation which the S genes control.

Secondly, the amount of seed set on pollination of backcross or F2 plants by violacea is greater than any produced by self-pollination, although the same S genes are at work. Thus the axillaris genes not merely weaken the operation of the S genes; they shift their operation so as to put it out of step in plants with differ proportions of axillaris genes. Or, the other way round, we may the same S genes can not merely control systems of different strengths, but systems which are less efficient with one another than each is within itself.

Now, we may ask, what happens when we cross two self-incompatible species, each with the S genes? This has been done for Nicotiana alata and N. forgetiana in the production of the garden form N. sanderae. Pseudo-compatibility, that is successful fertilization with pollen having an S allelemorph the same as in the style and therefore not legitimately capable of growth, is unknown in forgetiana. It occurs only rarely in alata. In their derivative it is common, especially with certain of the weaker allelemorphs. Thus the recombination between the general gene systems of two species has robbed each of its efficiency as a basis for the action of the S series.

FIG. 64.—Breakdown of the genetic determination of incompatibility in Petunia. P. violacea plants of the constitution S1S2 set seed from only about 1 per cent of flowers which have been self-fertilized (indicated by size of black square relative to the white one containing it). S1S2 plants recovered in the F2 of the cross with the self-compatible P. axillaris set seed from about 25 per cent of flowers after self-pollination and S1S2 plants recovered in the backcross to P. violacea are intermediate in behaviour. Thus the addition of genes from P. axillaris causes progressive breakdown of the incompatibility mechanism of P. violacea. It also causes some change in the operation of the mechanism which is left, as pollination of the backcross or F2 plants by P. violacea gives a greater set of seed than does selfing, with which the cross is identical in respect of S1 and S2 (based on Mather, 1943).

pp. 258-260

In genetic terms, breeding systems are now secn to be of two types. First, all those giving inbreeding and some giving outbreeding, like protandry and cyclical hermaphroditism, are controlled by general gene systems which do not show any special variation within the species. Their operation does not depend on diversity, that is on segregation. Secondly, the chief cross-breeding systems, sex and incompatibility, on the other hand, require segregation and therefore depend on the action of switch genes. But the existence of the mechanism which these genes switch, depends on a general gene system which does not need to show segregation.

On this basis new systems can come into existence by adjustment, through selection, of the general gene system; the switch gene, where it exists, is thereby given a progressively stronger effect. The evidence that this is at least sometimes the case arises from the method of breakdown seen already in Primula sinensis. Sudden breakdown can, of course, occur in the switch gene itself. Various species of Primula, such as the common primrose, sometimes have the pin-thrum type replaced, in nature, by a homostyle type with anthers and stigma at the same level. This change was found by Ernst in one case to be due to a change of the switch gene to a third allelomorph. The new type most inbreed with a regularity which is equal to the outbreeding of its predecessor, because, of course, the genetic background remains the same. Similarly, in ordinary incompatibility, the usual S allelomorphs can be replaced by a so-called fertility allelomorph, Sf, which no longer inhibits self-pollination or even any kind of cross-pollination.

Most fertility allelomorphs have been found in self-compatible species related to other species which are uniformly self-incompatible. But mutations to Sf have appeared in the otherwise regularly incompatible red clover. Moreover, in Anthrrhinum majus, but nowhere else so far as is known, a fertility gene exists, overriding the S system, but not allelomorphic to it. These various eases of breakdown show that a system which is built up gradually of many elements including an operator, the switch gene, can be knocked down by removing any one of them, especially, of course, by removing the operator.


All these facts and arguments relate to changes in the breeding system at one level, or at one time of operation. But, as we know, control occurs at many levels. How do they interact?

One system can be superimposed on another, while leaving all the evidence of the other plainly revealed to us. We then have a stratified system. For example consider wheat, any species of Triticum. The anthers and stigmata are thrust out into the wind to allow of cross-pollination, or so one would suppose; but in fact the anthers burst and pollinate the stigma inside the flower before it opens. Inbreeding is superimposed on outbreeding: a low hybridity optimum can replace a high one. This sequence of systems is confirmed when we look at a closely related cereal. Rye pushes out its anthers and stigma in just the same way; but instead of vitiating the crossing mechanisms by premature bursting, it reinforces it by incompatibility. Wheat has developed one way and rye the other, after their ancestors diverged. Of peas the same story can be told. To be sure, the cross-pollination was to have been by insects, but its vitiation is still by premature bursting of the anthers. And when we return to the mite Pediculopsis, premature mating is again the means by which outbreeding is suppressed while the sex system adapted to outbreeding is retained.

Outbreeding, so far as we know, never supervenes on inbreeding. Always it is the reverse. Complete inbreeding is evidently a dead end. The reasons for this we shall touch on later. But there are a variety of ways in which the effect of cross-breeding, the high degree of hybridity, may be maintained while the ancient system of crossing is allowed to lapse. One of these we have already seen in the allopolyploid. A second method is that of the truebreeding hybrid or complex heterozygote.