CROSS AND SELF-FERTILIZATION
Foxglove, with many species and varieties grown as biennials and perennials, is a lovely garden plant that is also well known for its toxicity and medicinal uses. Eighteenth century British physician and botanist William Withering is credited with being the first to systematically investigate the medicinal uses of Digitalis. His priority was disputed at the time by Erasmus Darwin, who also published on the use of this plant to treat certain diseases.52 The plant yields digitoxin and other cardiac glycosides used today in the treatment of irregular heartbeat and related ailments.
The most common foxglove species, Digitalis purpurea, is a biennial native to much of Europe, cultivated in gardens everywhere and often escaping to grow in profusion. Its lovely deep-throated purple spotted flowers, arranged in a spiral up the stem, are mainly visited by bumblebees (known to Darwin and contemporaries as humble-bees). Cross-pollination of the many flowers is assured by protandry, where the flowers start out functionally male and then pass into a female stage. New flowers are continually produced at the top of the stem, creating a flower age (and sex) gradient from pollen-shedding male flowers at the top of the stem to stigma-receptive female flowers toward the bottom.
Darwin noticed that bumblebees visiting Digitalis started at the bottom-most flowers and worked their way up, collecting pollen at the top before leaving the plant and making a beeline to the female flowers at the bottom of another spike. In one of his memorable field studies, while on a family holiday in coastal Barmouth, Wales, he set out to investigate foxglove self- and cross-pollination. In a field where the plants abounded, he placed a net over some individuals to keep insects away while leaving others uncovered. He then hand-pollinated some flowers under the net and left others alone to see if they might self-pollinate—but to make the selfing test more realistic, he simulated the windy seaside conditions by violently shaking the plants, surely a curious spectacle to any passersby. He found that the netted plants produced far fewer seeds than those out in the open, even when hand-pollinated, once again confirming for Darwin the central importance of outcrossing.53
Digitalis purpurea. The flowers of the common Foxglove are proterandrous; that is, the pollen is mature and mostly shed before the stigma of the same flower is ready for fertilisation. This is effected by the larger humble-bees, which, whilst in search of nectar, carry pollen from flower to flower. The two upper and longer stamens shed their pollen before the two lower and shorter ones. The meaning of this fact probably is that the anthers of the longer stamens stand near to the stigma, so that they would be the most likely to fertilise it; and as it is an advantage to avoid self-fertilisation, they shed their pollen first, thus lessening the chance. There is, however, but little danger of self-fertilisation until the bifid stigma opens; for Hildebrand found that pollen placed on the stigma before it had opened produced no effect. The anthers, which are large, stand at first transversely with respect to the tubular corolla, and if they were to dehisce in this position they would smear with pollen the whole back and sides of an entering humble-bee in a useless manner; but the anthers twist round and place themselves longitudinally before they dehisce. The lower and inner side of the mouth of the corolla is thickly clothed with hairs, and these collect so much of the fallen pollen that I have seen the under surface of a humble-bee thickly dusted with it; but this can never be applied to the stigma, as the bees in retreating do not turn their under surfaces upwards. …
I covered a plant growing in its native soil in North Wales with a net and fertilised six flowers each with its own pollen, and six others with pollen from a distinct plant growing within the distance of a few feet. The covered plant was occasionally shaken with violence, so as to imitate the effects of a gale of wind, and thus to facilitate as far as possible self-fertilisation. It bore ninety-two flowers and of these only twenty-four produced capsules; whereas almost all the flowers on the surrounding uncovered plants were fruitful. Of the twenty-four spontaneously self-fertilised capsules, only two contained their full complement of seed; six contained a moderate supply; and the remaining sixteen extremely few seeds. A little pollen adhering to the anthers after they had dehisced, and accidentally falling on the stigma when mature, must have been the means by which the above twenty-four flowers were partially self-fertilised; for the margins of the corolla in withering do not curl inwards, nor do the flowers in dropping off turn round on their axes, so as to bring the pollen-covered hairs, with which the lower surface is clothed, into contact with the stigma—by either of which means self-fertilisation might be effected.
Seeds from the above crossed and self-fertilised capsules, after germinating on bare sand, were planted in pairs on the opposite sides of five moderately-sized pots, which were kept in the greenhouse. The plants after a time appeared starved, and were therefore, without being disturbed, turned out of their pots, and planted in the open ground in two close parallel rows. …
Seedlings raised from intercrossed flowers on the same plant, and others from flowers fertilised with their own pollen, were grown in the usual manner in competition with one another on the opposite sides of ten pots. … In eight pots, in which the plants did not grow much crowded, the flower-stems on sixteen intercrossed plants were in height to those on sixteen self-fertilised plants, as 100 to 94. In the two other pots in which the plants grew much crowded, the flower-stems on nine intercrossed plants were in height to those on nine self-fertilised plants, as 100 to 90. That the intercrossed plants in these two latter pots had a real advantage over their self-fertilised opponents was well shown by their relative weights when cut down, which was as 100 to 78. The mean height of the flower-stems on the twenty-five intercrossed plants in the ten pots taken together was to that of the flower-stems on the twenty-five self-fertilised plants, as 100 to 92. Thus the intercrossed plants were certainly superior to the self-fertilised in some degree; but their superiority was small compared with that of the offspring from a cross between distinct plants over the self-fertilised, this being in the ratio of 100 to 70 in height. Nor does this latter ratio show at all fairly the great superiority of the plants derived from a cross between distinct individuals over the self-fertilised, as the former produced more than twice as many flower-stems as the latter and were much less liable to premature death.
Dionaea muscipula. Pen-and-ink drawing by John Ellis, on letter to Carl Linnaeus.