The Different Forms of Flowers on Plants of the Same Species

by Charles Darwin

CHAPTER VII. POLYGAMOUS, DIOECIOUS, AND GYNO-DIOECIOUS PLANTS.

The conversion in various ways of hermaphrodite into dioecious plants.
Heterostyled plants rendered dioecious.
Rubiaceae.
Verbenaceae.
Polygamous and sub-dioecious plants.
Euonymus.
Fragaria.
The two sub-forms of both sexes of Rhamnus and Epigaea.
Ilex.
Gyno-dioecious plants.
Thymus, difference in fertility of the hermaphrodite and female individuals.
Satureia.
Manner in which the two forms probably originated.
Scabiosa and other gyno-dioecious plants.
Difference in the size of the corolla in the forms of polygamous, dioecious, and
gyno-dioecious plants.

There are several groups of plants in which all the species are dioecious, and these exhibit no rudiments in the one sex of the organs proper to the other. About the origin of such plants nothing is known. It is possible that they may be descended from ancient lowly organised forms, which had from the first their sexes separated; so that they have never existed as hermaphrodites. There are, however, many other groups of species and single ones, which from being allied on all sides to hermaphrodites, and from exhibiting in the female flowers plain rudiments of male organs, and conversely in the male flowers rudiments of female organs, we may feel sure are descended from plants which formerly had the two sexes combined in the same flower. It is a curious and obscure problem how and why such hermaphrodites have been rendered bisexual.

If in some individuals of a species the stamens alone were to abort, females and hermaphrodites would be left existing, of which many instances occur; and if the female organs of the hermaphrodite were afterwards to abort, the result would be a dioecious plant. Conversely, if we imagine the female organs alone to abort in some individuals, males and hermaphrodites would be left; and the hermaphrodites might afterwards be converted into females.

In other cases, as in that of the common Ash-tree mentioned in the Introduction, the stamens are rudimentary in some individuals, the pistils in others, others again remaining as hermaphrodites. Here the modification of the two sets of organs appears to have occurred simultaneously, as far as we can judge from their equal state of abortion. If the hermaphrodites were supplanted by the individuals having separated sexes, and if these latter were equalised in number, a strictly dioecious species would be formed.

There is much difficulty in understanding why hermaphrodite plants should ever have been rendered dioecious. There would be no such conversion, unless pollen was already carried regularly by insects or by the wind from one individual to the other; for otherwise every step towards dioeciousness would lead towards sterility. As we must assume that cross-fertilisation was assured before an hermaphrodite could be changed into a dioecious plant, we may conclude that the conversion has not been effected for the sake of gaining the great benefits which follow from cross-fertilisation. We can, however, see that if a species were subjected to unfavourable conditions from severe competition with other plants, or from any other cause, the production of the male and female elements and the maturation of the ovules by the same individual, might prove too great a strain on its powers, and the separation of the sexes would then be highly beneficial. This, however, would be effected only under the contingency of a reduced number of seeds, produced by the females alone, being sufficient to keep up the stock.

There is another way of looking at the subject which partially removes a difficulty that appears at first sight insuperable, namely, that during the conversion of an hermaphrodite into a dioecious plant, the male organs must abort in some individuals and the female organs in others. Yet as all are exposed to the same conditions, it might have been expected that those which varied would tend to vary in the same manner. As a general rule only a few individuals of a species vary simultaneously in the same manner; and there is no improbability in the assumption that some few individuals might produce larger seeds than the average, better stocked with nourishment. If the production of such seeds were highly beneficial to a species, and on this head there can be little doubt, the variety with the large seeds would tend to increase. (7/1. See the facts given in ‘The Effects of Cross and Self-fertilisation’ page 353.) But in accordance with the law of compensation we might expect that the individuals which produced such seeds would, if living under severe conditions, tend to produce less and less pollen, so that their anthers would be reduced in size and might ultimately become rudimentary. This view occurred to me owing to a statement by Sir J.E. Smith that there are female and hermaphrodite plants of Serratula tinctoria, and that the seeds of the former are larger than those of the hermaphrodite form. (7/2. ‘Transactions of the Linnean Society’ volume 8 page 600.) It may also be worth while to recall the case of the mid-styled form of Lythrum salicaria, which produces a larger number of seeds than the other forms, and has somewhat smaller pollen-grains which have less fertilising power than those of the corresponding stamens in the other two forms; but whether the larger number of seeds is the indirect cause of the diminished power of the pollen, or vice versa, I know not. As soon as the anthers in a certain number of individuals became reduced in size in the manner just suggested or from any other cause, the other individuals would have to produce a larger supply of pollen; and such increased development would tend to reduce the female organs through the law of compensation, so as ultimately to leave them in a rudimentary condition; and the species would then become dioecious.

Instead of the first change occurring in the female organs we may suppose that the male ones first varied, so that some individuals produced a larger supply of pollen. This would be beneficial under certain circumstances, such as a change in the nature of the insects which visited the flowers, or in their becoming more anemophilous, for such plants require an enormous quantity of pollen. The increased action of the male organs would tend to affect through compensation the female organs of the same flower; and the final result would be that the species would consist of males and hermaphrodites. But it is of no use considering this case and other analogous ones, for, as stated in the Introduction, the coexistence of male and hermaphrodite plants is excessively rare.

It is no valid objection to the foregoing views that changes of such a nature would be effected with extreme slowness, for we shall presently see good reason to believe that various hermaphrodite plants have become or are becoming dioecious by many and excessively small steps. In the case of polygamous species, which exist as males, females and hermaphrodites, the latter would have to be supplanted before the species could become strictly dioecious; but the extinction of the hermaphrodite form would probably not be difficult, as a complete separation of the sexes appears often to be in some way beneficial. The males and females would also have to be equalised in number, or produced in some fitting proportion for the effectual fertilisation of the females.

There are, no doubt, many unknown laws which govern the suppression of the male or female organs in hermaphrodite plants, quite independently of any tendency in them to become monoecious, dioecious, or polygamous. We see this in those hermaphrodites which from the rudiments still present manifestly once possessed more stamens or pistils than they now do,—even twice as many, as a whole verticil has often been suppressed. Robert Brown remarks that “the order of reduction or abortion of the stamina in any natural family may with some confidence be predicted,” by observing in other members of the family, in which their number is complete, the order of the dehiscence of the anthers (7/3. ‘Transactions of the Linnean Society’ volume 12 page 98 or ‘Miscellaneous Works’ volume 2 pages 278-81.); for the lesser permanence of an organ is generally connected with its lesser perfection, and he judges of perfection by priority of development. He also states that whenever there is a separation of the sexes in an hermaphrodite plant, which bears flowers on a simple spike, it is the females which expand first; and this he likewise attributes to the female sex being the more perfect of the two, but why the female should be thus valued he does not explain.

Plants under cultivation or changed conditions of life frequently become sterile; and the male organs are much oftener affected than the female, though the latter alone are sometimes affected. The sterility of the stamens is generally accompanied by a reduction in their size; and we may feel sure, from a wide-spread analogy, that both the male and female organs would become rudimentary in the course of many generations if they failed altogether to perform their proper functions. According to Gartner, if the anthers on a plant are contabescent (and when this occurs it is always at a very early period of growth) the female organs are sometimes precociously developed. (7/4. ‘Beitrage zur Kenntniss’ etc. page 117 et seq. The whole subject of the sterility of plants from various causes has been discussed in my ‘Variation of Animals and Plants under Domestication’ chapter 18 2nd edition volume 2 pages 146-56.) I mention this case as it appears to be one of compensation. So again is the well- known fact, that plants which increase largely by stolons or other such means are often utterly barren, with a large proportion of their pollen-grains in a worthless condition.

Hildebrand has shown that with hermaphrodite plants which are strongly proterandrous, the stamens in the flowers which open first sometimes abort; and this seems to follow from their being useless, as no pistils are then ready to be fertilised. Conversely the pistils in the flowers which open last sometimes abort; as when they are ready for fertilisation all the pollen has been shed. He further shows by means of a series of gradations amongst the Compositae, that a tendency from the causes just specified to produce either male or female florets, sometimes spreads to all the florets on the same head, and sometimes even to the whole plant (7/5. ‘Ueber die Geschlechtsverhaltnisse bei den Compositen’ 1869 page 89.); and in this latter case the species becomes dioecious. In those rare instances mentioned in the Introduction, in which some of the individuals of both monoecious and hermaphrodite plants are proterandrous, others being proterogynous, their conversion into a dioecious condition would probably be much facilitated, as they already consist of two bodies of individuals, differing to a certain extent in their reproductive functions.

Dimorphic heterostyled plants offer still more strongly marked facilities for becoming dioecious; for they likewise consist of two bodies of individuals in approximately equal numbers, and what probably is more important, both the male and female organs differ in the two forms, not only in structure but in function, in nearly the same manner as do the reproductive organs of two distinct species belonging to the same genus. Now if two species are subjected to changed conditions, though of the same nature, it is notorious that they are often affected very differently; therefore the male organs, for instance, in one form of a heterostyled plant might be affected by those unknown causes which induce abortion, differently from the homologous but functionally different organs in the other form; and so conversely with the female organs. Thus the great difficulty before alluded to is much lessened in understanding how any cause whatever could lead to the simultaneous reduction and ultimate suppression of the male organs in half the individuals of a species, and of the female organs in the other half, whilst all were subjected to exactly the same conditions of life.

That such reduction or suppression has occurred in some heterostyled plants is almost certain. The Rubiaceae contain more heterostyled genera than any other family, and from their wide distribution we may infer that many of them became heterostyled at a remote period, so that there will have been ample time for some of the species to have been since rendered dioecious. Asa Gray informs me that Coprosma is dioecious, and that it is closely allied through Nertera to Mitchella, which as we know is a heterostyled dimorphic species. In the male flowers of Coprosma the stamens are exserted, and in the female flowers the stigmas; so that, judging from the affinities of the above three genera, it seems probable that an ancient short-styled form bearing long stamens with large anthers and large pollen-grains (as in the case of several Rubiaceous genera) has been converted into the male Coprosma; and that an ancient long-styled form with short stamens, small anthers and small pollen-grains has been converted into the female form. But according to Mr. Meehan, Mitchella itself is dioecious in some districts; for he says that one form has small sessile anthers without a trace of pollen, the pistil being perfect; while in another form the stamens are perfect and the pistil rudimentary. (7/6. ‘Proceedings of the Academy of Sciences of Philadelphia’ July 28, 1868 page 183.) He adds that plants may be observed in the autumn bearing an abundant crop of berries, and others without a single one. Should these statements be confirmed, Mitchella will be proved to be heterostyled in one district and dioecious in another.

Asperula is likewise a Rubiaceous genus, and from the published description of the two forms of A. scoparia, an inhabitant of Tasmania, I did not doubt that it was heterostyled; but on examining some flowers sent me by Dr. Hooker they proved to be dioecious. The male flowers have large anthers and a very small ovarium, surmounted by a mere vestige of a stigma without any style; whilst the female flowers possess a large ovarium, the anthers being rudimentary and apparently quite destitute of pollen. Considering how many Rubiaceous genera are heterostyled, it is a reasonable suspicion that this Asperula is descended from a heterostyled progenitor; but we should be cautious on this head, for there is no improbability in a homostyled Rubiaceous plant becoming dioecious. Moreover, in an allied plant, Galium cruciatum, the female organs have been suppressed in most of the lower flowers, whilst the upper ones remain hermaphrodite; and here we have a modification of the sexual organs without any connection with heterostylism.

Mr. Thwaites informs me that in Ceylon various Rubiaceous plants are heterostyled; but in the case of Discospermum one of the two forms is always barren, the ovary containing about two aborted ovules in each loculus; whilst in the other form each loculus contains several perfect ovules; so that the species appears to be strictly dioecious.

Most of the species of the South American genus Aegiphila, a member of the Verbenaceae, apparently are heterostyled; and both Fritz Muller and myself thought that this was the case with Ae. obdurata, so closely did its flowers resemble those of the heterostyled species. But on examining the flowers, the anthers of the long-styled form were found to be entirely destitute of pollen and less than half the size of those in the other form, the pistil being perfectly developed. On the other hand, in the short-styled form the stigmas are reduced to half their proper length, having also an abnormal appearance; whilst the stamens are perfect. This plant therefore is dioecious; and we may, I think, conclude that a short-styled progenitor, bearing long stamens exserted beyond the corolla, has been converted into the male; and a long-styled progenitor with fully developed stigmas into the female.

From the number of bad pollen-grains in the small anthers of the short stamens of the long-styled form of Pulmonaria angustifolia, we may suspect that this form is tending to become female; but it does not appear that the other or short-styled form is becoming more masculine. Certain appearances countenance the belief that the reproductive system of Phlox subulata is likewise undergoing a change of some kind.

I have now given the few cases known to me in which heterostyled plants appear with some considerable degree of probability to have been rendered dioecious. Nor ought we to expect to find many such cases, for the number of heterostyled species is by no means large, at least in Europe, where they could hardly have escaped notice. Therefore the number of dioecious species which owe their origin to the transformation of heterostyled plants is probably not so large as might have been anticipated from the facilities which they offer for such conversion.

In searching for cases like the foregoing ones, I have been led to examine some dioecious or sub-dioecious plants, which are worth describing, chiefly as they show by what fine gradations hermaphrodites may pass into polygamous or dioecious species.