Introduction
While Charles Darwin is famous throughout the world for the development of the theory of evolution and natural selection, few appreciate that he was also a preeminent botanist. Darwin’s work in botany is extremely varied and includes experiments that are still cited in college-level textbooks because of their elegant experimental design and results. And of course, Darwin’s botanical observations, along with his extensive knowledge of many other areas of science (for example, geology and zoology), were involved in shaping his ideas on evolution.
Darwin’s botanical interests were broad and eclectic. He published books on such far-ranging topics as domesticated plants (1875), orchid pollination (1877a), heterostyly (1877b), the effects of cross and self pollination (1878), plant movements and tropisms (1881, 1882), and insectivorous plants (1888). In addition to these works, Darwin also published botanical work in journals, was in regular correspondence with many of the outstanding botanists of the time (for example, Joseph Hooker and Asa Gray), and, in later life, worked with his son Francis on botanical research.
Darwin’s love of plants appears to have been deeply rooted in his childhood. His parents were both interested in gardening and maintained a varied collection of plants in their conservatory and gardens in Shrewsbury, where Darwin grew up. Indeed, one of the few images of Darwin as a child (age 6) show him kneeling with a potted plant on his thigh. In his autobiographical chapter, Darwin (1887) mentions that “…apparently I was interested at this early age in the variability of plants!” A schoolfellow remembers Darwin’s bringing a flower to school and saying that his mother had taught him how to identify the plant by studying the flower.
Darwin’s interest in botany reasserted itself when he attended Cambridge in 1828, where he was greatly influenced by the botanist, John S Henslow. In his own words (Darwin 1887: 52): “Before long I became well acquainted with Henslow, and during the latter half of my time at Cambridge took long walks with him on most days; so that I was called by some of the dons ‘the man who walks with Henslow;’ and in the evening I was very often asked to join his family dinner.” Henslow’s main research interest during this time was understanding patterns of variation within and between populations, work that is believed to have given Darwin material for his later understanding of variation and speciation (Kohn and others 2005).
Henslow is responsible for arranging Darwin’s position as gentleman naturalist on HMS Beagle. During the voyage, Darwin displayed great interest in the flora he encountered and collected more than 2000 herbarium specimens. His collections of “all plants in flower” from the Galápagos Islands, were the basis for the first flora of that archipelago and were largely responsible for his understanding of island endemism (Kohn and others 2005).
It would be no trivial task to report here on all of Darwin’s botanical work, so instead, I will feature a few examples that represent his use of rigorous scientific methodology, sharp powers of observation, and creative thinking. I will report his work on 1) heterostyly in Primula (primroses), 2) plant movements and phototropism, and 3) pollination mechanisms in orchids.
Heterostyly in Primula veris,the English Cowslip
Darwin was first exposed to an extraordinary observation relating to one of Great Britain’s most loved wild flowers, the English cowslip, by his mentor John Henslow: that the length of styles and stamens varied among individual plants (Kohn and others 2005). Some plants had flowers with long stamens and short styles — the thrum type; others had flowers with short stamens and long styles — the pin type (Figure 1). This phenomenon is known as heterostyly, and Darwin studied it extensively in the 1850s (Darwin 1877b). He also observed that the two flower types varied in pollen size; pollen produced by pin flowers was noticeably smaller in diameter than that produced by thrum flowers. What could be the explanation for these phenomena?
Figure 1. Figure from Darwin’s work on heterostyly in Primula species (1877) showing the long style and short stamens of the pin flowers and the short style and long stamens of the thrum flowers.
His first hypothesis was that Primula veris was tending toward dioecy (where a species has male individuals with only male flowers and female individuals with female flowers). His reasoning behind this was: “Pin plants with their longer carpels, smaller stamens and pollen grains are more feminine; conversely thrum plants are more masculine”. If this were true, then, he expected, pin plants should produce more seeds than thrum plants. To test this, he collected seeds from plants growing in different habitats (to negate possible environmental effects), then counted and weighed them. The results? Pin plants produced less seed than thrum by a proportion of nearly 3 to 4, suggesting that pin plants were certainly not more “feminine” than thrum.
His next hypothesis was: “The two forms of flowers in Primula are related to cross-pollination and prevention of inbreeding.” To test this he set up a sophisticated pollination experiment. First, he covered populations of Primula with fine netting to prevent insect pollination. He then hand pollinated the plants in the following combinations: 1) thrum plants pollinated with pin pollen and vice versa, 2) thrum plants pollinated with thrum pollen, and 3) pin plants pollinated with pin pollen. In cases in which he was using pollen from like plants (2 and 3 above), he always took the pollen from a different plant than the one being pollinated to avoid any effects of inbreeding. This alone shows the depths of his knowledge about reproduction and the care he took in his experimental design.
After the plants had set seed, he counted and weighed seeds from both 100 flowers and 100 capsules. He found that by all measures, plants pollinated by the opposite type of flower had markedly greater reproductive success. From this work he concluded: “The benefit of heterostyled dimorphic plants derives from.....the intercrossing of distinct plants” and “the pollen grains from the longer stamens.....become larger in order to allow the development of longer [pollen] tubes.”
Plant movements and phototropism
Darwin explored plant movements extensively, from the way vines and other plants circumnutate (successive bowing or bending in different directions of the growing tip of the stem) to sleep movements (folding of leaves up or down at night [Darwin 1881]) to movements of insectivorous plants (Darwin 1888). In all his explorations, he performed numerous experiments. For example, in insectivorous plants such as the Venus Flytrap (Dionaea muscipula) and Sundews (Drosera spp), he explored how food was absorbed by the leaves, what effect various “foodstuffs” had on the plant’s ability to react or absorb, and how the impulse to move was transmitted.
The elegant experiments of Darwin and his son Francis on phototropism — the growth of a plant towards a unidirectional source of light — are commonly cited in biology textbooks today (Darwin 1881). In their work on phototropism in Canary grass seedlings (Phalaris canariensis), they observed in experiments on seedlings raised in the dark, then exposed to a unidirectional source of light, a marked curvature toward the light. They formed a hypothesis that the tip of the seedling may be responsible for the curvature toward light. To test this hypothesis, they cut the tips off some seedlings while leaving a control group with tips intact. They found that those seedlings with the tips removed did not respond to a unidirectional source of light while the control group with tips intact bent markedly toward the light source.
But the question remained: Did the experimental seedlings remain upright due to their tips not being present to detect light or because they had been damaged? To address this question, they covered some seedling tips with opaque caps and, as controls, covered other tips with transparent caps or placed opaque collars around the base of the seedlings, leaving the tips exposed. They found that the seedlings with opaque caps remained upright, showing no signs of phototropism, while both controls did bend toward the light.
From all of this work, they concluded: “These results seem to imply the presence of some matter in the upper part which is acted on by light, and which transmits its effects to the lower part.” We now know that this “matter” is a plant hormone called auxin. Auxin is produced in the apical meristem of plants, is transported down the stem, and accumulates on the shady side of a plant subjected to unidirectional light. This increased concentration of auxin causes the cells on the dark side to enlarge, thus bending the plant toward light. Of course Darwin and his son knew nothing about this mechanism, but their work laid the foundation for subsequent experiments that led to our current understanding of auxins.
Pollination mechanisms in orchids
It is hard to conceive that any botanist worth his weight in chlorophyll would be immune to the charms and foibles of orchids, and Darwin was no exception. He was especially interested in the close relationship between the flowers of an orchid species and their pollinators (Darwin 1877a). There can be little doubt that his work on orchids provided him with ample material for understanding co-evolution.
Darwin made minute observations on pollination in diverse orchids, including the fascinating bee orchids (Ophrys species). Ophrys excel in the lengths they will go to attract a pollinator. Depending on the species, they mimic female bees, wasps, or beetles. To add to the ruse, they emit pheromones, and these “come hither” smells strongly attract male insects, causing the male to attempt copulation with the orchid flower. As the male pseudocopulates with the orchid flower, packets of pollen called pollinia are attached to his body. And of course, the male is drawn to other individuals of the same orchid species for similar reasons, depositing pollen on the receptive stigma, thus effecting cross-pollination. Darwin spent many hours in painstaking observations and experiments on Ophrys and other orchids to understand the mechanics of pollinia and their attachment to pollinators.
Darwin was fascinated by the observation that a bee orchid common to England, Ophrys apifera, was apparently “adapted to self-fertilization.” His further observations convinced him that these self-pollinating orchids still retained the mechanisms needed for pollination by bees. When he imitated a bee’s action using an object, the pollinia reacted as in other Ophrys, readily attaching to what would have been the bee’s head. He concluded that Ophrys apifera must have at one time been commonly pollinated by bees but, due to an insufficiency of pollinators, “became slightly modified so as to fertilise themselves” (Darwin 1877a).
A famous example of co-evolution in orchids that came in for its share of controversy was Darwin’s explanation for the pollination of Angraecum sesquipedale, an orchid native to Madagascar. This orchid has flowers with very long spurs — about 20–35 cm long! Orchids with spurred flowers usually offer a nectar reward at the base of the spur, to reward the moth pollinator. Darwin hypothesized that Angraecum must be pollinated by a moth with a proboscis long enough to reach the nectar and thus effect pollination. This idea was derided and even used as proof of creationism. In 1867, George Campbell published a book in which he argued that the complexity of A sesquipedale supports the idea that species were created by a supernatural being. Unfortunately for Campbell, a moth with a proboscis of the required length was found in 1903; it was first named Xanthopan morganii praedicta to honor Darwin’s correct prediction.
Summary
It is clear, even from the few examples given above, that Darwin’s botanical work was important to the development of his ideas on evolution and natural selection. Darwin began thinking about evolution soon after his return from the Beagle voyages, starting his notebooks on “transmutation” (evolution) in 1837. He was uniquely situated for the task of developing the theory of evolution, from his early exposure to Lamarckian evolutionary thinking through his grandfather (Erasmus Darwin) and Robert Grant at the University of Edinburgh, his early exposure to the work of Charles Lyell’s book on fossils and the botanist Henslow’s work on populations and speciation, his travels on the Beagle, and his broad knowledge of so many aspects of natural history. This is not to discount other attributes that uniquely placed Darwin to develop the theory: he was hard working and, since independently wealthy, able to spend all of his time on his science. Most importantly, he was able to think logically and creatively (“outside the box” as we say today).
There is no doubt that all the clues and scientific advancements needed to develop the theory of evolution and natural selection were present in the early 19th century. If Darwin had not proposed the theory of evolution, someone else would have. In fact, that is exactly what did happen! Because Darwin put off publication of his ideas, Alfred Russel Wallace caught up with him, and the two presented their findings simultaneously in 1858. But I think that Darwin deserves to have the greater part of the credit. He developed his understanding of evolution and natural selection well before Wallace and it was he who took on the enormous task in the Origin (1859) and elsewhere of convincing the world that evolution was real.