A Garden of Marvels

by Ruth Kassinger

  Darwin rushed the Origin into print, spurred by the knowledge that Alfred Russel Wallace was readying his own manuscript proposing a very similar theory. After publication, he was swamped with correspondence about the book and overwhelmed by the constant need to answer questions about it. In 1860, he turned to a study of plants, and orchids in particular, not only for psychological relief, but also to collect more evidence for his theory. In his book on fertilization in orchids, The Various Contrivances by Which Orchids Are Fertilised by Insects (1862), he would write, “It is an almost universal law of nature that the higher organic beings require an occasional cross with another individual. . . . Having been blamed for . . . propounding this doctrine without giving ample facts in [the Origin], I wish here to show that I have not spoken without having gone into details.”

  Wild orchids grew in profusion in the countryside near Darwin’s home southeast of London, and he began digging them up to transplant in his garden. After fully investigating British species, he branched into the more elaborate tropical ones. Expensive glass conservatories had become a status symbol among the wealthy in nineteenth-century Britain, and gathering a collection of exotic orchids was an upper-class hobby. Some aristocrats went so far as to hire a collector to scour the tropics for them. The socially well-connected Darwin reached out to those who might send him unusual specimens.

  Although he accumulated dozens of species, these were only a tiny fraction of the Orchidaceae, one of the largest botanical families. About twenty-five thousand species inhabit every ecological niche, including underground, of every continent except Antarctica. Orchid flowers are astoundingly diverse: They look like jugs, slippers, bees, strange sea anemones, spiders, frizzled ribbons, ducks in profile, long-eared donkey heads, as well as jasmine, crocus, violets, and pea flowers; they come in every color and color combination except true black; and they can be scentless or stink of rotting meat or waft intoxicating perfumes. The plants range in weight from less than an ounce to, in the case of the Grammatophyllum papuanum, a ton. Orchids seemed to fly in the face of evolution by natural selection. How could such fanciful structures have anything to do with the tough business of survival? As Thomas Huxley, Darwin’s friend and a chief evangelist for his theory, asked, “Who has ever dreamed of finding an utilitarian purpose in the forms and colours of orchids?”

  Darwin did, and he made a convincing case that orchids are a striking example of “descent by modification,” an iterative process in which a small adaptation leads to a slight improvement in successful fertilizations, increasing the numbers of offspring having that adaptation and spreading the adaptation throughout a population. Despite the variety in orchids’ appearances, all are built on a basic anatomical plan: three sepals, three petals (one of which is the labellum, or lip, where the pollinator lands), and the column. The column is a single, fingerlike organ that is home to both the stigmatic surface and packets of bright yellow pollen (pollinia) that protrude outward from atop slender stalks. The orchid’s strategy is to attract an insect to enter a flower in such a way that it is tagged with packets of pollinia. The stalks and their packets adhere to a body part—head, abdomen, back, or proboscis—of the visitor. Within seconds, the stalks wilt or twist in such a way that when the insect enters another flower, the pollinia are precisely positioned to miss the male portion of the column and contact the sticky stigmatic surface, where they detach. Darwin realized that every seemingly useless ridge and fold of the flowers, all their colors and markings, their scents, and all their odd projections have been shaped by natural selection to serve a reproductive function.

  So convinced was he of this arrangement that he confidently offered a prediction of the existence of an exceedingly strange and unknown moth. A friend had sent him several specimens of the star orchid of Madagascar, Angraecum sesquipedale, whose six-inch flowers have waxy white petals, a strong, spicy fragrance, and, at their base, a “green, whiplike nectary of astonishing length.” What insect, he wondered, could possibly reach the nectar at the bottom of this narrow, curving, twelve-inch-long nectary? He tried maneuvering needles and bristles into the flower, but with no success. Only by poking a wire down the full length of the spur was he able to reach the nectar. Given that the flower is white and has a pungent smell, he knew that the pollinator had to be a moth, and that it would have a tongue a full foot long. He also predicted that the moth would be large; he had found he had to exert a significant pressure to push down on a stigma in order to drop off the pollinia.

  His prediction was ridiculed by entomologists who had never seen a moth with a tongue anywhere near that length, but in 1903 just such a moth was discovered. The Angraecum sesquipedale orchid is pollinated by a brown hawk moth with a five-inch wingspan and a twelve-inch tongue. The tongue is usually curled up in a tight coil, but when the moth sees or smells its particular flower, liquid streams into the interior of its tongue, unwinding it like a party horn. The moth was named Xanthophan morganii praedicta.

  The orchid Angraecum sesquipedale and its pollinator Xanthophan morgani praedicta.

  Darwin thought orchids always provided a payoff to their pollinators in the form of nectar, and although he had heard of reports of nectarless flowers, he didn’t give them credence. Surely, the insects would learn not to waste their time visiting rewardless species. Any insect able to spot the species with empty flowers and avoid them would leave more progeny and spread its lie-detecting ability throughout the species.

  In this instance, Darwin was wrong, underestimating the precision of orchid mimicry. About one-third of all orchid species are cheaters, promising lunch but delivering nothing. There are orchids that mimic the appearance of nectar-filled flower species of completely unrelated genera. Donkey orchids, as John Alcock demonstrates in his delightful book, An Enthusiasm for Orchids: Sex and Deception in Plant Evolution, have evolved to look astoundingly like members of the pea family. Pink Enamel orchids appear to have five identical shiny, bright pink petals, and look like a number of meadow wildflowers that offer nectar. These orchids may not fool all the bees all the time, but they don’t need to. Inside their pollinia are millions of tiny pollen grains, far more than in a pea flower’s anthers. Orchids need dupe only a few bees to arrange transportation for their bountiful pollen. Meanwhile, they preserve their energy by forgoing the manufacture of nectar.

  The bee orchids (members of the Ophrys genus) are equally deceitful, but instead of a false promise of food they dangle the possibility of sex. An Ophrys labellum has evolved to resemble the backside of a female bee whose head appears to be plunged into the flower. The male bee, spotting what looks like a bulbous, furry bee bottom and getting whiffs of a specific fragrance that telegraphs “receptive virgin female who is exactly your type,” pounces and tries to copulate. (If you want to take a walk on the wild side, you can find clips of bee and Ophrys pseudocopulation on YouTube.) After about a minute of unsatisfactory lovemaking to a flower, he gives up and flies off in search of a more satisfying partner, unwittingly carrying away orchid pollen.

  Research shows that he flies some distance away before trying again. Why doesn’t he just try the next flower on the next branch? The answer is not because the embarrassed bee wants to avoid any witnesses to his previous humiliation. The reason lies in the evolution and complexity of orchid fragrance. Each Ophrys species has evolved to produce the precise mix of hydrocarbon compounds that imitates the dozen or more compounds produced by the female of only one pollinator bee species. In this way, the orchid ensures that the frustrated male bee will seek another blossom (disguised as a bee) of its own species, carrying its pollen only to where it can be effective. But if the frustrated male bee were to move only to another flower of the same plant, the orchid would not have accomplished its goal of cross-pollination. So, the orchid has two other tricks up its flower to ensure that the lover moves farther on. Researchers at the Institute of Zoology in Vienna have discovered that after Ophrys sphegodes has been pollinated by its pseudocopulating pollinator be
e, the flower immediately produces a new fragrance compound that is the faithful duplicate of farnesyl hexanoate, the compound that female bees emit after they have successfully mated. A whiff of that pheromone in the vicinity quickly sends the male bee on his way. In other orchid species, the male bee can sense subtle variations in the mix of the sex-related compounds produced by individual plants—perhaps a few more molecules of compound number 8 and several fewer of compound number 12—and he avoids the flowers of the plant that have already proved so disappointing.

  Why doesn’t natural selection make history of males that waste their time trying to tryst with a flower? It appears that the male bees are caught in a bind. Those who are quickest off the mark and beat out their rivals for real virgin female bees are most successful in passing their genes to the next generation. Since there are far more virgin bees than deceitful orchids, on balance male bees who make the occasional mistake of mating with a flower prevail over those who dillydally and discriminate. The orchid is quite satisfied by the amorous bee. It has attracted an avid pollinator highly likely to carry its pollen to exactly the right flower at minimal cost, just a sexy skirt and the right perfume.

  twenty-six

  Scent and Sex

  Darwin couldn’t appreciate the exquisite precision of orchids’ mimicry of scent. It wasn’t until the mid-1970s that scientists were able, with the use of a gas chromatograph/mass spectrometer, to tease apart the individual organic chemical compounds of fragrance and measure the volumes of those compounds. While a rose by any other name still smells as sweet, horticultural scientists now can define every molecule that creates that sweetness. There is no longer anything ineffable about the fragrance of a rose or an orchid, or, as I learn from Professor David Clark at the University of Florida, a petunia.

  I meet up with Dave in August in one of the experimental greenhouses behind the building that houses his office and labs. Dave sounds like Appalachia and looks like a man who spends his time with old-fashioned petunias; he’s a cheerful man with a healthy pink complexion. He heads a research group at the university dedicated to improving floral and vegetable crops through a combination of biotechnology and conventional breeding. Petunias are a major focus of his work, and we start by looking at the plants he’s working on. Petunias can’t take the heat of August in Florida, so inside the greenhouse the air is cooled to about 80 degrees. I’m expecting a glorious display, but all the flowers trembling slightly in the light breeze have white petals and long, narrow throats. They’re nice, but hardly the first plant I’d put in my shopping cart at the garden center.

  Aesthetically, Dave’s petunias may not be an exciting group, but scientifically they are. In the last decade or so, the garden petunia has become a “model species,” a species that researchers use to study the biology of a broader group of organisms. The petunia is in the same family (Solanaceae) as tomato, potato, tobacco, eggplant, and pepper, plants that constitute the most economically valuable group of agricultural plants other than row crops like corn, wheat, and soybeans. What scientists learn by delving deeply into petunias can improve crops that nourish the body as well as the soul.

  The petunias Dave grows are Petunia x hybrida cv “Mitchell Diploid,” the equivalent of the medical researcher’s white mouse. Much of the “Mitchell’s” genome has been decoded, making it easy to silence or add genes and explore their function. “Mitchell,” like the wild Petunia axillaris it closely resembles, has big flowers that produce a lot of volatiles. (Volatiles are substances that easily change from liquid to vapor: all the better to smell you, my dear.) This makes the variety an ideal subject for investigating the biochemistry of fragrance.

  The scent of “Mitchell” is made up of a dozen or so complex compounds, including clove oil, a sort of medicinal root beer scent, wintergreen, and rose oil. Rose oil is hands-down the most important volatile in the cosmetics and perfume industries. Sad to say—and no surprise to anyone who has been given a bouquet of hothouse roses or bent over to sniff a garden rosebush—the genes that code for rose oil, while still in the genome, are often no longer expressed. The oil used in expensive eye cream or Chanel No. 5 comes from cabbage roses and damask roses, which are cultivated primarily in Bulgaria and sell for about four thousand dollars per pound. It isn’t that commercial rose breeders have purposefully eliminated scent from roses, but in selecting and breeding for color, form, longevity, disease resistance, and a host of other traits, scent has been inadvertently lost.

  None of the edible Solanaceae have flowers with appreciable fragrance, but you will find fragrance compounds in their fruit. The same molecules that drift into the air to draw pollinators to petunias reside in eggplants, peppers, and tomatoes. What are fragrance molecules doing there? Fruits evolved to attract animals that disperse their seeds, and sugars and proteins are a significant part of the attraction. Some of those proteins contain essential amino acids, “essential” meaning that animals cannot synthesize them and so must eat them to survive. Phenylalanine (fen-l-AL-uh-neen) is one such amino acid. It is also a component of many compounds in petunia fragrance and in tomatoes. In fruits, color says “I’m ripe” and fragrance says “I’m good for you.”

  Of course, it is not the scent per se of the tomato that draws you to eat one, but the taste you anticipate. Taste is in large part a function of fragrance because our tongues perceive only the chemical compounds of sweet, sour, bitter, salty, and umami or savory flavors. (Pinch your nose closed, and you won’t be able to tell the difference between a puree of strawberry and a puree of pineapple.) One of the components of a tasty tomato is rose oil. Dave’s lab helped identify the gene for rose oil in an heirloom tomato and managed to engineer it into “Mitchell” petunias. The petunia flowers came up smelling like roses.

  This snipping and splicing of genes creates a transgenic or genetically modified (GM) plant. In the mid-1980s and 1990s, it seemed that the future of agriculture would be in GM plants. Scientists had visions of stitching vitamins, amino acids, and all sorts of other goodies into the genomes of fruits and vegetables. The breeding limitations imposed by the genetic differences that make a species a species were going to be history. Plant breeding would take place in petri dishes. “Lots of traditional breeders happened to retire at that time,” Dave says, “and were replaced with molecular biologists who were cloning genes and creating plants that jumped natural species barriers.”

  It didn’t work out that way. Some major crops were indeed engineered to resist herbicides, viruses, insects, freezing, and drought, but genetically manipulated food, it turned out, makes some people very uneasy. In the United States, regulations were put in place to help ensure that transgenic crops don’t compromise health and are safe for the environment. Whether the regulations achieve these goals and whether GM crops really hold any danger is a matter of much debate, but there’s no doubt that the expense of the research and the documentation required to meet regulations at various federal and state agencies is significant. According to the World Bank, the cost of preparing a regulatory application for one transgenic corn variety ranges from $6 million to $15 million. To gain approval of even a nonedible crop, say a pink “Rose Perfume” Wave petunia that has a tomato gene inserted to enhance its scent, Dave tells me, would cost a breeder a million dollars—and that would be the expense for just that particular pink. The breeder would have to get approvals for each of the twenty-plus colors in the Wave series that contained the spliced gene.

  “The cost of the R&D and the regulations can pay off if you’re talking about millions of acres and billions of dollars,” Dave says. “But the market value of the entire petunia crop in the U.S. is only three or four hundred million dollars, and that’s at the retail level. Plus, the average market life of a petunia variety is five, six, maybe seven years. Then, consumers want something different. Anyhow, what’s the dollar value of a pink petunia with a better scent? You just can’t get stakeholders interested.” In general, transgenics only make sense for commodity crops. Improvin
g flowers and vegetables is still the province of conventional breeders.

  Scientists, however, have changed conventional breeding, now that they are armed with the tools of molecular biology and data from genomic sequencing. Say you are a breeder and you have a patent on a white petunia with a minty fragrance and a striking pink-and-green-star petunia with no fragrance. It occurs to you that if your pink-and-green petunia had a mint scent, it would sell well. Thanks to Dave’s lab, you know that the white petunia makes ten fragrance compounds, including minty alcohols, and in what proportions. You also know which of its genes are responsible for making each of those scents and where on the petunia chromosome each of those genes lie. Now, in your lab, you can snip out those genes with enzymes and multiply them with recombinant DNA technology. Then you can insert those genes into bacteria of the genus Agrobacterium. Finally, you infect your pink-and-green petunias with the bacteria, which transfer fragrance genes.

  Once you are satisfied with your transgenic petunia, you do not plant it. Instead you grind up its leaves, subject them to DNA analysis, and see roughly where those white-petunia fragrance genes have landed in the green-and-pink petunia genome. Then you can start creating the old-fashioned way, that is, by transferring pollen from white petunias to stigmas of pink-and-green-star petunias (and vice versa) and then collecting seeds from pollinated flowers. In the past, you would have had to plant thousands of seeds, then water and fertilize and devote air-conditioned greenhouse space to them for two years until the plants flowered and you could discover which hybrids looked beautiful and smelled minty. Today, however, you need only wait five weeks for the seeds to sprout, grind up a little leaf from each seedling, and conduct DNA analysis to see which individuals have the DNA that matches your lab-created transgenic. You still have to grow those individuals to see which branch most prolifically, have the most blossoms, set the most seeds, etc., but you have reduced the time and cost of development radically.