Darwin's Backyard

by James T. Costa

  Three examples of Melipona beecheii cells dissected to show faceted walls that develop where cells intersect. From Plate III of Pierre Huber’s paper “Notice sur la Mélipone domestique, abeille domestique Mexicaine,” published in 1836.

  He argued as much in the Origin: “it occurred to me that if the Melipona had made its spheres at some given distance from each other, and had made them of equal sizes and had arranged them symmetrically in a double layer, the resulting structure would probably have been as perfect as the comb of the hive-bee.” To back this up he sent some calculations to Prof. Miller, his mathematician friend, who concurred. In the Origin Darwin describes his and Tegetmeier’s experiments, and finishes with a stirring summary of hexagonal cell evolution: “Thus, as I believe, the most wonderful of all known instincts, that of the hive-bee, can be explained by natural selection having taken advantage of numerous, successive, slight modifications of simpler instincts.” Natural selection worked by “slow degrees, more and more perfectly” to lead the bees to build more regularly:

  That individual swarm which wasted least honey in the secretion of wax, having succeeded best, and having transmitted by inheritance its newly acquired economical instinct to new swarms, which in their turn will have had the best chance of succeeding in the struggle for existence.15

  Darwin didn’t intend his bumblebee-to-Melipona-to-honeybee series to be taken literally. That is, he did not mean that bumblebees evolved into Melipona bees, which in turn gave rise to honeybees. Rather, the bumblebee and Melipona style of cell construction sheds light on what the cell-building behavior of the honeybee’s ancestors must have been like, showing the evolutionary pathway to modern honeybees’ cells. His point is that simplified intermediate stages must exist for even the most complex, intractable structures or behavioral adaptations. “A series,” as he put it in regard to a different but related subject, “impresses the mind with the idea of an actual passage.”16

  Time-Out for Bad Behavior

  Honeybee cell-building was just one of three cases Darwin explored as “difficulties” in understanding instinct. The other two, slave-making ants and cuckoos—both bizarre cases of brood parasitism—seemed to cry out for explanation. He found himself distracted from his honeybee work thinking about them, probably because they, too, held deeper implications. He would go about his work on them similarly to the way he found relatives of honeybees that had transitional behaviors. Call it Darwin’s time-out to study some bad behavior.

  The case of the cuckoos (Cuculus canorus) had been known for centuries. These birds, widespread in Europe, are obligate brood parasites incapable of rearing their own young, not even able to build a nest. (Their penchant for getting others to rear their young gave rise to the term “cuckold.”) How could such an extreme form of parasitic behavior get its start? Piecing together information on the behavior of other species in the cuckoo family (Cuculidae) in Europe and North America, Darwin found variation in degree and form of brood parasitism, consistent with the idea of an evolutionary series. On one end of the spectrum Darwin found opportunistic parasites occasionally practicing “egg dumping” (laying eggs surreptitiously in the nests of other birds)—having eggs in more than one basket, as it were, helps spread around the effort and risk of brood-rearing, and boosts the parasite’s reproductive success. This is termed “facultative brood parasitism” today, and is found in North American yellow-billed cuckoos. These birds usually rear their own young, but given a chance will also lay some of their eggs in the nests of other yellow-billed cuckoos, or even of other species. Darwin noted that the European cuckoo is found at the other end of the spectrum: it is a parasite not only wholly dependent upon hosts for brood-rearing, but whose young also invariably kill the young of the hosts and monopolize their care efforts. This is an extreme form of obligate brood parasitism. Darwin suggested a scenario where distant ancestors of today’s cuckoos first benefitted from the accidental laying of eggs in the wrong nest. Selection may have then favored the evolution of facultative brood parasitism, a kind of opportunism. This in turn could have set the stage for the evolution of the extreme form of brood parasitism found in European cuckoos, where the birds avoid expending the time and energy of building their own nest and focus completely on locating the nests of other birds to parasitize.

  The other form of “bad behavior” that caught Darwin’s attention was the recently discovered phenomenon of slave-making ants. Like the cuckoos, in its extreme form this behavior entails a parasite that is completely dependent upon a host to rear young. Again, how to explain the evolution of such obligate parasitic behavior as a gradual process? Once again Darwin looked to “collateral relatives,” making a case for transitions based on what related species do. From the accidental parasite to the occasional or opportunistic (facultative parasitism) to the extreme of complete dependency (obligate parasitism), he sought to find natural variation in the behavior among related species as a possible evolutionary pathway.

  Darwin knew something about slave-making ants from Kirby and Spence’s Introduction to Entomology, first published in 1818. Many a person had witnessed the predatory raids of certain ants, assuming they were contests for territory or food stores, not comprehending what was actually happening. Henry David Thoreau, in 1846, witnessed a battle near his cabin on Walden Pond: “The legions of these Myrmidons covered all the hills and vales in my woodyard, and the ground was already strewn with the dead and dying,” he wrote in Walden. Thoreau saw it as “internecine war, the red republicans on the one hand, and the black imperialists on the other,” evoking the carnage of human conflict.17

  Formica sanguinea, a dulotic (slave-making) ant species studied by Darwin. Drawing by Leslie C. Costa.

  Given Thoreau’s strong antislavery sentiments he might have viewed the conflict in a different light had he read Kirby and Spence. These authors anticipated readers’ incredulity at an astonishing form of insect behavior. What would the reader say when told that “certain ants are affirmed to sally forth from their nests on predatory expeditions, for the singular purpose of procuring slaves to employ in their domestic business?”, they asked. Kirby and Spence credited Pierre Huber as “the discoverer of this almost incredible deviation of nature.” Huber found that two ant species engage in raids on the nests of other ants in their vicinity: Formica rufescens and the appropriately named F. sanguinea (whose name means “bloody ant”—for their reddish coloration, but resonant with their behavior). These ants invade the nests of their quarry, killing off any adult ants that resist them and “ant-napping” the young, carrying the brood back to their own nest like booty-bearing pirates making for their lair. The fate of the brood is not, however, to become so many ant snacks; the raiders permit them to mature, and having imprinted (in the scientific sense) on their captors they believe themselves part of the group, and go about performing all of the work of the colony as if it were their own—and I mean all the work: nest building, cleaning, foraging, raising the brood of their captives, even defending to the death should the colony be threatened. Huber experimentally showed that F. rufescens was completely dependent upon the “slave” ants, so utterly incapable of even feeding themselves that they would die if deprived of their care. F. sanguinea, in contrast, could do some work, but not much. It appears to be an opportunistic (or facultative) slave-maker, engaging in the practice as opportunity knocks in contrast to the “obligate” slaver F. rufescens, which can’t survive on its own.

  The fact that early observers referred to this phenomenon as “slavery” speaks volumes: they could not help comparing it with human slavery, but the comparison is a poor one in several respects—not least the fact that these ant interactions are interspecific, while the human institution of slavery involves members of the same species. Nonetheless, the label stuck even in the scientific literature, although the preferred scientific term is dulosis. The inevitable comparison with human slavery resonated deeply with Darwin—he and his family were vehemently abolitionist, heirs to a proud fam
ily tradition of antislavery activism going back to his maternal grandfather Josiah Wedgwood I, whose famous abolitionist cameo brooch raised funds for the cause with its striking image of a manacled African and the resonant plea “Am I not a man and a brother?” Slavery was only abolished completely in Britain and its territories in 1833, but Darwin witnessed its brutality firsthand in Brazil while on the Beagle voyage. Darwin was not one to anthropomorphize nature, yet he could not resist referring to this predatory instinct of Formica as “odious.”

  One of the two species that Huber discovered as slave-makers was not found in Britain and the other one was rare, so naturalists there had little opportunity to study the phenomenon. Then Darwin read a paper by Frederick Smith, his entomological correspondent in the British Museum. Smith mentioned in his paper that F. sanguinea was locally abundant in Hampshire, a coastal county in southern England, where he had witnessed them launch a raid. Darwin wrote Smith in late February 1858 with a list of questions: in nonslavemaking ants, has Smith ever seen stray workers of one species inhabiting the nest of another species? No, Smith replied. Does Formica sanguinea “always & invariably make slaves,” Darwin wondered, or only occasionally? Smith thought they always did—“I never myself met with a community without numbers of other species” in the nest. In regard to ants that tend to be “enslaved,” do they feed their own queens in their own nests, or do the queens feed themselves with food brought by the workers? Smith was unsure about this.18 Darwin also asked for pointers on identifying this species. He wanted to see a raid himself. Smith advised him that morning or evening was the best time to see a raid, especially in the summertime when vulnerable pupae were in the nest for the taking.

  That April of 1858 Darwin headed south to Moor Park for a couple of weeks’ treatment with Dr. Lane—perfect for relaxation. He wrote Emma that he fell asleep on the grass after one long walk, awaking to “a chorus of birds singing around me, & squirrels running up the trees & some Woodpeckers laughing, & it was as pleasant a rural scene as ever I saw, & I did not care one penny how any of the beasts or birds had been formed.”19 An idyll, but the question of the origin of the beasts and birds was never really far from his mind. The park was perfect for ant-watching, and Darwin described in another letter to Emma how he would “loiter for hours in the Park, & amuse myself by watching the Ants: I have great hopes I have found the rare Slave-making species.”20

  He sent specimens to Smith for confirmation. Darwin got to wondering if and how ants of different colonies recognized one another, and tried a simple transplantation experiment: what happens if an ant from one colony is plunked down among ants of another colony? Well, it didn’t end well for the stranger, as his notes reveal: “I took several times some hill-ants (F. rufa) from their own nest & placed them on another; they were always extremely much agitated & were instantaneously attacked by the inhabitants: whereas when I returned several of the same lots to their own nest, they seemed immediately to recognise their comrades & be recognised by them.”21 In a letter to Willy from Moor Park he commented on this experiment, reporting that although thousands of ants inhabit each ant mound, “each seems to know all its comrades, for they pitch unmercifully into a stranger brought from another ant-hill.”22 Darwin did not do much more than this with his ants, but John Lubbock (who combined a facility for experimental entomology with the more traditional Lubbock family pursuits of banking and politics) took up the question, experimenting extensively with recognition and other forms of communication in ants in the 1880s (see Chapter 10). The key to understanding what’s going on here, like the mystery of bumblebee buzzing places Darwin also never grasped, was chemical markers.

  Darwin returned home in early May and got back to working on his bees. With all the ups and downs of bees’ cells, ants were out of mind for a while. But following the tumultuous events of late June and early July 1858, he got another chance to look for slave-making ants when the family headed south for some rest. They stopped for a week in Hartfield to visit with Emma’s sister, and then went on to Sandown on the Isle of Wight. From Hartfield he wrote a letter to his old friend Hooker, first thanking him for his part in what has been called the “delicate arrangement” over Wallace’s manuscript, but also commenting that when he got to the Isle of Wight he would begin working on an abstract of his species book. The plan at that time was to write a long review paper, an unhappy prospect. “I will set to work at abstract,” he wrote, “though how on earth I shall make anything of an abstract in 30 pages of Journal I know not, but will try my best.” He also revealed a more interesting diversion, telling Hooker that he “had some fun here in watching a slave-making ant, for I could not help rather doubting the wonderful stories, but I have now seen a defeated marauding party, & I have seen a migration from one nest to another of the slave-makers, carrying their slaves . . . in their mouths.”23

  The family soon arrived on the Isle of Wight. He began on the abstract, but before long gave up the idea of a journal paper and eventually decided instead on writing what was to become On the Origin of Species. Exploring the sandy heaths and woodlands, he was rewarded with witnessing another myrmecine slave raid. He noted that “only the largest & medium sized were carrying pupae.”24 He continued to make observations at every opportunity over the next year, observations that were later reported in the Origin. How to understand the evolution of so extreme a lifestyle, one in which in some cases the marauding ants are so dependent on their quarry that they cannot even feed themselves? One key question was whether slave-making behavior varies between and within species. Over the course of two field seasons he observed that it did have a range. That meant selection could act upon the behavior, and as with bees’ cells a transitional series was at least possible. “By what steps the instinct of F. sanguinea originated I will not pretend to conjecture,” he wrote in the Origin.25 But then he does: if a few ant pupae captured for food escaped this fate and, once emerged as adults, helped the colony instead, the host colony could benefit just enough relative to their competitors that selection might favor raiding for the sake of adding to their labor force and not their larder. Once this instinct is acquired, Darwin reasoned, natural selection could further modify it, step by useful step, even to the point of the ants being “abjectly dependent” on slaves. Thus he met his objective of coming up with a plausible scenario of a gradual evolutionary sequence for slave-making in ants, just as he did for the parasitic cuckoos. Modern biologists agree that Darwin’s scenario for the evolution of dulosis is basically correct—it is an elaboration of “normal” foraging and predatory activity that involved capturing the young for food. But Darwin saw further lessons: “Finally, it may not be a logical deduction, but to my imagination it is far more satisfactory to look at such instincts as the young cuckoo ejecting its foster-brothers,—ants making slaves,—the larvae of ichneumonidae feeding within the live bodies of caterpillars,—not as specially endowed or created instincts, but as small consequences of one general law, leading to the advancement of all organic beings, namely, multiply, vary, let the strongest live and the weakest die.”26

  That last statement may have seemed jarring to readers, but writing as one who had felt the deep, unspeakable pain of losing a cherished child to illness, he would rather not attribute life’s miseries—including those inflicted by parasitic species—to a benevolent deity, however much his vicar friends urged that there was a plan behind it all, that all was for the best. He couldn’t accept that. An important implication, too, was that there was no slavery by divine design, running counter to pro-slavery advocates who saw the occurrence of the “peculiar institution” in nature as justification.27

  The fact that behavioral traits can be bred into domesticated varieties is an indication that some instincts or behaviors can be shaped by selection in nature. Darwin was sure it was true throughout the animal kingdom, including both the most “wonderful” and most “odious” of behaviors, from the busy bees to the noxious cuckoos and slave-making ants. He wanted that fact about
species to be acknowledged widely: the good, the bad, and the ugly alike arise through a gradual process of evolution by natural selection.

  Experimentising: Bees’ Cells and Bubbles

  Unless you’re a beekeeper, or good friends with one, it won’t be very easy to experiment with cell building à la Darwin, but the next best thing is dissecting some honeycomb. First, check out some hexagonal cell-building online: in the BBC program The Code (www.bbc.co.uk/code), Oxford mathematician Marcus du Sautoy explains why the hexagonal cell-building of bees is more space-efficient than the other two polygons (squares and equilateral triangles) that fit together without leaving gaps: www.youtube.com/watch?v=F5rWmGe0HBI.

  I. Honeycomb Dissection

  A. Materials

  • Honeycomb (can be purchased online, and can be found packed with honey at some health foods stores and farmers’ markets)

  • Razor blade, craft knife, or sharp paring knife

  • Tray, plate, or shallow dish

  B. Procedure

  1. Drain the honeycomb of honey as best you can over a bowl, to save as much honey as possible for enjoyment later. The remainder can be dissolved by letting the honeycomb sit in a bowl of lukewarm water, changing the water every 10 minutes, until most of the honey is gone. The comb is very delicate—handle with care.