Darwin's Backyard

by James T. Costa

  He wasn’t the only one. William Tegetmeier (1816–1912), editor of The Field, the Farm, the Garden: The Country Gentleman’s Newspaper, was an authority on poultry and fancy pigeons, subjects on which he and Darwin had corresponded for a few years. Darwin was surprised to discover that his correspondent was also something of a bee fancier. Tegetmeier regularly exhibited new bee hive designs at Entomological Society meetings, and came up with the idea of giving bees blocks of wax in various configurations to better understand their building behavior. Tegetmeier’s ingenuity would prove to be helpful to Darwin, but for now he was still struggling to master the geometry of bees’ cells. His brother tried to help—for all of his idleness Erasmus certainly had a flair for mathematics. But Charles, who candidly lamented that his “noddle is not capacious enough to retain or comprehend Mathematics,” may have found that ’Ras obscured rather than clarified the matter by sending him calculations like this: “The obtuse ∠ at c is in the plane of the paper [therefore sign] Kc = radius of passing thro’ obtuse ∠s Kb = 12 distance of centers = distance from center of sphere to rhomb.”12 Whew! Darwin may have been feeling more obtuse than the angles here.

  He fared better with his old friend William Hallowes Miller, a crystallographer and professor of mineralogy at Cambridge. Who better to help him understand bee geometry, “the most difficult of all instincts to comprehend on my theory,” as he lamented to Hooker, than someone whose stock-in-trade is planes and angles? Darwin left a long list of questions with Miller, and after a false start his friend got back to him with encouraging results. Miller even sent him instructions for constructing a paper model of a bees’ cell based on a rhombic dodecahedron—a 12-sided polygon where each facet is a 4-sided rhomb. If certain axes of this dodecahedron were elongated, Miller said, the structure would take the familiar form of a bee’s cell.

  Darwin soldiered on. In the weeks before Wallace’s Ternate essay arrived at Down House he oscillated between triumph and despair. In early May he declared to his eldest son Willy, then staying at his tutor’s to prepare for his entrance exams for Cambridge, that he thought he had “settled the theory of Bees-cells.” A couple of weeks later, however, he wrote again saying that he had “come to heavy grief” over bees’ cells. The cause was Swiss naturalist François Huber, author of Nouvelles Observations sur les Abeilles (New Observations on Bees), first published in 1792. In a later edition, Darwin read that Huber, who made significant contributions to the study of bees despite being blind from an early age, suggested that the walls of certain cells were already angular before other adjoining cells were constructed. Alarmed, Darwin wrote in the margin “fatal to my theory.” His only hope was that Huber was wrong.

  Darwin would have to see for himself, using “a grand observatory Hive” lent by a neighbor. “I am going to watch,” he declared to Willy, “for I cannot bear throwing up all my work.” That’s the kind of stick-to-itiveness so typical of Darwin. His friend John Innes, the local vicar, helped out, and barely a week later he had thrown himself into apiculture with gusto, making quite an impression on Emma: “Only think how bold Papa has become,” she wrote Willy, marveling how “he hived a swarm of bees all himself . . . he & Mr Innes go about wonderful figures in their bee dresses with white veils on their hats.”

  This was one area of investigation where Darwin was playing catch-up, unlike so many research topics where he was in the vanguard from the get-go. Beekeeping was an ancient art form that was then experiencing much innovation in hive designs, methods of honey extraction, and other husbandry techniques. It was difficult to become an apiculturist overnight, and though Darwin tried in his usual ebullient hands-on way he also relied heavily upon the assistance and advice of friends more expert than himself, especially Waterhouse, Innes, and Tegetmeier. About the same time he was donning bee suits with Innes in early June 1858, Tegetmeier suggested giving the bees unworked wax as a way to observe the earliest stages of cell construction. If these start out as concavities, little bowl-shaped impressions like you would get if you pressed the curved bottom of a test tube into soft wax, that would be consistent with his and Darwin’s conviction that the bees initially construct cylindrical cells that are subsequently modified into hexagons. Darwin put it to the test.

  It was a success! Darwin wrote Tegetmeier with the news: “I have got some excavated hemispherical bases in artificial wax—hurrah! I thank you cordially for this capital suggestion.” Weeks later he was caught up in the turmoil over his sick child, 2-year-old Charles Waring, who had contracted and would die from scarlet fever, and Wallace’s manuscript, which looked like it would scoop his life’s work. Thinking about his bees may have helped keep him anchored. Tegetmeier too was always experimentising, and reported his latest results in a paper at the July 5, 1858, meeting of the Entomological Society of London. He also displayed his latest observation hive, consisting of three glass plates per side. When he gave the bees a bar of wax to work, they fashioned cylindrical cells with concave bases. As new cells were added at the comb’s edge, he found that the outer edges of the original ones, now surrounded by other cells, were transformed into hexagons.

  One would think that this settled the matter, but some naturalists apparently had much invested in the belief that bees constructed perfect hexagons from the start, and, more to the point, that this “fact” proved the bees were divinely inspired. John Edward Gray, the Keeper of Zoology at the British Museum and president of the Society, spoke up to express his impatience with that view: “the attempt made by Natural Theologians to prove that the formation of an hexagonal rather than a cylindrical cell indicated the possession of a greater degree of Divine wisdom bestowed upon the insect, was the greatest piece of humbug they had ever brought forward.”13 Hymenopterist Frederick Smith of the British Museum, about whom we will learn more later, said he was not prepared to argue one way or another, but pointed out that when he tried to convert paper cylinders to hexagons he was not successful, and that some wasps construct hexagons from scratch, rather like building up a hexagonal chimney bottom to top. That was when Tegetmeier announced his next round of experiments, this time using colored wax to trace precisely how and where the bees excavate and what they do with the excavated wax.

  It was an inspired idea, and inspiring: Darwin soon seized on the technique. Alkanet was the coloring agent of choice, a popular source of red dye since antiquity. Made from plant roots, it puts red in rouge, lipstick, and other cosmetics; wood stains (“rosewood”); and even foods like the curry Rogan Josh, which takes its name from the Indian term for alkanet, Ratan Jot. That summer Darwin and Tegetmeier gave the bees blocks of wax with a thin red layer, a marker to see what the bees were doing as they built their cells.

  Accidental Architects

  In early September 1858 Tegetmeier visited Darwin to talk bees and compare notes. Darwin was happy to let his friend take the lead on reporting their findings, rather than his usual approach of publishing himself in “letter to the editor” fashion. He was distracted, grieving the loss of his son in late June and in the throes of deciding whether to abandon his “big species book” Natural Selection and, if he did, the best format to make his theory public and preserve his priority in the wake of Wallace’s unwelcome essay. Later that month Tegetmeier gave a paper at the British Association meeting in Leeds, describing his and Darwin’s experiments with red-colored wax. Their experiments, repeated with various modifications, showed “that the excavations were in all cases hemisphaerical, that the wax excavated was always used to raise the walls of the cells, and that the cells themselves, before others were formed in contact with them, were always cylindrical.”

  Tegetmeier’s idea of using red-tinted wax as a tracer of the bees’ activity was just the kind of simple and effective experimental approach that Darwin loved. He put the red-wax technique to good use in several experiments. In one he gave the bees a thick wax block coated with just a thin layer of red wax. This revealed that the first thing the bees do as they make new comb is to exc
avate small circular pits. As they deepen and widen these pits they turn into shallow bowls or cup-shaped depressions about the diameter of a honeycomb cell. When the excavations by adjacent bees intersected, the bees began to erect a flat wall between the growing cells. But then Darwin noticed something really interesting: in this single-layer comb, hexagonal walls went atop the circular edge of the depressions, with no sign of the usual three-sided pyramidal bases of double-sided comb. This was because the wax block was so thick it was not possible for the bees to build back-to-back comb in their usual way. However, when he put a thinner strip of red wax in the hive the bees started excavating pits on both sides. They do not line up the cells exactly opposite one another, however. Rather, the cells are offset, such that a given cell on one side sits at the intersection of three cells on the other side. Each cell shares a flat wall with each of three cells opposite—thus terminating at the base in a three-sided pyramid rather than a bowl. This makes the honeycomb stronger than an arrangement with cells directly back-to-back, since each cell is backed by walls of three opposite cells.

  In this experiment, however, the strip of wax Darwin gave the bees was so thin that they only worked it to a limited extent. The bees were on their way to producing pyramidal bottoms of cells, and different degrees of this development were in evidence at the points where they ceased to excavate, before they could break into another cell. In yet another experiment, Darwin covered edges of cells with a thin layer of red-colored wax. “I invariably found,” he wrote, “that the colour was most delicately diffused by the bees by atoms of the coloured wax having been taken from the spot on which it had been placed, and worked into the growing edges of cells all around.” In other words, the bees were continually working and reworking cells, taking a bit of wax here and adding a bit there as the comb grew. Trial and error, constant improvement. In arguing that the bees’ cells are not perfect, Darwin would have been intrigued to learn that some 80 years later mathematicians discovered a hexagonal cell shape with a prismatic four-sided base that is more efficient at cell-packing than the honeybee’s pyramidal-ended cells.14

  By the time Tegetmeier’s paper was published early in 1859 Darwin had settled on the format he would use for explaining his theory in full: a concise book—concise relative to the length Natural Selection would have been, anyway. After some deliberation he dubbed it On the Origin of Species. There, in Chapter 7, he summarized his experiments with Tegetmeier, satisfied that the hexagonal cells of honeybees emerged from properties of the placement and elaboration of initially circular cells. “Grant whatever instincts you please,” he wrote in the Origin, “and it seems at first quite inconceivable how they can make all the necessary angles and planes, or even perceive when they are correctly made. But the difficulty is not nearly so great as it at first appears: all this beautiful work can be shown, I think, to follow from a few very simple instincts.” Modern biologists would agree. Honeycomb likely takes on its distinctive form through context-dependent rules followed by the bees during construction, in combination with the physical properties of wax and cell shape. The intriguing hypothesis of “stigmergy” postulates that properties of the nest structure itself triggers certain construction rules in insect builders, a form of self-organization where each step in construction, simple behaviors in and of themselves, stimulates the next step. This fascinating idea, applied most successfully to the construction of wasp and termite nests, is one expression of the “extended phenotype” concept articulated by the Oxford evolutionary biologist Richard Dawkins. Here the comb is an extension of the bees themselves. Insofar as the physical structure affects survival and reproductive success, and is constructed in whole or in part through heritable genetic traits, natural selection can act upon it. And, the simplest way for selection to alter nest architecture is by altering those simple behavioral rules that worker bees follow in cell construction—in the same way that a slight deviation from a path of travel, like a simple fork in the road, can lead to dramatically different destinations, small changes in construction rules early on can lead to dramatically different structural outcomes. That’s where the bigger picture comes in, as Darwin appreciated. He wondered if there was evidence that modification of simple behavioral rules of construction can lead to this “most wonderful of all known instincts?” He thought so.

  Detail showing the three-dimensional structure of honeycomb. (Left) Three-sided pyramidal bases of cells, each face of which is also one face of the base of each of three opposite cells. (Right) Hexagonal cells, showing 120-degree angles between walls. Photographs by the author.

  Ask the Relatives

  Even before throwing himself into honeycomb geometry Darwin started collecting as many examples of bees’ handiwork as he could—characteristically, by writing to contacts near and far imploring them to send him specimens. Just as individual bees built their hexagonal cells in stages beginning with circles and cylinders, so too, Darwin thought, did this stepwise process reflect the likely evolutionary trajectory leading to the exquisitely complex honeybees. In something of a behavioral version of von Baer’s “developmental law,” where earlier developmental stages were thought to reflect ancestral states of a species, he was sure that the incipient, cylindrical, stage of honeybees’ hexagonal cells meant that ancestors of these bees built solely spherical or cylindrical cells. Honeybees thus represented a more recent, advanced, state of cell development. Why would selection have favored this? The idea was that in the struggle for existence, selection acting on the ancestors of honeybees to improve reproductive success led to maximizing the number of cells per unit area while also economizing on the quantity of wax needed for those cells. More cells potentially mean more brood that can be reared in a given period of time, and more storage space for honey (vital for getting the colony through the winter). And, crucially, the hexagonal shape requires less wax.

  He asked Tegetmeier what wax “costs” the bees to produce, in terms of amount of energy. Their currency is food, mainly sugar in the form of the honey they produce. His friend calculated that 15 pounds (6.8 kg) of sugar was needed for every pound (0.45 kg) of wax, probably a rough calculation based on how much he fed his colonies per season and how much they grew on average in that time. Our current estimate is that it takes about 0.2 ounce (6 g) of honey for the bees to synthesize 0.04 ounce (1 g) of wax. To try to understand what that means for the energy budget of a colony, here’s how much effort it takes for one bee to make 6 g of honey. Each flower yields a tiny amount of nectar. On average a bee’s crop can store about 30 mg of nectar at a time, so besides the multiple floral visits to fill up its crop, it takes more than 200 crops-full of nectar just to condense down and process to 6 g of honey. The hexagonal cell means less wax needed and more energy saved—energy that could be put into brood production and nest hygiene, and that much more food put up for the winter. It’s worth pointing out that overwintering as honeybees do is unusual for insects: rather than going dormant, these insects create a warm microenvironment by metabolically burning honey for heat production. It’s an expensive lifestyle (rather like our own).

  Darwin was sure that natural selection acted on honeybee ancestors to favor the evolution of hexagonal cells to save the bees energy. He thus needed to show that simpler, less efficient, transitional forms were possible. He looked to “collateral descendants”—related species—to see if gradations are found. He began with his old friends the bumblebees.

  Bumblebees are taxonomically of a different genus (Bombus) than honeybees, but are from the same tribe (Apini). Like honeybees, they are social, but differ in important ways. Bumblebee colonies last only a year, and the bees typically nest in the ground. And, as Darwin knew, they build more or less spheroidal waxen cells of various sizes that are randomly clumped together, in which they raise their brood and store honey. Bumblebees are the perfect contrast with their geometrician relatives, but Darwin needed to find species intermediate between the two. He was excited to learn about the so-called “Mexican bee,”
Melipona domestica, which make a rudimentary comb of spherical to cylindrical cells, with flat walls where they intersect. Now dubbed M. beecheii and placed in the same family (Apidae) as honeybees and bumblebees but a different subfamily (the Meliponinae), this stingless bee was semidomesticated centuries if not thousands of years ago by the indigenous people of Mexico, where it is known as Xunan-kab, or Royal Mayan bee. Darwin came across an account of this bee in a paper by Pierre Huber, son of the Swiss apidologist François Huber, whom we met earlier in this chapter. The younger Huber, a distinguished entomologist like his father, published a paper with wonderfully detailed plates illustrating the bees’ nests and the unique “hives” created by the indigenous Mexicans to maintain colonies. They basically took a hollowed log or branch, stoppered both ends, and hung it from trees or the eaves of their dwellings. Darwin was more excited by the cutaway drawings of the cells, showing spheroid cells stuck together in a rudimentary comb, with curved walls except where they intersect other such cells. There the walls were made flat by the bees, inevitably taking on a multifaceted form where several came into contact. It was the very intermediate arrangement that Darwin sought: placing their cells next to one another allowed wall-sharing between adjacent cells, saving wax relative to the independent cells made by bumblebees.