Darwin's Backyard

by James T. Costa

  Great laurel rhododendron (Rhododendron maximum) flowers. Darwin studied the up-curved stamens and pollinator “gangway” of rhododendron and a host of other flowers. Photograph by the author.

  Sprengel was Darwin’s initial guide, and one of the plants he discussed was the common barberry (Berberis). Barberries are the often-disparaged hardy plants associated with uninspired plantings at malls and gas stations (further disparaged by knowing biologists because these are aggressively invasive plants in North America, and host of the parasitic stem rust fungus that attacks wheat). But they have their charms, as Darwin appreciated: barberries provide one of the best examples of spring-action stamens. Small clusters of yellow flowers dangle from slender petioles. As the flower matures, the stamens cock back like catapults, loaded with pollen. At the slightest touch by a bee the stamens spring, showering the visitor. Darwin credited the German botanist Joseph Gottlieb Kölreuter (1733–1806), of Karlsruhe, with showing this mechanism as early as 1788. (In fact today Kölreuter, more than Sprengel, is considered the father of insect pollination biology.)

  Darwin realized that the maturation of male and female parts of the flower were timed to reduce the chances of self-pollination, and also served as a device to control the timing of pollen pickup and delivery by insects. That’s what happens in salvia: the stamens ripen first, and dab visiting bees with pollen via a lever mechanism. The immature pistil is held out of the way at this stage, but as the flower ages the stamens wither while the pistil has a growth spurt, elongating dramatically to hang down at the front of the gangway. Pollen-bearing bees visiting flowers at this stage need to squeeze under the pistil, the stigma scraping pollen from the bee’s back. Darwin marveled at the contrivance: “I can no more doubt the final cause [purpose] of this structure than I can of a certain mouse-trap.”17 He marveled too at a rather different and bizarre form of pollination found in certain arums. This group has an inflorescence characterized by a spadix—a distinctive column or spike crowded with tiny flowers—and a leafy bract called a spathe, which often surrounds the spadix like a hood or cape. The common Peace lily (Spathiphyllum cochlearispathum) of florists’ shops is a good example of the general morphology, with a spadix hooded by a snow-white spathe. Darwin was intrigued by a common British woodland species, Arum maculatum, variously called lords-and-ladies, cuckoo-pint, friar’s cowl, or Jack-in-the-pulpit.

  In these arums, the purple, poker-shaped spadix is partly hooded by a green spathe. Unlike the spadix of many species, the part that is visible does not actually bear the flowers. That’s where things got interesting for Darwin. Lower down, the spadix disappears into a bulbous chamber formed by a swelling of the spathe base. The spadix shaft in the chamber bears three types of flowers, each arranged in a ring around the shaft: at the very bottom are female flowers, which produce nectar, above which is a ring of male flowers, and above them at the top of the chamber and practically blocking its narrow neck is a ring of sterile flowers with bristly filaments. These filaments prevent large insects from entering, but it had long been known that small ones, especially certain flies, can get past them and into the secret chamber. Like many arums this plant produces a scent repugnant to our nose—one author described it as “foul and urinous”—but irresistible to flies, its main pollinators. The attraction is all the greater because these remarkable plants can generate heat through a process called thermogenesis, which helps volatilize the odorous compounds and provides a cozy refuge for visiting insects. (The early-blooming North American arum skunk cabbage, Symplocarpus foetidus, can generate enough heat to melt snow.)

  Leading botanical authorities of Darwin’s time assumed the hapless flies flew into the chamber and never saw the light of day again. Darwin assumed otherwise since these plants are not carnivorous. In March of 1842, on a visit to see his father and sisters at Shrewsbury, he dissected the bulbous spathes of a few specimens and found 30 to 60 small midges trapped inside. Many were indeed dead, but others were alive, pollen-dusted and crawling a bit groggily around inside. Would they have been doomed had he not opened the chamber? In Effects of Cross and Self Fertilisation in the Vegetable Kingdom, published 34 years later, he explained:

  Darwin investigated the pollination biology of wild arum (Arum maculatum) in 1842, showing that this plant entices unwary midges into the bulbous chamber below the spadix, releasing them once they are doused in pollen. Drawing by Leslie C. Costa.

  In order to discover whether the living ones could escape and carry pollen to another plant, I tied in the spring of 1842 a fine muslin bag tightly round a spathe; and on returning in an hour’s time several little flies were crawling about on the inner surface of the bag. I then gathered a spathe and breathed hard into it; several flies soon crawled out, and all without exception were dusted with arum pollen. These flies quickly flew away, and I distinctly saw three of them fly to another plant about a yard off; they alighted on the inner or concave surface of the spathe, and suddenly flew down into the flower.18

  Looking inside, he confirmed that the flies had transported pollen. What’s going on with this dipteran chamber of horrors? The ring of filaments of the sterile flowers at the top of the chamber forms an insect trap. Attracted by the odor within, the flies squeeze their way through the barrier, but finding their way out again is not so easy. This arum is protandrous, with male flowers maturing first: by the next day the large anthers of the male flowers ripen and shed lots of pollen, covering the duped flies as they walk around the chamber trying to escape. Some die in the process, their bodies littering the floor of the chamber. Within about 24 hours the filaments blocking the entrance wither and the pollen-covered survivors fly free at last . . . only to be quickly duped by another arum. By that time the male flowers have faded and it’s the female flowers’ turn to mature. Their stigmas become receptive just as the air is filled with the groggy pollen-dusted flies. Chances are small that they’ll reenter the same flower that duped them the first time, so when they’re conned again they are likely to facilitate cross-pollination.

  A different form of protandry that Darwin studied is found in the common foxglove (Digitalis purpurea), a perennial garden favorite with its spike of large, deep-throated purple spotted flowers. This species is mainly visited by large bumblebees, and has a neat trick to ensure cross-pollination. A mature plant has from around 10 to dozens of flowers arranged in a spiral up the stem, at the top of which new flower buds are continually produced. Being protandrous, in a given well-developed spike the lowermost flowers are older and so have passed into the female phase, while the middle to upper flowers are still male. Darwin noticed that bumblebees tended to start at the bottom of the spike of one individual (female flowers) and work their way up, picking up pollen from the upper (male) flowers before leaving the plant to find another. At the next plant they go to the lower, female, flowers first again, setting the stage for cross-pollination. (More recent studies found that the female flowers also produce more nectar than do male flowers, a big incentive to ensure the bees start there.)

  Ever the experimentalist, Darwin wanted to test if these plants depend on crossing for good seed set and vigorous growth. The opportunity to work with large wild populations presented itself in 1869 while on a family holiday in the scenic coastal town of Barmouth, Wales, on Cardigan Bay. This holiday was meant to be more recuperative than usual for him, since earlier that year he took a serious tumble off of his horse and was lucky not to have been seriously injured or killed. As it was he was pretty sore, but the peace and quiet of field work at the seaside worked wonders. He found a spot thick with foxgloves overlooking the harbor and estuary and set up an experiment: “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.”19 That wo
uld have been a peculiar sight for passing day-trippers, had any spotted a man out in a field seemingly throttling a netted foxglove plant. The little study bore fruit in more ways than one: he found that of the 92 flowers on the netted plant (including the 12 he had hand-pollinated), only 24 seed capsules were produced (and just two of those were full of seeds). All around the plants left uncovered were, in contrast, chock-full of seeds.

  He carefully collected the seeds, keeping those from self- and cross-pollinated flowers separate. On returning home he germinated them in his greenhouse and, once they were large enough, transferred the seedlings to the garden. The following summer he measured the flower spikes produced by the surviving plants and found a whopping difference in vigor: the cross-pollinated plants grew to 51.33 inches on average, while the surviving self-fertilized plants were 30 percent smaller, at 35.87 inches. (Mortality was higher with self-pollination too.) This study was yet another striking demonstration of the power of cross-fertilization, another brick in the evidentiary edifice he was building.

  To Cross or Not to Cross

  Darwin realized that some plants self-fertilize, some even frequently, but he was convinced that most are as indifferent to their own pollen as they are to pollen from distant genera or families. He had little concept of why, but today we understand that self-incompatibility, as the phenomenon is called, is controlled by a simple genetic mechanism involving one or more compatibility genes. These genes consist of many different variants (alleles) in the collective gene pool of the species, but in good Mendelian fashion each individual plant contains just two alleles, one copy of each gene inherited maternally and the other paternally. The self-incompatibility genes have so many variant alleles that individuals are nearly always heterozygous—containing dissimilar variants of the gene obtained from each parent, as opposed to identical variants (in which case they would be homozygous for that gene). In fact, if a pollen grain landing on a stigma possesses the same compatibility allele or alleles as those of the plant bearing the stigma, it will fail to develop a pollen tube and thus cannot fertilize the flower. Since self-produced pollen has by definition the same alleles as those found in ovules of the same individual, self-fertilization is prevented.

  This is a basic description of self-incompatibility, but bear in mind that things are more complex than that in the botanical world. While exclusive selfing, as self-fertilization is called, may be rare, in lots of species some degree of selfing is not only tolerated, but ensured. Naturally, Darwin was intrigued, and in May 1862 he wrote Hooker about his investigation of a phenomenon later dubbed cleistogamy, production of tiny specialized flowers that self-pollinate. Nearly half of all flowering plant species exhibit “mixed-mating,” producing both selfed and outcrossed progeny, and many plant groups even sport specialized flowers that exclusively self-pollinate right in the bud, not even bothering to open. These so-called cleistogamous (closed-breeding) flowers are far more common than even the keenest gardeners likely realize: a comprehensive review conducted in 2007 found that nearly 700 species distributed among 228 genera and 50 plant families bear cleistogamous flowers. Among them are a host of garden favorites: many violets, orchids, sorrels, and legumes among others produce cleistogamous flowers along with their showy (chasmogamous—open-breeding) flowers. You can be excused if you haven’t noticed the cleistogamous ones—not designed for visibility since pollinators are irrelevant, they tend to be small and bud-like, produced on pale stems close to the ground. They either lack petals altogether or the petals are reduced to mere scales, nectaries are dispensed with, and even the stamens and pistils are rudimentary.

  At the time, Darwin was cogitating over insect pollination, plant crosses, insectivorous plants, orchids—anything but working on his domestication book. “I have been amusing myself by looking at the small [cleistogamous] flowers of Viola . . . what queer little flowers they are,” he wrote Hooker.20 He was trying to figure out how the pollen produced in the closed flower gets transferred to the stigma, and had written to the ever-obliging Daniel Oliver at Kew for help. With correspondents like Oliver he investigated seed production by cleistogamy in violets and other flowers, and delved into the literature to see how widespread the phenomenon was. Fifteen years after that letter to Hooker he dedicated an entire chapter in Forms of Flowers to this curious phenomenon, including the results of many experiments. He concluded correctly that there is a twofold advantage to cleistogamy. When regular pollination fails due to adverse conditions like bad weather or pollinator paucity, the cleistogamic flowers act as an insurance policy, selfing to ensure seed production. Second, they can produce an abundance of seeds with very little investment since the flowers are small, bud-like, and lack nectar.

  The idea of small, closed, selfed flowers as a reproductive insurance policy made sense to Darwin, but selfing by regular flowers strutting their floral stuff to entice pollinators was puzzling. The latter seemed to be especially common in leguminous plants, a group that includes peas, beans, and their relatives—a convenient group for study. In October 1857 he wrote a letter to the Gardeners’ Chronicle describing the lever-action mechanism of kidney beans: the style is curved in a left-hand loop (“like a French horn”) within the modified petal called the keel. The stamens are housed within this looped tube as well. The two lower petals protrude at the bottom and present a landing platform for visiting bees. Their weight depresses these petals, and the stigma at the tip of the style pops out of its looped tube. Darwin noted that just below the stigma the style has a brush of fine hairs that is moved backward and forward each time a bee lands on the flower. Like a botanical pipe cleaner, the brush sweeps shed pollen out of the tube, gradually pushing it onto the stigma. “Hence the movement of the pistil indirectly caused by the bees,” Darwin wrote, “would appear to aid in the fertilisation of the flower by its own pollen.”21 He mimicked the effect of the bees by gently pulling the wing-petals, and noticed that, at the same time, a visiting insect would get a dose of pollen too. Some pollination thus likely occurs by crossing in addition to selfing, he surmised. He tested his idea with an enclosure experiment. In each of three replicates he covered two groups of flowers with netting. One group he left undisturbed, but once a day he reached under the netting of the other group and manually tugged on the protruding lower petals of each flower, simulating a landing bee. Then he waited for seed set. “Not one of the undisturbed flowers set a pod,” he reported, “whereas the greater number (but not all) of those which I moved . . . set fine pods with good seeds.”

  In an 1858 follow-up article he gave the results of a scaled-up version of the experiment. The uncovered plants were nearly three times as productive as the covered ones. Darwin found it remarkable that even though the beans self-pollinate, they rely on insect agency to do so—leading him back to Knight’s Law and his conviction that they are cross-pollinated at least occasionally by bees. In the long haul of ecological and evolutionary time, even rare outcrossing is all it takes to reinvigorate the population and ensure continued fertility and adaptability. Darwin hypothesized that selfing eventually leads to reduced pollen potency, whereupon pollen from other individuals—nearly always present at low concentration owing to the movement of the bees—will be the only pollen that can fertilize. The reinvigorated progeny can then get away with selfing again for a period of time. We don’t quite look at it that way today—it’s not that the potency of pollen declines, but rather that too much selfing permits the expression of deleterious recessive genetic traits. But his instinct was basically correct that cross-fertilization is where it’s at, evolutionarily speaking. To Darwin this seemingly simple idea had far-reaching implications, from the origin of sexes to coadaptation to what we would call ecological interconnectedness in the web of life.

  One of Darwin’s most famous examples of interconnectedness found in On the Origin of Species stems, in fact, from a pollination experiment. Indeed, this work on bees and red clover may be the earliest discussion of an ecological food chain in the scientifi
c literature. Insofar as the food chain idea underpins the seminal concept of ecological food webs, Darwin’s clover experiment is foundational in the history of the science of ecology. He described a food chain based on flower-visiting bees: based on experiments, he said, “I have found that the visits of bees, if not indispensable, are at least highly beneficial to the fertilisation of our clovers.” Insofar as bumblebees are the main visitors to common red clover and heartsease (violets), “I have very little doubt, that if the whole genus of humble-bees became extinct or very rare in England, the heartsease and red clover would become very rare, or wholly disappear.” But the chain of influence extends further than that:

  The number of humble-bees in any district depends in a great degree on the number of field-mice, which destroy their combs and nests . . . Now the number of mice is largely dependent, as every one knows, on the number of cats; and Mr. Newman says, “Near villages and small towns I have found the nests of humble-bees more numerous than elsewhere, which I attribute to the number of cats that destroy the mice.” Hence it is quite credible that the presence of a feline animal in large numbers in a district might determine, through the intervention first of mice and then of bees, the frequency of certain flowers in that district!22