FORMS OF FLOWERS, POLLINATION
Primula is a large genus, with nearly 500 species and countless cultivars, all low-growing perennial herbs, with tufted rosettes of leaves highlighted by showy flowers arranged as umbels on naked stalks. Darwin worked on several species including three common in his woods and meadows, P. veris (cowslip), P. vulgaris (primrose), and the uncommon P. elatior (oxlip), and five other species including P. sinensis from China. One significant insight from his experiments involved oxlips, long regarded as the hybrid offspring of primroses and cowslips. His early ideas about the plants were published in the first edition of Origin,126 but after experiments crossbreeding them, he determined that they were true species rather than varieties, earning him further respect from botanists. The plants were omitted from later editions of Origin when he realized his mistake.
Many of the cases of strongly-marked varieties or doubtful species well deserve consideration; for several interesting lines of argument, from geographical distribution, analogical variation, hybridism, &c., have been brought to bear on the attempt to determine their rank. I will here give only a single instance,—the well-known one of the primrose and cowslip, or Primula veris and elatior. These plants differ considerably in appearance; they have a different flavour and emit a different odour; they flower at slightly different periods; they grow in somewhat different stations; they ascend mountains to different heights; they have different geographical ranges; and lastly, according to very numerous experiments made during several years by that most careful observer Gärtner, they can be crossed only with much difficulty. We could hardly wish for better evidence of the two forms being specifically distinct. On the other hand, they are united by many intermediate links, and it is very doubtful whether these links are hybrids; and there is, as it seems to me, an overwhelming amount of experimental evidence, showing that they descend from common parents and consequently must be ranked as varieties.
By 1860, Darwin had become curious about the two distinct kinds of flowers found in primroses, one with long pistils and short stamens (so-called “pin” flowers, which Darwin called “female”) and the other just the opposite, with short pistils and long stamens (“thrum,” or “male” flowers to Darwin). He knew that botanists and other observers were aware of this curious dimorphism, termed heterostyly today, but also that no one considered their purpose. At first Darwin thought the morphs were evolving into separate sexes, that he fortuitously caught them in the very process of diverging. But in 1860, soon after the publication of Origin, he began crossing experiments, beginning with putting his kids to work collecting the different morphs—281 “male” flowers and 241 “female” in one productive haul. He observed and measured pollen grains of each morph and did a series of tests crossing pollen between them, establishing “legitimate marriages” that yielded seed, where the stigma of one form is pollinated by pollen from stamens of another form, and fruitless “illegitimate marriages” when pollen from the same plant was transferred its own stigma. He grew plants for several generations this way and counted the seeds produced by each morph, hypothesizing that the “male” flowers would produce fewer seeds since they were becoming less and less “female.”
He found just the opposite, however—“male” flowers produced more seeds, not fewer—thus running headlong into what his friend Thomas Henry Huxley called the “great tragedy of science,” namely, “the slaying of a beautiful hypothesis by an ugly fact.”127
Darwin ultimately abandoned the idea that the flower morphs were evolving separate sexes and came to see them as an adaptation to promote outcrossing between individuals as much as possible. The results of his observations and experiments were first presented at the Linnean Society of London in 1862, and then in Forms of Flowers in 1877, with more experiments described in Cross and Self Fertilisation. Darwin’s research on primulas began his great interest in other genera and families with heterostyly; so much so that he wrote in his autobiography, “No little discovery of mine ever gave me so much pleasure as the making out the meaning of heterostyled flowers.”128
If a large number of Primroses or Cowslips (P. vulgaris and veris) be gathered, they will be found to consist, in about equal numbers, of two forms, obviously differing in the length of their pistils and stamens. Florists who cultivate the Polyanthus and Auricula are well aware of this difference, and call those which display the globular stigma at the mouth of the corolla “pin-headed” or “pin-eyed,” and those which display the stamens “thrum-eyed.” I will designate the two forms as long-styled and short-styled. Those botanists with whom I have spoken on the subject have looked at the case as one of mere variability, which is far from the truth.
In the Cowslip, in the long-styled form, the stigma projects just above the tube of the corolla and is externally visible; it stands high above the anthers, which are situated halfway down the tube, and cannot be easily seen. In the short-styled form, the anthers are attached at the mouth of the tube, and therefore stand high above the stigma; for the pistil is short, not rising above halfway up the tubular corolla. The corolla itself is of a different shape in the two forms, the throat or expanded portion above the attachment of the anthers being much longer in the long-styled than in the short-styled form. Village children notice this difference, as they can best make necklaces by threading and slipping the corollas of the long-styled flowers into each other. But there are much more important differences. The stigma in the long-styled plants is globular, in the short-styled it is depressed on the summit, so that the longitudinal axis of the former is sometimes nearly double that of the latter. The shape, however, is in some degree variable; but one difference is persistent, namely, that the stigma of the long-styled is much rougher: in some specimens carefully compared, the papillae which render the stigmas rough were in the long-styled form from twice to thrice as long as in the short-styled. There is another and more remarkable difference, namely, in the size of the pollen-grains. I measured with the micrometer many specimens, dry and wet, taken from plants growing in different situations, and always found a palpable difference. …
There is also a difference in shape, the grains from the short-styled plants being nearly spherical, those from the long-styled being oblong with the angles rounded; this difference in shape disappears when the grains are distended with water. Lastly, as shall presently see, the short-styled plants produce more seed than the long-styled.
To sum up the differences:—The long-styled plants have a much longer pistil, with a globular and much rougher stigma, standing high above the anthers. The stamens are short; the grains of pollen smaller and oblong in shape. The upper half of the tube of the corolla is more expanded. The number of seeds produced is smaller.
The short-styled plants have a short pistil, half the length of the tube of the corolla, with a smooth depressed stigma standing beneath the anthers. The stamens are long; the grains of pollen are spherical and larger. The tube of the corolla is of the same diameter till close to its upper end. The number of seeds produced is larger.
Long-styled, left. Short-styled, right.
I have examined a large number of flowers; and though the shape of the stigma and the length of the pistil vary, especially in the short-styled form, I have never seen any transitional grades between the two forms. There is never the slightest doubt under which form to class a plant. I have never seen the two forms on the same plant. I marked many Cowslips and Primroses, and found, the following year, that all retained the same character, as did some in my garden which flowered out of their proper season in the autumn. … An excellent proof of the permanence of the two forms is seen in nursery gardens, where choice varieties of the Polyanthus are propagated by division; and I found whole beds of several varieties, each consisting exclusively of the one or the other form. The two forms exist in the wild state in about equal numbers: I collected from several different stations, taking every plant which grew on each spot, 522 umbels; 241 were long-styled, and 281 short-styled. No difference in tint or size could be perceived in the two great masses of flowers.
I examined many cultivated Cowslips (P. veris) or Polyanthuses, and Oxlips; and the two forms always presented the same differences, including the same relative difference in the size of the pollen-grains. …
The first idea which naturally occurred was, that the species were tending towards a dioicous condition; that the long-styled plants, with their rougher stigmas, were more feminine in nature, and would produce more seed; that the short-styled plants, with their long stamens and larger pollen-grains, were more masculine in nature. Accordingly, in 1860, I marked some Cowslips of both forms growing in my garden, and others growing in an open field, and others in a shady wood, and gathered and weighed the seed. In each of these little lots the short-styled plants yielded, contrary to my expectation, most seed. …
In 1861, I tried the result in a fuller and fairer manner. I transplanted in the previous autumn a number of wild plants into a large bed in my garden, treating them all alike. …
The season was much better this year than the last, and the plants grew in good soil, instead of in a shady wood or struggling with other plants in the open field; consequently the actual produce of seed was considerably greater. Nevertheless, we have the same relative result; for the short-styled plants produced more seed than the long-styled in the proportion of three to two. …
For the sake of clearness, the general result is given in the following diagram, in which the dotted lines with arrows represent how in the four unions pollen has been applied.
We here have a case new, as far as I know, in the animal and vegetable kingdoms. We see the species of Primula divided into two sets or bodies, which cannot be called distinct sexes, for both are hermaphrodites; yet they are to a certain extent sexually distinct, for they require for perfect fertility reciprocal union. They might perhaps be called sub-dioicous hermaphrodites. As quadrupeds are divided into two nearly equal bodies of different sexes, so here we have two bodies, approximately equal in number, differing in their sexual powers and related to each other like males and females. There are many hermaphrodite animals which cannot fertilize themselves, but must unite with another hermaphrodite: so it is with numerous plants; for the pollen is often mature and shed, or is mechanically protruded, before the flower’s own stigma is ready; so that these hermaphrodite flowers absolutely require for their sexual union the presence of another hermaphrodite. But in Primula there is this wide difference, that one individual Cowslip, for instance, though it can with mechanical aid imperfectly fertilize itself, for full fertility must unite with another individual; but it cannot unite with any individual in the same manner as an hermaphrodite Snail or Earth-worm can unite with any other one Snail or Earth-worm; but one form of the Cowslip, to be perfectly fertile, must unite with one of the other form, just as a male quadruped must and can unite only with a female.
Pulmonaria officinalis. Watercolor by Elizabeth Wharton, British Flowers.