Fertilisation of Orchids

Darwin's speculations on the origin of species convinced him that cross-fertilisation played an important role in keeping specific forms consistent. He rejected the doctrine that the characteristics of a species were static, and was aware from animal husbandry that inbreeding could lead to changes, often deleterious. He thought that natural outbreeding through cross-fertilisation would keep wild species homogenous yet vigorous. Cross-fertilisation would confer an evolutionary advantage by spreading favourable changes throughout a reproductive community. His ideas were contrary to the common supposition that plants were usually self-fertilising, and so every summer Darwin investigated the contribution of insect pollination to the cross-pollination of flowers.[3][4]

Musk orchids (Herminium monorchis) in grassland

In the summer of 1841 Charles and Emma Darwin moved from the turmoil of London to the countryside, to Down House, a quiet former parsonage in the village of Downe. He wrote, "The flowers are here very beautiful".[5] Darwin followed the recommendation of his friend, the leading botanist Robert Brown, and read Das entdeckte Geheimnis der Natur im Bau und in der Befruchtung der Blumen (The Secret of Nature in the Form and Fertilisation of Flowers Discovered[6]).[3] The little known book, published in 1793 by Christian Konrad Sprengel but never translated into English, introduced the idea that flowers were created by God to fulfill a teleological purpose: insects would act as "living brushes" to cross-fertilise plants in a symbiotic relationship. This functional view was rejected and mostly forgotten, as it contradicted the common belief that flowers had been created for beauty, and were generally self-fertilising. For Darwin, the concept of evolution gave new meaning to Sprengel's research into the mechanisms for cross-fertilisation. He welcomed its support for his supposition that cross-fertilisation in flowering plants tended to allow their offspring to avoid possible disadvantages resulting from self-fertilisation,[7] and by 1845 he had verified many of Sprengel's observations.[8]

A favourite walk took the Darwin family to a spot above the quiet Cudham valley, teeming with orchids including Cephalanthera, Neottia, fly orchids and musk orchids. They called this place "Orchis Bank", and the whole family became involved in Darwin's researches.[9] Darwin observed orchids every summer, but in twenty years, only on two occasions (when he noticed butterflies "sucking O. pyramidalis and Gymnadenia") did he see insects visiting flowers.[10] In 1854, Darwin began to work full-time on the origin of species.[11] He examined orchids and counted how often one or both pollinia (pollen masses) had been removed from their flowers, indicating that they had been visited by insects.[12] He experimented with insect pollination to investigate whether, by cross-fertilising field crops such as Fabaceae, they would yield more vigorous offspring, and published letters about his inconclusive results in The Gardeners' Chronicle in 1857 and 1858. He next applied Sprengel's methods to empirical research on orchids.[4][13] Despite delays caused by recurring illness, he made progress on writing his planned "Big Book" on evolution, but when Alfred Russel Wallace's letter prompted joint publication of both of their theories of natural selection in 1858, Darwin quickly wrote On the Origin of Species as an abstract of his theory, published on 22 November 1859.[11] In this book, he gave credence to Sprengel's ideas on the advantages of "intercrossing",[14] and noted: "Many of our orchidaceous plants absolutely require the visits of moths to remove their pollen masses and thus to fertilise them".[15] He introduced his new concept, the process of coevolution, describing the co-adaptation of bumblebees and red clover, and speculating "how a flower and a bee might slowly become, either simultaneously or one after the other, modified and adapted in the most perfect manner to each other, by the continued preservation of individuals presenting mutual and slightly favourable deviations of structure". This was a theme he developed in his orchid book.[16][17]

Head of a moth with its proboscis laden with seven pairs of pollinia from Orchis pyramidalis

During 1861, botany became a preoccupation for Darwin, and his projects became serious scientific pursuits. He continued his study of orchids throughout the summer, writing to anyone who might be able to supply specimens he had not yet examined.[32] Field naturalists, botanists, and country gentry sent specimens from across the British Isles. Darwin also tramped around the countryside with tin cans and biscuit boxes, collecting specimens which his gardeners potted up for him. His family joined in, and neighbours contributed to the research. As he had only a cold greenhouse, a friend on the other side of the village who had a hot-house allowed him to use that, and offered the services of his gardener to look after the delicate specimens. Darwin's aim was to show how the complex structures and life cycles of the plants could be explained by natural selection rather than by the handiwork of God; he saw the huge variety of flowers as a collection of ad hoc evolutionary adaptations.[33] In June he described his examination of bee orchids as a passion,[34] and his findings on insect fertilisation of orchids as "beautiful facts".[35]

There were several replies to Darwin's enquiry in The Gardeners' Chronicle seeking evidence to support his idea that pollen masses attached themselves to a convenient place on an insect's back or head, usually its proboscis, to transport the pollen to another flower. One envelope appeared to be empty when it arrived at Down House, but when he looked further before discarding it he found several insect mouthparts with pollen masses attached.[36] To help their daughter Henrietta convalesce from illness, the Darwins arranged to spend two months in Torquay. Darwin wrote:

I have, owing to many interruptions, not been going on much with my regular work (though I have done the very heavy jobs of variation of Pigeons, Fowls, Ducks, Rabbits Dogs &c) but have been amusing myself with miscellaneous work.—I have been very lucky & have now examined almost every British Orchid fresh, & when at sea-side shall draw up rather long paper on the means of their fertilisation for Linn. Socy & I cannot fancy anything more perfect than the many curious contrivances.[37]

He sought advice on obtaining the exotic South American Catasetum, to see it eject pollen masses, as "I am got intensely interested on subject & think I understand pretty well all the British species."[37] They went to Torquay on 1 July,[38] and Darwin began writing his orchid paper.[39] By 10 August, he feared his paper would run "to 100 M.S. folio pages!!! The beauty of the adaptations of parts seems to me unparalleled ... I marvel often as I think over the diversity & perfection of the contrivances."[40]

Catasetum macrocarpum from Suriname ejects its pollen masses at insects.

The family returned to Downe on 27 August,[38] and Darwin again wrote to the Gardeners' Chronicle appealing for assistance as he was "very anxious to examine a few exotic forms".[41] His requests to the wealthy enthusiasts who had taken up the fashionable pursuit of growing rare orchids brought large numbers of specimens. These would be a test of his theory: previously aspects such as coloration of plants and animals had often been regarded as having no adaptive function. For example, Thomas Henry Huxley was strongly influenced by German idealism and in 1856 had asked if it was "to be supposed for a moment that the beauty of colour and outline ... are any good to the animals? ... Who has ever dreamed of finding an utilitarian purpose in the forms and colours of flowers ... ?" Darwin had, and in the orchids he tackled the most difficult case. His ideas would transform the way naturalists thought about coloration.[42][43]

The completed Orchis paper came to 140 folio pages, and Darwin decided against presenting it at the Linnean Society of London, thinking of publishing a pamphlet instead. He offered the draft to John Murray who agreed to publish it as a book.[44] Although Darwin feared a lack of public interest, he hoped it would serve to "illustrate how Natural History may be worked under the belief of the modification of Species".[45] In discussions with Asa Gray about natural theology, he wrote that "it really seems to me incredibly monstrous to look at an orchid as created as we now see it. Every part reveals modification on modification."[46]

As a popular and acceptable activity, botany had been taken up by many middle class ladies, and Darwin included these botany enthusiasts in his correspondence. On the recommendation of John Lindley, Darwin wrote to Lady Dorothy Nevill, who responded generously by sending numerous exotic orchids, and requested a signed photograph of him to hang in her sitting room next to portraits of her other notable friends, including Hooker.[33][47]

Illustration from Darwin's Linnean Society paper on Catasetum pollination

The orchid book was delayed because of illness, but Darwin continued to "look at it as a hobby-horse, which has given me great pleasure to ride".[48] He was particularly astounded by the long spur of the Angraecum sesquipedale flowers, one of the orchids sent by the distinguished horticulturist James Bateman,[49] and wrote to Hooker "Good Heavens what insect can suck it[?]"[50]

By November, a specimen of the exotic South American Catasetum orchid Hooker had given to Darwin had shown its "truly marvellous" mechanism, by which it shot out a pollinium at any insect touching a part of the flower "with sticky gland always foremost".[51] This plant had astonished botanists in 1836 when Robert Hermann Schomburgk stated that he had seen one plant growing three distinct flowers which usually grew separately and had wrongly been categorised as three distinct genera, namely Catasetum tridentatum, Monachanthus viridis, and Myanthus barbatus. John Lindley had remarked that "such cases shake to the foundation all our ideas of the stability of genera and species." One of Darwin's correspondents told of delight at growing a beautiful specimen of Myanthus barbatus imported from Demerara, then dismay when the plant flowered the next year as a simple Catasetum.[52][53]

In view of this interest, Darwin prepared a paper on Catasetum as an extract from his forthcoming book, which was read to the Linnean Society of London on 3 April 1862.[54] Darwin solved the puzzle by showing that the three flowers were the male, female, and hermaphrodite forms of a single species, but as they differed so much from each other, they had been classified as different genera.[55]

Darwin sent the incomplete manuscript to his publisher John Murray on 9 February 1862, while he was still working on the last chapter. Although anxious that the book might not sell, he could "say with confidence that the M.S. contains many new & very curious facts & conclusions".[56] When the book was printed, he sent out presentation copies to all the individuals and societies who had helped him with his investigations, and to eminent botanists in Britain and abroad for review.[55]

On 15 May 1862 the book was published under the full title of On the Various Contrivances by Which British and Foreign Orchids Are Fertilised by Insects, and On the Good Effects of Intercrossing.[1] In August, Darwin was "well contented with the sale of 768 copies; I shd. hope & expect that the remainder will ultimately be sold",[57] but the book sold slowly and less than 2,000 copies of the first edition were printed. An expanded edition translated into French was published in Paris in 1870, and in 1877 Murray brought out a revised and expanded second edition, with the shortened title The Various Contrivances by Which Orchids Are Fertilised by Insects. This was also published by D. Appleton & Company of New York in 1877, and a German translation was published in the same year. Despite being well praised by botanists, only about 6,000 copies of the English editions had been sold by 1900.[1]

The pollination mechanism of Orchis mascula is given as an example of a mechanism for transferring pollen to insects: the diagram from the book shows all the petals cut away except the lowest petal, the labellum, which extends back to form a tubular nectary below the column.

In the first chapter Darwin described the British orchids he had studied, giving detailed explanations of their various mechanisms for transferring pollen to insects.[59] The first mechanism described is that of Orchis mascula, which serves as an introduction to the explanation of other Orchidaceae. In the upper part of the flower a petal shelters the male organ which has two packages of pollen grains, held together by thin elastic threads. These pollen masses stand side by side and have stalks down to adhesive balls in a cup which keeps them moist and sticky. When an insect lands on the large projecting lower petal, the labellum, and pushes its head and proboscis into the centre of the flower and down to the nectary, it breaks the cup and the adhesive balls attach the pollen masses to the front of the insect. As the insect flies off, each stalk rotates the pollen mass downwards and forwards so that when the insect lands on another flower the pollen masses attached to the insect pass under the male organ and leave pollen on the female organ, achieving cross fertilisation.[59] Darwin envisaged:

A poet might imagine, that whilst the pollinia are borne from flower to flower through the air, adhering to a moth's body, they voluntarily and eagerly place themselves, in each case, in that exact position in which alone they can hope to gain their wish and perpetuate their race.[60]

This is followed by descriptions of the differences in the mechanisms of several other orchids. In Orchis pyramidalis, the adhesive balls are combined together into a strap or saddle shape, which curls round the thin proboscis of a moth or butterfly to attach to it the pair of pollen masses, illustrated in the book by figure 4 showing a moth's head with seven pairs of pollen masses attached to its proboscis.[61]

When an Orchis mascula pollen mass attaches itself to a probe, its stalk slowly rotates downwards.

While the bee orchid showed adaptation for self-fertilisation, its mechanism also enabled occasional cross-fertilisation, creating the biological diversity that Darwin felt was needed for vigorous survival, which could not be provided by self-fertilisation.[62] As an example of "how beautifully everything is contrived", Darwin described how he had found that in Spiranthes flowers the pollen is ready for collection before access is open for the female organ to receive pollen. At Torquay he had watched bees visiting spires of these flowers, starting at the bottom of the spire and working their way up to the topmost flowers. He speculated that if bees moved from top to top of the spires, the pollen clusters they collected from the most recently opened flowers would be wasted as the topmost flowers on the next spike would not be ready to receive pollen. A bee starting at the lowest flowers on the first spire it visited would continue up until it reached flowers that still had their pollen masses to attach to the bee, then would fly to the mature lower flowers on another plant, and fertilise them. By this co-ordinated process, the bee would add "to her store of honey" while perpetuating the flowers "which will yield honey to future generations of bees".[63]

The mechanism by which Catasetum saccatum ejects its pollen is explained by a sectional illustration, shown here to the right of an earlier print showing the plant.

The book moves on to the various foreign orchids Darwin had received from others. His experiments showed that the "astonishing length" of the 111⁄2 inch (290 mm) long nectary hanging from Angraecum sesquipedale flowers implied the need for an as yet unknown moth with a proboscis 10–11 inches (250–275 mm) long to pollinate these flowers in Madagascar. He viewed this as the outcome of a coevolutionary race, writing that "there has been a race in gaining length between the nectary of the Angræcum and the proboscis of certain moths".[64][65] This wastefulness is familiar in modern terms as the idea of an evolutionary arms race, but was disturbing to biologists of the time who believed that adaptations were the outcome of benevolent divine purpose.[66]

Darwin described "the most remarkable of all Orchids", Catasetum, and showed how in these flowers, "as throughout nature, pre-existing structures and capacities [had been] utilised for new purposes". He explained the mechanism in which the pollen masses of the pollinium were connected by a bent stalk or pedicel to a sticky disc kept moist at the back of the flower. When an insect touched an "antenna" projecting from the back of the flower, this released the bent pedicel which sprang straight and fired the pollinium, sticky disc first, at the insect. In experiments, Darwin had imitated this action using a whalebone spring. He vividly illustrated how the flower ejected the pollinium with considerable force: "I touched the antennæ of C. callosum whilst holding the flower at about a yard's distance from the window, and the pollinium hit the pane of glass, and adhered to the smooth vertical surface by its adhesive disc."[67]

Darwin noted that the essential nectar, secreted to attract insects, seemed also in some cases to act as an excretion: "It is in perfect accordance with the scheme of nature, as worked out by natural selection, that matter excreted to free the system from superfluous or injuring substances should be utilised for purposes of the highest importance."[68] Homologies of the flowers of orchids showed them all to be based on "fifteen groups of vessels, arranged three within three, in alternating order". He disparaged the idea that this was an "ideal type" fixed by the Omnipotent Creator, but attributed it instead to its "descent from some monocotyledonous plant, which, like so many other plants of the same division, possessed fifteen organs, arranged alternately three within three in five whorls; and that the now wonderfully changed structure of the flower is due to a long course of slow modification,—each modification having been preserved which was useful to each plant, during the incessant changes to which the organic and the inorganic world has been exposed".[69][70]

Describing the final end state of the whole flower cycle as the production of seed, he set out a simple experiment in which he took a ripe seed capsule and arranged the seeds in a line, then counted the seeds in one-tenth of an inch (2.5 mm). By multiplication he found that each plant produced enough seeds to plant 1-acre (4,000 m²) of ground, and the great grandchildren of a single plant could "carpet the entire surface of the land throughout the globe" if unchecked.[71]

In conclusion, he felt that the book had "shown that Orchids exhibit an almost endless diversity of beautiful adaptations. When this or that part has been spoken of as contrived for some special purpose, it must not be supposed that it was originally always formed for this sole purpose. The regular course of events seems to be, that a part which originally served for one purpose, by slow changes becomes adapted for widely different purposes."[72] He was almost exasperated by the inventiveness of forms in nature; "In my examination of Orchids, hardly any fact has so much struck me as the endless diversity of structure,—the prodigality of resources,—for gaining the very same end, namely, the fertilisation of one flower by the pollen of another."[73] His focus on detail was justified, as "The use of each trifling detail of structure is far from a barren search to those who believe in natural selection."[69] The "contrivances and beautiful adaptations" slowly acquired through slight variations, subjected to natural selection "under the complex and ever-varying conditions of life", far transcended the most fertile imagination. The mechanisms to transport the pollen of one flower or of one plant to another flower or plant underlined the importance of cross-fertilisation: "For may we not further infer as probable, in accordance with the belief of the vast majority of the breeders of our domestic productions, that marriage between near relatives is likewise in some way injurious,—that some unknown great good is derived from the union of individuals which have been kept distinct for many generations?"[74]

In 1867, zoological artist Thomas William Wood drew a speculative illustration of a then unknown moth pollinating Angraecum sesquipedale, based on Alfred Russel Wallace's descriptions.[84]

Although the book contradicted the prevailing natural theology and its teleological approach to design in nature, the Saturday Review thought that it would avoid the angry polemics aroused by On the Origin of Species. The Literary Churchman welcomed "Mr. Darwin's expression of admiration at the contrivances in orchids", only complaining that it was too indirect a way of saying "O Lord, how manifold are Thy works!" (Psalm 104:24)[83] Darwin regarded these theological views as irritating misunderstandings, but wrote to Asa Gray describing his approach as a "flank movement on the enemy". By showing that the "wonderful contrivances" of the orchid have discoverable evolutionary histories, Darwin was countering claims by natural theologians that the organisms were examples of the perfect work of the Creator.[78][85]

There was considerable controversy surrounding Darwin's prediction that a moth would be found in Madagascar with a long proboscis matching the nectary of Angraecum sesquipedale. An anonymous article in the Edinburgh Review of October 1862 by George Campbell, 8th Duke of Argyll, argued that Darwin's wording implied purpose, and concluded that "We know, too, that these purposes and ideas are not our own, but the ideas and purposes of Another." He considered Darwin's explanations the "most unsatisfactory conjectures", and raised obscure metaphysical objections while supporting a kind of creative evolutionism. Emma Darwin thought that although Argyll was "quite opposed" to Darwin's views, "he praises the Orchids in such an enthusiastic way that he will do it a good turn". Darwin was delighted to find that a well written article "smashing" Argyll's review was by one of Darwin's own nephews.[86]

Argyll went on in his 1867 book The Reign of Law to cleverly ridicule Darwin's ideas, particularly the prediction of a moth in Madagascar with a proboscis 10–11 inches (250–275 mm) long.[86] He believed that adaptations showed divine purpose, not a mindless evolutionary arms race.[66] In his response Creation by Law later that year, Alfred Russel Wallace produced a detailed explanation of how the nectary could have evolved through natural selection, and stated that he had carefully measured moths in the British Museum, finding that the proboscis of Macrosila cluentius from South America was 91⁄4 inches (235 mm) long, and the proboscis of Macrosila morganii from tropical Africa (since renamed Xanthopan morganii) was 71⁄2 inches (190 mm) long. An enquiry raised in 1873 was answered by Darwin's friend Hermann Müller, who stated that his brother Fritz Müller had caught a sphinx moth in Brazil with a proboscis nearly 10 inches (250 mm) long. Darwin's anticipation was fully met in 1903, when a subspecies of Xanthopan morganii was found in Madagascar with a proboscis about 12 inches (300 mm) long, and was named Xanthopan morganii praedicta to celebrate this verification of a testable prediction made by Darwin on the basis of his theory of natural selection.[84][87]