As two objects in most respects opposed, namely, cross-fertilisation and self-fertilisation, have in many cases to be gained, we can understand the co-existence in so many flowers of structures which appear at first sight unnecessarily complex and of an opposed nature. We can thus understand the great contrast in structure between cleistogene flowers, which are adapted exclusively for self-fertilisation, and ordinary flowers on the same plant, which are adapted so as to allow of at least occasional cross-fertilisation. (10/21. Fritz Muller has discovered in the animal kingdom ‘Jenaische Zeitschr.’ B. 4 page 451, a case curiously analogous to that of the plants which bear cleistogene and perfect flowers. He finds in the nests of termites in Brazil, males and females with imperfect wings, which do not leave the nests and propagate the species in a cleistogene manner, but only if a fully-developed queen after swarming does not enter the old nest. The fully-developed males and females are winged, and individuals from distinct nests can hardly fail often to intercross. In the act of swarming they are destroyed in almost infinite numbers by a host of enemies, so that a queen may often fail to enter an old nest; and then the imperfectly developed males and females propagate and keep up the stock.) The former are always minute, completely closed, with their petals more or less rudimentary and never brightly coloured; they never secrete nectar, never are odoriferous, have very small anthers which produce only a few grains of pollen, and their stigmas are but little developed. Bearing in mind that some flowers are cross-fertilised by the wind (called anemophilous by Delpino), and others by insects (called entomophilous), we can further understand, as was pointed out by me several years ago, the great contrast in appearance between these two classes of flowers. (10/22. ‘Journal of the Linnean Society’ volume 7 Botany 1863 page 77.) Anemophilous flowers resemble in many respects cleistogene flowers, but differ widely in not being closed, in producing an extraordinary amount of pollen which is always incoherent, and in the stigma often being largely developed or plumose. We certainly owe the beauty and odour of our flowers and the storage of a large supply of honey to the existence of insects.
ON THE RELATION BETWEEN THE STRUCTURE AND CONSPICUOUSNESS OF FLOWERS, THE VISITS OF INSECTS, AND THE ADVANTAGES OF CROSS-FERTILISATION.
It has already been shown that there is no close relation between the number of seeds produced by flowers when crossed and self-fertilised, and the degree to which their offspring are aaffected by the two processes. I have also given reasons for believing that the inefficiency of a plant’s own pollen is in most cases an incidental result, or has not been specially acquired for the sake of preventing self-fertilisation. On the other hand, there can hardly be a doubt that dichogamy, which prevails according to Hildebrand in the greater number of species (10/23. ‘Die Geschlecter Vertheiling’ etc. page 32.),—that the heterostyled condition of certain plants,—and that many mechanical structures—have all been acquired so as both to check self-fertilisation and to favour cross-fertilisation. The means for favouring cross-fertilisation must have been acquired before those which prevent self-fertilisation; as it would manifestly be injurious to a plant that its stigma should fail to receive its own pollen, unless it had already become well adapted for receiving pollen from another individual. It should be observed that many plants still possess a high power of self-fertilisation, although their flowers are excellently constructed for cross-fertilisation—for instance, those of many papilionaceous species.
It may be admitted as almost certain that some structures, such as a narrow elongated nectary, or a long tubular corolla, have been developed in order that certain kinds of insects alone should obtain the nectar. These insects would thus find a store of nectar preserved from the attacks of other insects; and they would thus be led to visit frequently such flowers and to carry pollen from one to the other. (10/24. See the interesting discussion on this subject by Hermann Muller, ‘Die Befruchtung’ etc. page 431.) It might perhaps have been expected that plants having their flowers thus peculiarly constructed would profit in a greater degree by being crossed, than ordinary or simple flowers; but this does not seem to hold good. Thus Tropaeolum minus has a long nectary and an irregular corolla, whilst Limnanthes douglasii has a regular flower and no proper nectary, yet the crossed seedlings of both species are to the self-fertilised in height as 100 to 79. Salvia coccinea has an irregular corolla, with a curious apparatus by which insects depress the stamens, while the flowers of Ipomoea are regular; and the crossed seedlings of the former are in height to the self-fertilised as 100 to 76, whilst those of the Ipomoea are as 100 to 77. Fagopyrum is dimorphic, and Anagallis collina is non-dimorphic, and the crossed seedlings of both are in height to the self-fertilised as 100 to 69.
With all European plants, excepting the comparatively rare anemophilous kinds, the possibility of distinct individuals intercrossing depends on the visits of insects; and Hermann Muller has proved by his valuable observations, that large conspicuous flowers are visited much more frequently and by many more kinds of insects, than are small inconspicuous flowers. He further remarks that the flowers which are rarely visited must be capable of self-fertilisation, otherwise they would quickly become extinct. (10/25. ‘Die Befruchtung’ etc. page 426. ‘Nature’ 1873 page 433.) There is, however, some liability to error in forming a judgment on this head, from the extreme difficulty of ascertaining whether flowers which are rarely or never visited during the day (as in the above given case of Fumaria capreolata) are not visited by small nocturnal Lepidoptera, which are known to be strongly attracted by sugar. (10/26. In answer to a question by me, the editor of an entomological journal writes—“The Depressariae, as is notorious to every collector of Noctuae, come very freely to sugar, and no doubt naturally visit flowers:” the ‘Entomologists’ Weekly Intelligencer’ 1860 page 103.) The two lists given in the early part of this chapter support Muller’s conclusion that small and inconspicuous flowers are completely self-fertile: for only eight or nine out of the 125 species in the two lists come under this head, and all of these were proved to be highly fertile when insects were excluded. The singularly inconspicuous flowers of the Fly Ophrys (O. muscifera), as I have elsewhere shown, are rarely visited by insects; and it is a strange instance of imperfection, in contradiction to the above rule, that these flowers are not self-fertile, so that a large proportion of them do not produce seeds. The converse of the rule that plants bearing small and inconspicuous flowers are self-fertile, namely, that plants with large and conspicuous flowers are self-sterile, is far from true, as may be seen in our second list of spontaneously self-fertile species; for this list includes such species as Ipomoea purpurea, Adonis aestivalis, Verbascum thapsus, Pisum sativum, Lathyrus odoratus, some species of Papaver and of Nymphaea, and others.
The rarity of the visits of insects to small flowers, does not depend altogether on their inconspicuousness, but likewise on the absence of some sufficient attraction; for the flowers of Trifolium arvense are extremely small, yet are incessantly visited by hive and humble-bees, as are the small and dingy flowers of the asparagus. The flowers of Linaria cymbalaria are small and not very conspicuous, yet at the proper time they are freely visited by hive-bees. I may add that, according to Mr. Bennett, there is another and quite distinct class of plants which cannot be much frequented by insects, as they flower either exclusively or often during the winter, and these seem adapted for self-fertilisation, as they shed their pollen before the flowers expand. (10/27. ‘Nature’ 1869 page 11.)
That many flowers have been rendered conspicuous for the sake of guiding insects to them is highly probable or almost certain; but it may be asked, have other flowers been rendered inconspicuous so that they may not be frequently visited, or have they merely retained a former and primitive condition? If a plant were much reduced in size, so probably would be the flowers through correlated growth, and this may possibly account for some cases; but the size and colour of the corolla are both extremely variable characters, and it can hardly be doubted that if large and brightly-coloured flowers were advantageous to any species, these could be acquired through natural selection within a moderate lapse of time, as indeed we see with most alpine plants. Papilionaceous flowers are manifestly constructed in relation to the visits of insects, and it seems improbable, from the usual character of the group, that the progenitors of the genera Vicia and Trifolium produced such minute and unattractive flowers as those of V. hirsuta and T. procumbens. We are thus led to infer that some plants either have not had their flowers increased in size, or have actually had them reduced and purposely rendered inconspicuous, so that they are now but little visited by insects. In either case they must also have acquired or retained a high degree of self-fertility.
If it became from any cause advantageous to a species to have its capacity for self-fertilisation increased, there is little difficulty in believing that this could readily be effected; for three cases of plants varying in such a manner as to be more fertile with their own pollen than they originally were, occurred in the course of my few experiments, namely, with Mimulus, Ipomoea, and Nicotiana. Nor is there any reason to doubt that many kinds of plants are capable under favourable circumstances of propagating themselves for very many generations by self-fertilisation. This is the case with the varieties of Pisum sativum and of Lathyrus odoratus which are cultivated in England, and with Ophrys apifera and some other plants in a state of nature. Nevertheless, most or all of these plants retain structures in an efficient state which cannot be of the least use excepting for cross-fertilisation. We have also seen reason to suspect that self-fertilisation is in some peculiar manner beneficial to certain plants; but if this be really the case, the benefit thus derived is far more than counter-balanced by a cross with a fresh stock or with a slightly different variety.
Notwithstanding the several considerations just advanced, it seems to me highly improbable that plants bearing small and inconspicuous flowers have been or should continue to be subjected to self-fertilisation for a long series of generations. I think so, not from the evil which manifestly follows from self-fertilisation, in many cases even in the first generation, as with Viola tricolor, Sarothamnus, Nemophila, Cyclamen, etc.; nor from the probability of the evil increasing after several generations, for on this latter head I have not sufficient evidence, owing to the manner in which my experiments were conducted. But if plants bearing small and inconspicuous flowers were not occasionally intercrossed, and did not profit by the process, all their flowers would probably have been rendered cleistogene, as they would thus have largely benefited by having to produce only a small quantity of safely-protected pollen. In coming to this conclusion, I have been guided by the frequency with which plants belonging to distinct orders have been rendered cleistogene. But I can hear of no instance of a species with all its flowers rendered permanently cleistogene. Leersia makes the nearest approach to this state; but as already stated, it has been known to produce perfect flowers in one part of Germany. Some other plants of the cleistogene class, for instance Aspicarpa, have failed to produce perfect flowers during several years in a hothouse; but it does not follow that they would fail to do so in their native country, any more than with Vandellia, which with me produced only cleistogene flowers during certain years. Plants belonging to this class commonly bear both kinds of flowers every season, and the perfect flowers of Viola canina yield fine capsules, but only when visited by bees. We have also seen that the seedlings of Ononis minutissima, raised from the perfect flowers fertilised with pollen from another plant, were finer than those from self-fertilised flowers; and this was likewise the case to a certain extent with Vandellia. As therefore no species which at one time bore small and inconspicuous flowers has had all its flowers rendered cleistogene, I must believe that plants now bearing small and inconspicuous flowers profit by their still remaining open, so as to be occasionally intercrossed by insects. It has been one of the greatest oversights in my work that I did not experimentise on such flowers, owing to the difficulty of fertilising them, and to my not having seen the importance of the subject. (10/28. Some of the species of Solanum would be good ones for such experiments, for they are said by Hermann Muller ‘Befruchtung’ page 434, to be unattractive to insects from not secreting nectar, not producing much pollen, and not being very conspicuous. Hence probably it is that, according to Verlot ‘Production des Varieties’ 1865 page 72, the varieties of “les aubergines et les tomates” (species of Solanum) do not intercross when they are cultivated near together; but it should be remembered that these are not endemic species. On the other hand, the flowers of the common potato (S. tuberosum), though they do not secrete nectar Kurr ‘Bedeutung der Nektarien’ 1833 page 40, yet cannot be considered as inconspicuous, and they are sometimes visited by diptera (Muller), and, as I have seen, by humble-bees. Tinzmann (as quoted in ‘Gardeners’ Chronicle’ 1846 page 183, found that some of the varieties did not bear seed when fertilised with pollen from the same variety, but were fertile with that from another variety.)
It should be remembered that in two of the cases in which highly self-fertile varieties appeared amongst my experimental plants, namely, with Mimulus and Nicotiana, such varieties were greatly benefited by a cross with a fresh stock or with a slightly different variety; and this likewise was the case with the cultivated varieties of Pisum sativum and Lathyrus odoratus, which have been long propagated by self-fertilisation. Therefore until the contrary is distinctly proved, I must believe that as a general rule small and inconspicuous flowers are occasionally intercrossed by insects; and that after long-continued self-fertilisation, if they are crossed with pollen brought from a plant growing under somewhat different conditions, or descended from one thus growing, their offspring would profit greatly. It cannot be admitted, under our present state of knowledge, that self-fertilisation continued during many successive generations is ever the most beneficial method of reproduction.