The Different Forms of Flowers on Plants of the Same Species

by Charles Darwin

THE MEANS BY WHICH PLANTS MAY HAVE BEEN RENDERED HETEROSTYLED.

This is a very obscure subject, on which I can throw little light, but which is worthy of discussion. It has been shown that heterostyled plants occur in fourteen natural families, dispersed throughout the whole vegetable kingdom, and that even within the family of the Rubiaceae they are dispersed in eight of the tribes. We may therefore conclude that this structure has been acquired by various plants independently of inheritance from a common progenitor, and that it can be acquired without any great difficulty—that is, without any very unusual combination of circumstances.

It is probable that the first step towards a species becoming heterostyled is great variability in the length of the pistil and stamens, or of the pistil alone. Such variations are not very rare: with Amsinckia spectabilis and Nolana prostrata these organs differ so much in length in different individuals that, until experimenting on them, I thought both species heterostyled. The stigma of Gesneria pendulina sometimes protrudes far beyond, and is sometimes seated beneath the anthers; so it is with Oxalis acetosella and various other plants. I have also noticed an extraordinary amount of difference in the length of the pistil in cultivated varieties of Primula veris and vulgaris.

As most plants are at least occasionally cross-fertilised by the aid of insects, we may assume that this was the case with our supposed varying plant; but that it would have been beneficial to it to have been more regularly cross- fertilised. We should bear in mind how important an advantage it has been proved to be to many plants, though in different degrees and ways, to be cross- fertilised. It might well happen that our supposed species did not vary in function in the right manner, so as to become either dichogamous or completely self-sterile, or in structure so as to ensure cross-fertilisation. If it had thus varied, it would never have been rendered heterostyled, as this state would then have been superfluous. But the parent-species of our several existing heterostyled plants may have been, and probably were (judging from their present constitution) in some degree self-sterile; and this would have made regular cross-fertilisation still more desirable.

Now let us take a highly varying species with most or all of the anthers exserted in some individuals, and in others seated low down in the corolla; with the stigma also varying in position in like manner. Insects which visited such flowers would have different parts of their bodies dusted with pollen, and it would be a mere chance whether this were left on the stigma of the next flower which was visited. If all the anthers could have been placed on the same level in all the plants, then abundant pollen would have adhered to the same part of the body of the insects which frequented the flowers, and would afterwards have been deposited without loss on the stigma, if it likewise stood on the same unvarying level in all the flowers. But as the stamens and pistils are supposed to have already varied much in length and to be still varying, it might well happen that they could be reduced much more easily through natural selection into two sets of different lengths in different individuals, than all to the same length and level in all the individuals. We know from innumerable instances, in which the two sexes and the young of the same species differ, that there is no difficulty in two or more sets of individuals being formed which inherit different characters. In our particular case the law of compensation or balancement (which is admitted by many botanists) would tend to cause the pistil to be reduced in those individuals in which the stamens were greatly developed, and to be increased in length in those which had their stamens but little developed.

Now if in our varying species the longer stamens were to be nearly equalised in length in a considerable body of individuals, with the pistil more or less reduced; and in another body, the shorter stamens to be similarly equalised, with the pistil more or less increased in length, cross-fertilisation would be secured with little loss of pollen; and this change would be so highly beneficial to the species, that there is no difficulty in believing that it could be effected through natural selection. Our plant would then make a close approach in structure to a heterostyled dimorphic species; or to a trimorphic species, if the stamens were reduced to two lengths in the same flower in correspondence with that of the pistils in the other two forms. But we have not as yet even touched on the chief difficulty in understanding how heterostyled species could have originated. A completely self-sterile plant or a dichogamous one can fertilise and be fertilised by any other individual of the same species; whereas the essential character of a heterostyled plant is that an individual of one form cannot fully fertilise or be fertilised by an individual of the same form, but only by one belonging to another form.

H. Muller has suggested that ordinary or homostyled plants may have been rendered heterostyled merely through the effects of habit. (6/5. ‘Die Befruchtung der Blumen’ page 352.) Whenever pollen from one set of anthers is habitually applied to a pistil of particular length in a varying species, he believes that at last the possibility of fertilisation in any other manner will be nearly or completely lost. He was led to this view by observing that Diptera frequently carried pollen from the long-styled flowers of Hottonia to the stigma of the same form, and that this illegitimate union was not nearly so sterile as the corresponding union in other heterostyled species. But this conclusion is directly opposed by some other cases, for instance by that of Linum grandiflorum; for here the long-styled form is utterly barren with its own-form pollen, although from the position of the anthers this pollen is invariably applied to the stigma. It is obvious that with heterostyled dimorphic plants the two female and the two male organs differ in power; for if the same kind of pollen be placed on the stigmas of the two forms, and again if the two kinds of pollen be placed on the stigmas of the same form, the results are in each case widely different. Nor can we see how this differentiation of the two female and two male organs could have been effected merely through each kind of pollen being habitually placed on one of the two stigmas.

Another view seems at first sight probable, namely, that an incapacity to be fertilised in certain ways has been specially acquired by heterostyled plants. We may suppose that our varying species was somewhat sterile (as is often the case) with pollen from its own stamens, whether these were long or short; and that such sterility was transferred to all the individuals with pistils and stamens of the same length, so that these became incapable of intercrossing freely; but that such sterility was eliminated in the case of the individuals which differed in the length of their pistils and stamens. It is, however, incredible that so peculiar a form of mutual infertility should have been specially acquired unless it were highly beneficial to the species; and although it may be beneficial to an individual plant to be sterile with its own pollen, cross-fertilisation being thus ensured, how can it be any advantage to a plant to be sterile with half its brethren, that is, with all the individuals belonging to the same form? Moreover, if the sterility of the unions between plants of the same form had been a special acquirement, we might have expected that the long-styled form fertilised by the long-styled would have been sterile in the same degree as the short-styled fertilised by the short-styled; but this is hardly ever the case. On the contrary, there is sometimes the widest difference in this respect, as between the two illegitimate unions of Pulmonaria angustifolia and of Hottonia palustris.

It is a more probable view that the male and female organs in two sets of individuals have been by some means specially adapted for reciprocal action; and that the sterility between the individuals of the same set or form is an incidental and purposeless result. The meaning of the term “incidental” may be illustrated by the greater or less difficulty in grafting or budding together two plants belonging to distinct species; for as this capacity is quite immaterial to the welfare of either, it cannot have been specially acquired, and must be the incidental result of differences in their vegetative systems. But how the sexual elements of heterostyled plants came to differ from what they were whilst the species was homostyled, and how they became co-adapted in two sets of individuals, are very obscure points. We know that in the two forms of our existing heterostyled plants the pistil always differs, and the stamens generally differ in length; so does the stigma in structure, the anthers in size, and the pollen-grains in diameter. It appears, therefore, at first sight probable that organs which differ in such important respects could act on one another only in some manner for which they had been specially adapted. The probability of this view is supported by the curious rule that the greater the difference in length between the pistils and stamens of the trimorphic species of Lythrum and Oxalis, the products of which are united for reproduction, by so much the greater is the infertility of the union. The same rule applies to the two illegitimate unions of some dimorphic species, namely, Primula vulgaris and Pulmonaria angustifolia; but it entirely fails in other cases, as with Hottonia palustris and Linum grandiflorum. We shall, however, best perceive the difficulty of understanding the nature and origin of the co-adaptation between the reproductive organs of the two forms of heterostyled plants, by considering the case of Linum grandiflorum: the two forms of this plant differ exclusively, as far as we can see, in the length of their pistils; in the long-styled form, the stamens equal the pistil in length, but their pollen has no more effect on it than so much inorganic dust; whilst this pollen fully fertilises the short pistil of the other form. Now, it is scarcely credible that a mere difference in the length of the pistil can make a wide difference in its capacity for being fertilised. We can believe this the less because with some plants, for instance, Amsinckia spectabilis, the pistil varies greatly in length without affecting the fertility of the individuals which are intercrossed. So again I observed that the same plants of Primula veris and vulgaris differed to an extraordinary degree in the length of their pistils during successive seasons; nevertheless they yielded during these seasons exactly the same average number of seeds when left to fertilise themselves spontaneously under a net.

We must therefore look to the appearance of inner or hidden constitutional differences between the individuals of a varying species, of such a nature that the male element of one set is enabled to act efficiently only on the female element of another set. We need not doubt about the possibility of variations in the constitution of the reproductive system of a plant, for we know that some species vary so as to be completely self-sterile or completely self-fertile, either in an apparently spontaneous manner or from slightly changed conditions of life. Gartner also has shown that the individual plants of the same species vary in their sexual powers in such a manner that one will unite with a distinct species much more readily than another. (6/6. Gartner ‘Bastarderzeugung im Pflanzenreich’ 1849 page 165.) But what the nature of the inner constitutional differences may be between the sets or forms of the same varying species, or between distinct species, is quite unknown. It seems therefore probable that the species which have become heterostyled at first varied so that two or three sets of individuals were formed differing in the length of their pistils and stamens and in other co-adapted characters, and that almost simultaneously their reproductive powers became modified in such a manner that the sexual elements in one set were adapted to act on the sexual elements of another set; and consequently that these elements in the same set or form incidentally became ill-adapted for mutual interaction, as in the case of distinct species. I have elsewhere shown that the sterility of species when first crossed and of their hybrid offspring must also be looked at as merely an incidental result, following from the special co-adaptation of the sexual elements of the same species. (6/7. ‘Origin of Species’ 6th edition page 247; ‘Variation of Animals and Plants under Domestication’ 2nd edition volume 2 page 169; ‘The Effects of Cross and Self-fertilisation’ page 463. It may be well here to remark that, judging from the remarkable power with which abruptly changed conditions of life act on the reproductive system of most organisms, it is probable that the close adaptation of the male to the female elements in the two forms of the same heterostyled species, or in all the individuals of the same ordinary species, could be acquired only under long-continued nearly uniform conditions of life.) We can thus understand the striking parallelism, which has been shown to exist between the effects of illegitimately uniting heterostyled plants and of crossing distinct species. The great difference in the degree of sterility between the various heterostyled species when illegitimately fertilised, and between the two forms of the same species when similarly fertilised, harmonises well with the view that the result is an incidental one which follows from changes gradually effected in their reproductive systems, in order that the sexual elements of the distinct forms should act perfectly on one another.