The Evolution of Genetic Systems
C. D. Darlington, 1958

Sterility: The Contradiction

i. Sterility of Crossing

Zygotes which reach maturity must inherently have arisen from the fusion of viable gametes which have given viable products. The problem of sterility is how such a zygote can itself produce gametes, or its gametes produce zygotes, that are not viable; in other words how it can form gametes unlike those from which it is derived. It may do so under three kinds of conditions. First, an unfavourable environment may prevent development taking the same course as it has taken in the past. Secondly, differentiation may fail to provide uniform conditions of reproduction. A production of an excessive number of egg cells, or of unfavourably placed egg cells, where the young offspring are nursed by the female parent, may result in the destruction of some. All other instances of failure of development of gametes and zygotes fall into the third class. They are due to genetic variation.

Genetic sterility is in the simplest case relational. It arises from crossing dissimilar forms. The parents may fail to copulate in species crosses of animals. The pollen may fail to germinate on the style or grow down it in cross-fertilisation between races or species. The same is true mutatis mutandis in animals. These obstacles to fertilisation are physiologically similar to those producing self-sterility in hermaphrodite plants and animals, where as we saw they are due to lack of genetic differences. A specific gene mutation is known in Zea mays to cause cross-sterility.1 Or again the new zygote produced may fail to develop beyond an early stage, either in the simplest case owing to its new and untried genetic constitution being unsatisfactory or, in the mammals, owing to the relationship of embryo to mother being unsatisfactory. In the higher plants the endosperm also plays a part. This can be most simply shown in the occurrence of differences between reciprocal crosses of diploid and polyploid plants.

For example in crosses between diploid and tetraploid forms the normal products of reduction and fertilisation are evidently at a disadvantage in many species for a majority of the progeny are the results of aberrant processes of which we should not have evidence in normal breeding. Equally in Primula sinensis and Campanula persicifolia we find a discrimination against triploid progeny as follows:

Primula Campanula
fertility progeny fertility progeny
2X x 4X nil - 0.1% 4X and 3X
4X x 2X 0.1% 3X and 4X 0.3% 3X, 4X and 2X

The non-triploid progeny are of two kinds. They are either diploids arising from a lack of fertilisation of the eggs of the tetraploid parent. Or they are tetraploids arising from a lack of reduction of the pollen or eggs of the diploid parent.

These abnormalities are uncommon; hence the relative sterility of the crosses. The same principles hold for crosses between diploid and polyploid species.2

Each of these types of sterility involves physiological problems peculiar to the particular case. The effect of all of them is to restrict the size of the breeding group by genetic isolation, and they act as a direct limitation, as we shall see, on all the other types of sterility.

ii. Sterility of the Individual

Two other kinds of genetic sterility may be described in more general terms. They are properties of the individual irrespective of cross- or self-fertilisation. One is genotypic sterility and is due to the organism being different from its parent or parents in having some abnormality of its reproductive processes determined by its individual genotype. Such sterility may take effect (equally in maize or Drosophila) at any stage of development. It arises earliest by the abortion of the sexual organs, later by the suppression of chromosome pairing at meiosis through lack of precocity and last of all by a failure in the development of the germ cells which have been satisfactorily formed.

These genotypic properties may appear as a result of inbreeding or of crossing between two races or species. Usually in either case they affect one sex alone. And usually in plants the anthers are more susceptible to abortion than the ovules, but in Zea mays and Rubus idaeus mutations are known affecting each separately. Such mutations may be used as we saw in establishing sexual differentiation. In animal crosses where the sexes are separated on different individuals it is usually the hybrid sex which is sterilised in this way.3 The reason for this is fairly clear. The XX sex has one X and one set of autosomes from each parent, the XY or XO has no X from one parent and the Y being largely inert does not take its place. The hybrid sex is as we may say unbalanced. The result is that in crosses between species in Drosophila the pairing of the chromosomes is suppressed at meiosis in the male and the testes are underdeveloped. In the female however the chromosomes pair and the eggs are fertile if back-crossed to one of the parents. Some of the males in this back-crossed generation are fertile. They no longer have the wrong combination of X and autosome genes.4

The other kind of individual sterility, and the one which we are in a position to analyse most exhaustively, is due to a lack of uniformity in the products of segregation. This lack of uniformity we may describe as due to the formation by a zygote of gametes genetically different from those which gave rise to it. But what is more to the point is that it depends on the zygote having arisen from the fusion of genetically differing gametes; that is to its being a hybrid, and a hybrid which undergoes crossing-over and segregation at meiosis so as to produce new combinations of genes in a gametic set of chromosomes.

The failure of fertility that we get from these recombinations expected at meiosis in hybrids we may describe as segregational sterility. We may consider it in relation to the three kinds of hybrids in which it occurs, gene hybrids, structural hybrids and numerical hybrids, using at the same time the special behavior of tetraploids of hybrid and non-hybrid origin as a test of our conclusions.

iii. Sterility and Balance

We may see the effect of segregation on sterility most simply in a triploid plant. Spores are formed with all numbers of chromosomes between the haploid and the diploid. Those with intermediate numbers are unbalanced. They develop on the female side to produce egg cells. On the male side however, on account of the longer life of the spore, a proportion usually die before the pollen grain germinates. When they survive the balanced and unbalanced grains have to compete in growing down the style; only a small proportion succeed in fertilising the egg cells and these are likely to be the balanced ones. When a triploid is crossed as a female with a diploid as a male, the result is therefore a higher proportion of unbalanced progeny than in the reciprocal cross. This is notwithstanding a certain differential mortality among the young embryos which also reduces the proportion of unbalanced ones. When the triploid is the male parent very few progeny except diploids and simple trisomics are usually produced.

Sterility of a triploid is thus due to unbalance in the progeny. Now there are occasional plant species which do not show any serious effect of unbalance. This is sometimes due to the basic set being itself polyploid in origin, and sometimes to there being so much translocation and duplication of segments of chromosomes that a mechanical diploid is physiologically a polyploid. This is evidently true of Hyacinthus orientalis, n=8, for in this species different plants with all chromosome numbers from 16 to 32 are equally vigorous. In keeping with this lack of depression from unbalance, they are also almost equally fertile: how fertile exactly we still need to know. It is also in keeping with this situation that vigorous diploid plants deficient of chromosome segments have been found both in cultivation and in wild populations.

How are we to describe the Hyacinthus situation? There are various ways of representing it. But for the present the easiest is no doubt to say that each chromosome is nearly self sufficient. Each chromosome has its own balance. Differentiation there must be; but it is as much within as between chromosomes.5

Absolute deficiency is, in the normal situation, an even more serious cause of sterility than unbalance. Rhoeo discolor having a ring of twelve chromosomes can produce, through errors in the orientation of the ring, pollen grains with five and seven chromosomes instead of six. Those with five never reach the first mitosis. Those with seven may germinate and they may perhaps grow down the style. They never give rise to offspring. Or so it seems for the seedlings all have the same uniform number and appearance as the parent.

These examples show us why a hybrid like Raphanus-Brassica is sterile. Owing to lack of pairing, pollen grains and embryo-sacs are produced with all numbers and combinations of chromosomes; none of the parental types are reproduced except by a rare chance, and a balanced combination will arise only by complete non-reduction; that is by omission of one of the two sexual processes.

In an entirely opposite way, as we saw, following complete pairing and crossing-over in every chromosome of the diploid Primula kewensis the original parental combinations are even less likely to be produced. In consequence likewise the hybrid is absolutely sterile. In the tetraploid through pairing and segregation of similar chromosomes, uniform and balanced gametes are produced and the plant is fertile.

Fig. 28 Diagram showing the alternative conditions of segregational sterility. (a) in a hybrid diploid, (b) in a non-hybrid tetraploid. After Darlington, 1932a
The position of an autotetraploid is significantly different. Its chromosomes, as a rule, change partners at pachytene and, forming chiasmata in these different associations, they remain quadrivalents at metaphase. These quadrivalents are, except perhaps under very special conditions, incapable of regular orientation and segregation in every cell. With linear orientation three-and-one segregation often results. In this way a tetraploid cherry with eight potential quadrivalents has given a segregation of 19 : 13 instead of 16 : 16. With indifferent diamond-shaped co-orientation of the four chromosomes two may be left on the plate at anaphase to divide as univalents. Moreover, trivalents and true univalents often occur (Fig. 28). Thus there is irregularity of segregation in the autotetraploid and infertility is the result.

iv. Selection for Fertility There are two kinds of exceptional circumstance under which these rules do not hold. The first is that of the undifferentiated chromosome complement, as in Hyacinthus, where tetraploidy and even triploidy fail to destroy fertility. The second is that revealed by comparison of a number of species of Tulipa which are evidently autotetraploids. These vary in the number of quadrivalents they form at meiosis subject to two conditions: the numbers of changes of partner at pachytene and the frequency of chiasmata. Since the frequency of chiasmata per chromosome is always reduced in a tetraploid owing to the larger nucleus and the slower pairing some tetraploids such as T. chrysantha have hardly more than the minimum of one chiasma per bivalent. Quadrivalents are therefore almost entirely excluded.6 Thus, if sexual fertility is important for a new tetraploid, selection in meiotic behavious should readily improve it. Experiments with tetraploid rye have shown what can be done. In the course of four years selection for fertility improvements have been made in the proportion of good seed set and in the proportion of this seed which had the balanced tetraploid number and therefore gave good plants. Moreover this improvement was correlated with a reduction of laggards and of unequal segregation at meiosis in the pollen mother cells.7 Rye is an outbreeding plant. In rice, an inbreeder, parallel results have been obtained but only where the diploids have been produced by crossing varieties. Inbred diploids give tetraploids in which selection has no effect: there is no variation in the genotypic control of meiosis from which the breeder can select.8 By such processes of selection we may suppose that Dahlia variabilis which seems to have arisen as an autotetraploid garden plant in pre-Columbian Mexico has come to combine regular quadrivalent formation and seed-fertility with free tetraploid segregation.9 The new unselected autotetraploid however always forms univalents. It thus yields unbalanced gametes, and its fertility is reduced. Now here is the contrast and, if you like, the paradox. The fertile diploid gives an infertile autotetraploid. The sterile diploid gives a fertile allotetraploid. There is a negative correlation between the fertility of diploids ant that of the tetraploids they give rise to. Hence autotetraploids in nature do not usually establish themselves as new species unless sexual fertility can be to some extent dispensed with. If we enquire into their occurrence among plants we are at once led to discover how this happens. We find that the autotetraploid forms nearly always arise in individuals or varieties which differ from the average character of the species in having a greater propensity for vegetative reproduction. They are, we may say, pre-adapted to polyploidy. Or, better still perhaps, we may say that polyploidy and vegetative propagation mutually select one another.10

v. The Splitting of Groups Let us return with the knowledge which these principles give us to consider sterility within a natural diploid breeding group of common size and stability. Within such a group cross-fertilisation takes place between pairs of gametes which differ in respect of a varying number of changes in genes and in their arrangement. We find that a proportion of the zygotes produced fail to develop and we can trace this failure to the recombinations that occur at meiosis. Sometimes it is due to crossing-over within inversions giving deficient gametes and zygotes. Sometimes it is due to irregularity in segregation following failure of pairing at meiosis. Sometimes it is due to two chromosomes which are necessary to one another failing to pass to the same gamete. They may be complementary to one another either though one containing a segment of chromosome actually removed from the other (as we see was the case in Oenothera) or they may contain independent mutations which cannot work separately. What happens to a breeding group in which variation increases and fertility consequently decreases? Clearly any change which will reduce the amount of variation in the group will enjoy an increasing advantage. How can this be done? By any means which will split the group into parts; that is any kind of genetic isolation. Any self-fertilising individual, any new polyploid, any asexually propagating type, at once breaks itself off from the main group and escapes from the disadvantages. Any divergence from the normal breeding system will separate the divergent race and split the group. Any structural change which binds together genes in the hybrid will achieve a similar result. For it will limit recombination. It will mitigate segregational sterility. Its effect will also depend on a genetic isolation, but an isolation of chromosome segments, from which an isolation of individuals, a splitting of the group or the species, will only later be derived.

The group breaks into two. Sterility brings its remedy. The new smaller groups have less variation within their limits and are more fertile than the old. But if cross-sterility does not readily develop, if genetic isolation does not crop up, or if sexual reproduction can be to a great extent dispensed with, as in some sections of Rosa and Rubus, a population will arise which will vary between moderate fertility and absolute sterility. In such a population the discontinuity of species may cease to be recognisable.

Sterility is therefore the contradiction inherent in variation and recombination. A stock that is invariable will become pure breeding and completely fertile. Even if it varies, and yet suppresses the recombination of variants that would occur by the crossing of individuals or by the crossing-over and segregation of chromosomes, it will still remain pure-breeding and completely fertile. Sterility is the price the species pays in the death of a part of its immediate progeny for the advantages of recombination and adaptation in its more remote posterity. It may be said that this price is inevitable. That is not true for every group of plants and animals; there are some species which avoid paying it, or postpone paying it, or pay it in a different currency. We will now see how they are able to succeed.