FORMS OF FLOWERS, POLLINATION
Among the more than 200 species of Linum, the largest genus in the flax or linseed family, many are cultivated for their beautiful flowers while others are grown for food and fiber. The common flax Linum usitatissimum, a species cultivated since antiquity, is so versatile that its very name, usitatissimum, is thought to derive from the Latin meaning “most useful.” Linum was most useful to Darwin as a nice illustration of floral dimorphism, found in about half of Linum species, where one plant type, or morph, bears long-styled pistils and short stamens, and another morph has short-styled pistils and long stamens. Darwin was the first naturalist to recognize the functional (and adaptive) significance of this phenomenon, termed heterostyly. He had first discovered flower dimorphism in primroses (see p. 171), but found Linum to be an even better example.
When he became aware of Linum floral dimorphism in 1861, Darwin initiated a series of crossing experiments with the species L. grandiflorum and L. perenne, procured with the help of his friends at the Royal Botanic Gardens, Kew. The results, first presented in a paper to the Linnean Society of London88 and later incorporated into Forms of Flowers, proved as puzzling as they were interesting. As far as he could make out with a microscope, pollen from the two morphs were identical. Yet, the short-style morph proved fertile with pollen from either morph, while flowers of the long-style morph could only be fertilized with pollen from short-style plants. He called fertile matches “legitimate” crosses, and infertile ones “illegitimate.” Noting that “it may be said that the two pollens and the two stigmas mutually recognise each other by some means,”89 Darwin correctly inferred that this recognition system functioned to prevent self-fertilization and promote outcrossing, presaging the discovery in the next century of genetic and biochemical self-recognition mechanisms in plants—in particular the widespread self-incompatibility (SI) genetic system.1 His results prompted an analysis of the differences between wind and insect pollination.
It has long been known that several species of Linum present two forms, and, having observed this fact in L. flavum more than thirty years ago, I was led, after ascertaining the nature of heterostylism in Primula, to examine the first species of Linum which I met with, namely, the beautiful L. grandiflorum. This plant exists under two forms, occurring in about equal numbers, which differ little in structure but greatly in function. The foliage, corolla, stamens, and pollen-grains (the latter examined both distended with water and dry) are alike in the two forms. … The difference is confined to the pistil; in the short-styled form the styles and the stigmas are only about half the length of those in the long-styled. A more important distinction is that the five stigmas in the short-styled form diverge greatly from one another and pass out between the filaments of the stamens, and thus lie within the tube of the corolla. In the long-styled form, the elongated stigmas stand nearly upright and alternate with the anthers. In this latter form, the length of the stigmas varies considerably, their upper extremities projecting even a little above the anthers or reaching up only to about their middle. Nevertheless, there is never the slightest difficulty in distinguishing between the two forms; for, besides the difference in the divergence of the stigmas, those of the short-styled form never reach even to the bases of the anthers. In this form, the papillae on the stigmatic surfaces are shorter, darker-coloured, and more crowded together than in the long-styled form; but these differences seem due merely to the shortening of the stigma, for in the varieties of the long-styled form with shorter stigmas, the papillae are more crowded and darker-coloured than in those with the longer stigmas. Considering the slight and variable differences between the two forms of this Linum, it is not surprising that hitherto they have been overlooked. …
Linum grandiflorum. Long-styled form, left. Short-styled form, right. s = stigma
The absolute sterility (judging from the experiments of 1861) of the long-styled plants with their own-form pollen led me to examine into its apparent cause; and the results are so curious that they are worth giving in detail. The experiments were tried on plants grown in pots and brought successively into the house.
Pollen from a short-styled plant was placed on the five stigmas of a long-styled flower, and these, after thirty hours, were found deeply penetrated by a multitude of pollen-tubes, far too numerous to be counted; the stigmas had also become discoloured and twisted. I repeated this experiment on another flower, and in eighteen hours the stigmas were penetrated by a multitude of long pollen-tubes. This is what might have been expected, as the union is a legitimate one. The converse experiment was likewise tried, and pollen from a long-styled flower was placed on the stigmas of a short-styled flower, and in twenty-four hours the stigmas were discoloured, twisted, and penetrated by numerous pollen-tubes; and this, again, is what might have been expected, as the union was a legitimate one. …
I could add other experiments; but those now given amply suffice to show that the pollen-grains of a short-styled flower placed on the stigma of a long-styled flower emit a multitude of tubes after an interval of from five to six hours and penetrate the tissue ultimately to a great depth; and that after twenty-four hours the stigmas thus penetrated change colour, become twisted, and appear half-withered. On the other hand, pollen-grains from a long-styled flower placed on its own stigmas, do not emit their tubes after an interval of a day, or even three days; or at most only three or four grains out of a multitude emit their tubes, and these apparently never penetrate the stigmatic tissue deeply, and the stigmas themselves do not soon become discoloured and twisted.
The plants both of L. perenne and grandiflorum grew with their branches interlocked, and with scores of flowers of the two forms close together; they were covered by a rather coarse net, through which the wind, when high, passed; and such minute insects as Thrips could not, of course, be excluded; yet we have seen that the utmost possible amount of accidental fertilisation on seventeen long-styled plants in the one case, and on eleven long-styled plants in the other, resulted in the production, in each case, of three poor capsules; so that when the proper insects are excluded, the wind does hardly anything in the way of carrying pollen from plant to plant. I allude to this fact because botanists, in speaking of the fertilisation of various flowers, often refer to the wind or to insects as if the alternative were indifferent. This view, according to my experience, is entirely erroneous. When the wind is the agent in carrying pollen, either from one sex to the other, or from hermaphrodite to hermaphrodite, we can recognise structure as manifestly adapted to its action as to that of insects when these are the carriers. We see adaptation to the wind in the incoherence of the pollen,—in the inordinate quantity produced (as in the Coniferae, Spinage, &c.),—in the dangling anthers well fitted to shake out the pollen,—in the absence or small size of the perianth,—in the protrusion of the stigmas at the period of fertilisation,—in the flowers being produced before they are hidden by the leaves,—and in the stigmas being downy or plumose (as in the Gramineae, Docks, &c.), so as to secure the chance-blown grains. In plants which are fertilised by the wind, the flowers do not secrete nectar, their pollen is too incoherent to be easily collected by insects, they have not bright-coloured corollas to serve as guides, and they are not, as far as I have seen, visited by insects. When insects are the agents of fertilisation (and this is incomparably the more frequent case with hermaphrodite plants), the wind plays no part, but we see an endless number of adaptations to ensure the safe transport of the pollen by the living workers.
Lupinus pilosus. Water and bodycolor on vellum by English School artist, Album of Garden Flowers.