Can Females Rule the Hive?

You learn a lot about people by how they talk about animals

The problem

After decades of studying animal behavior, I’ve learned a few things. The first is that I’m pretty dumb. There’s so much information available, and so much more to be discovered (which will change what’s currently “known”), it’s impossible to know more than a tiny fraction. The second thing I’ve learned is that animal behavior and its physiological underpinnings are complex emergent processes that can’t be explained by grasping at selected ‘facts’, or passing on easily digestible explanatory nuggets — no matter how enticing (or click-worthy) they may be.

I’ve also learned that people have an uncontrollable compulsion to draw social, political, or moral lessons from animal behavior, and then bicker back-and-forth about the underlying biology, as if — once settled — that will decide the moral question, du jour.

The problem is, of course, that the answers to political or moral questions aren’t in the biology. It really doesn’t matter that animals commit infanticide, sexual cannibalism, or kill each other for no apparent reason. I don’t think people should do any of those things. Analogously, the fact that some fish are sequential hermaphrodites, or that male Syngnathid fishes (seahorses and pipefishes) incubate their fertilized eggs has nothing to do with how I raise my children.

On the other hand, there are important lessons to be learned from animals for those who aren’t hobbled by anthropo-narcissism, and can see beyond the surface phenomena. Consider, again, those fish that change their reproductive status between male and female. The take-home message is not that sex is ‘non-binary’. The lesson is that complex physiological processes “involve coordinated transformations across multiple biological systems, including behavioral, anatomical, neuroendocrine and molecular axes,” and the processes can be influenced by the social status of the fish. OK, that’s cool. But, it takes far more effort to understand the epigenetic consequences of the fish’s subjective ‘perceptions’ of its social status than it does to use the naked fact that it changes sex as an ideological bludgeon. Most people never manage the former. They seem much more content to bicker about the definition of ‘fish sex’ than to learn about — and become fascinated by – the beautiful intricacies of biology.

Of course, this is nothing new. You may be aware of the recent back-and-forth over honey bee sex. Although I think that the disagreement was a simple misunderstanding between two writers who actually agree — and that’s another story — the whole thing is interesting to me because it speaks to my larger point.

The disagreement had to do with how to interpret the unique caste system of the honey bees. That’s a tricky thing to understand. It even confused Darwin. The honey bee hive houses three castes of bees: a large reproductive female (the queen), thousands of non-reproducing female workers, and hundreds of male drones who have no stingers and don’t do any work in the hive. Several of the males will mate with the queen during an annual “nuptual flight,” at which time the queen acquires and stores sufficient sperm to last her entire reproductive lifetime. Then, as autumn approaches, all of the males are driven out of the hive to ensure sufficient resources for the overwintering females.

Historically, the seemingly idyllic but enigmatic structure of the honey bee colony has posed a number of difficulties for those who wish to use the bees as a model for human behavior. When I wrote “Can Females Rule the Hive? — which examined the controversy over honey bee sex and gender roles in early (16^th-18^th century) British beekeeping books — I explained how the ‘woke social justice warriors’ of the time used their misinterpretations of bee biology to promote their personal and political ideologies. The story is fascinating because it parallels precisely what’s going on today. Perhaps there’s a lesson to be learned.

The beginning

The story begins with Edward Topsell’s Historie of Serpents. Or, The Second Booke Of Living Creatures published in 1608, “…wherein is contained their divine, naturall, and morall descriptions… names, conditions, kindes and natures of all venemous beasts… and the wonderfull worke of God in their creation.” As you can tell, this was a time when there was no distinction between a popular book and a scientific book.

Unique among the animals that Topsell described, he saw the bees and their hive as a perfectly structured, hierarchical society that represented the ideal model by which all humans should live, a tightly knit cooperative led by a king surrounded by noble, warlike male soldiers. So, through this lens, it was inevitable that Topsell would presume the queen bee to be a “king”:

He that is elected Monarch Casar, and captaine generall of the whole swarme, is ever of a tall, personable, and heroycall stature, being twice so high as the rest, his wings shorter, his legs straight, brawny, and strong, his gate, pace, and manner of walking is more lofty, stately and upright, of a venerable countenance, and in his forehead there is a certaine red spot or mark with a Diadem, for he far differeth from the popular and inferior sort in his comlinesse, beauty, and honor.

However, the drones — or male “soldiers” — posed a problem for Topsell.  Some earlier beekeeping books had correctly pointed out that the unarmed (stingless) drones don’t do any work in the hive; in fact, some suggested that beekeepers kill the males to save the hive’s resources (e.g., Fitzherbarde's Booke of Husbandry published in 1523).

The idea that the males were expendable idlers was anathema to Topsell (and those others) who saw the hive as a reflection of their ideal society, run by kings, fathers, and husbands, and secured in part by primogeniture. So, Topsell did what many more would do, and what the ideologically motivated do now.  He made the bees fit his political model by ’twisting’ the truth a bit, and claiming both that the males are necessary to the daily goings-on of the hive, and that they do, in fact, possess a stinger (confusing, it seems, the drones with the female workers):

The prince of philosophers [Aristotle] confoundeth the sexe of Bees, butthe greatest company of learned Writers do distinguish them… the soundersort (in my judgment) will neither know nor acknowledge any other males but their Dukes and Princes, who are more able & handsome, greater and stronger than any of the rest, who stay ever at home ... as those whom nature pointed out to be the fittest to be stander-bearers ... and ever to be ready at the elbows of their loves to do them right. . .. If any Souldier looseth his sting in fight, like one that had his Sword or Spear taken from him, he is presently discouraged and dispaireth, not living long, through extreamity of griefe.

Topsell's descriptions were more than wishful thinking, of course. He, and many writers to follow, saw more than a convenient metaphor in the honey bees. They saw a divine model of the way things should be, an orderliness written into the very fabric of nature:

Bees are governed and doe live under a Monarchy… and their King being deeply bound to them by an oath, they exceedingly honor and love… For these are the laws of Nature not written with Letters, but even imprinted and engraven in theyr conditions and manners… Whereas the Almightie hath created all things for the use & service of man, so especially among the rest hath he made bees, not onely that they should be unto us patterns and presidents of politicall and oeconomicall vertues… but even Teachers and Schoolmasters instructing us in certaine divine knowledge, and like extraordinary prophets, premonstrating the successe & event of things to come.

As beekeeping became more widespread in Britain during the first six decades of the 17^th century, a number of original beekeeping books were published, the most important of which was Charles Butler's Feminine Monarchy (1609). Although Butler begrudgingly acknowledged that the queen and workers are female, and the drones male, it was a bitter pill for him to swallow. Nonetheless, that was the biological ground truth. So, in order to remain true to the biological facts and continue to use the bees as a social metaphor, those who wrote after Butler had to contrive some fantastical interpretations of life in the hive.

The first important book to tackle the problem of a ‘model society’ run by females was Richard Remnant’s A Discourse or Historie of Bees (1637).

Remnant recognized that the hive is a "female Monarchie… ruled and run by females," and that the male drones are only produced as needed to fertilize eggs and keep the hive warm. However, he was a bit confused about the biology. Remnant thought that the females "doe blow their brood in the cells or holes of their combs." That is, he thought females literally blew eggs into the honeycomb cells through their mouths (a belief common among the ancients), and that the drones subsequently fertilized the eggs. That, he thought, adequately explained the production of the “common” bees. However,  given her royal status, he couldn’t figure out how the queen was born.

Remnant figured that if the hive represents a monarchy, the monarch certainly couldn’t be born of a commoner. But, he reasoned, if he queen gives rise to new queens, then where is her “royal” mate? After all, the drones are all lazy, ne’er-do-wells; there’s not a regal one among them:

Whether the Queens blow the Queens I am not very certaine, but take it to be so, because of the fairness and excellency of the creature and the difference that is between her and the common Bees… But that there is any odds, excellency or use of the males one above the other, I find not.

So, by postulating a commonsense (though inaccurate) view of reproduction among the commoners, but remaining undecided about the queen, Remnant was left with only a single anomaly to explain: Whether the existence of a feminine monarchy among the bees is an indication that "It is lawful for women to govern in a commonwealth [or] … in private houses and families.” In the former case, Remnant answered that women may govern only when the "male sex is wanting; or secondly otherwise disabled by natural disability: as here [in the hive]; nature not having enabled the male to governe, the female doth it.”

However, when it comes to the home and family, Remnant gave this poetic warning:

Ill thrives the haplesse family that shows,

A cock that silent and a hen that crowes.

I know not which live more unnatural lives,

Obeying husbands, or commanding wives.

The final lesson Remnant drew from the hive was that "out of the experience of ruling Bees may be learned how to rule most women: for there is some resemblance between them." Bees are sensible and wary, teachy and passionate, and so are women. But, if both are "…well governed, and kept in good order, [they] are very industrious, but let them out of order, or ill handled, and there comes no good of them, but hurt and trouble."

Interestingly (and much like today), some 17^th century authors thought that they could more convincingly promote their social agenda if they manipulated the pronouns that they used. For instance, when the Reverend Samuel Purchas published his well-received beekeeping book, Theatre of Political Flying Insects (1657), he was keenly aware of the queen’s sex: "Though a king in place and power," he wrote, "the [monarch] is in sex a female." However, this recognition notwithstanding, he insisted on referring to the queen with the pronoun "hee."

Bees... [live] under one commander who is not an elected Governor ...nor hath hee his power by lot... nor is hee by hereditary succession placed in the throne ...but by Nature hath hee the SOVEREIGNTY over all, excelling all in goodliness and goodness, and mildness, and majesty.

Purchas carried the idea of the queen acting like a male to the extreme when, in discussing the reproduction of the royal caste, he claimed that the queen actually "injects a spermatical substance thick like cream" into the queen cells of the honey comb.”

Throughout the mid-17^th century, books about bees served both as authoritative biology books and, more importantly, practical guides to the popular craft of beekeeping. So, in order to be commercially successful, the books had to provide the most up-to-date information about what goes on in the hive, and that was always improving. At the same time, however, the authors had political agendas to promote. In order to achieve both of these goals, interpretations of the bees’ biology and behavior would have to become progressively more convoluted.

Science formalizes

By the early 18^th century, science was becoming formalized and professionalized in Britain and Europe. Restrictions on scientific discourse imposed by organizations like the Royal Society of London (founded in 1660) disallowed the flights of fancy and morality lessons that had been an integral part of the beekeeping literature.

At the same time, beekeeping remained widely practiced in Britain, and there was a strong, general interest in science among the burgeoning middle class who had both the time and money to pursue this and other types of leisure activities. So, beekeeping books became separated from the formalized scientific literature which released them from the intellectual restrictions imposed by the scientific societies. In other words, beekeeping books became the equivalent of the intellectually unregulated, popular science books, magazines, and blogs that glut our bookshelves and fill our inboxes today.

The new middle-class readers were an eager market for ambitious ‘quasi-scientific’ authors. However, when it came to honeybees, the audience was particularly knowledgeable. In response to that market, a new genre of popular beekeeping books was born, unrestrained by the limitations of experimental investigation and the demands of mutual agreement imposed by institutionalized scientific discourse, yet bound by their audience's knowledge about the basic biology of the honey bee.

However, the authors of this new genre were caught on the horns of a dilemma. On the one hand, they still wanted to use the honey bees as a guiding metaphor for human conduct. On the other hand, none of the emerging scientific discoveries about honey bee gender roles supported the ideologies that they wanted to promote.

During the early 18^th century, male and female gender roles were becoming more polarized in all social spheres. The division of labor between home and workplace was becoming increasingly rigid, and severe restrictions were developing as to the economic, political, and social options available to women, especially to those of the middle and upper classes (to whom the new beekeeping books were directed). Central to the limitations on gender role options was a redefinition of womanhood that cast women as "chaste, desexualized, and harmless dependent[s] whose only function [is] to uphold the values of a new age."

As gender distinctions became more ossified, gender roles were seen to be separated by nature as well as by function. Female sexuality was acknowledged only after marriage and was then restricted to one's husband. Likewise, male sexuality was defined by an equally inaccurate (and equally intransigent) stereotype: In juxtaposition and opposition to the desexualized female stood the lustful patriarch, whose prowess was linked to rationality, power, and conquest. To support this gender role ideology, the authors of the new beekeeping books had to deny, distort, or explain away those facts about the honey bees that didn’t fit these social mores — sometimes going to fantastic extremes to do so.

The first of these new books was Joseph Warder's True Amazons or Monarchy of Bees (1722). Warder was an astute observer of nature, and an empiricist at heart: "After great Pains taken, and curious observations made, with the Use of the best Glasses, I must come to this certain Conclusion, that all the working Bees are Female."

However, when it came to the males, Warder could not bring himself to refer to them by the “vulgar” and “ignominious Name of a Drone." Instead, he chose to use the term "male-bees." Then, in support of the reigning gender role definitions for men, Warder simply made up a story.

Warder described the males as “noble” little creatures, hardworking and industrious in the tasks given to them by nature (procreation, sitting on the eggs, and warming the hive). By tending to these chores, Warder claimed, the males actually free the workers to tend to their appointed duties, "…so that the Male-Bee is not only of great use but of absolute necessity, not only to the Being but to the well-being of the Colony of Bees."

Warder also made it clear that the drones’ lack of a stinger didn’t make them the emasculated, lazy creatures some had accused them of being. Instead, he claimed, they were actually quite formidable with voices so loud and dreadful that they cause “…Fear where no Fear is, especially to the fair and timorous Sex." They are, he continued, the "obedient Masculine servants of the hive" who are, after their brief afternoon flights, "kindly receiv'd by their imperious Dames… especially in… the chief Time of their Breeding." As to the proof of their sex, Warder noted a strong argument against their being male: The fact that they are under the domination of the females. In the end, however, he had to admit that his dissections confirmed their sex to be male.

The True Amazons… remained the standard work on beekeeping in Britain until 1744 when it was superseded by Melisselogia, or The Female Monarchy by John Thorley. Although Thorley claimed to have based his writing on forty years of observation and experience, he submerged many of the accepted facts about the bees in order to promote his personal worldview. On the one hand, his anatomy was up-to-date, and he settled for good the sex of the queen by reporting his observation of a queen laying eggs as she walked across his palm.

On the other hand, Thorley saw profound life lessons in the hive, especially for women. To the qualities usually attributed to the honey bees — cooperativeness, loyalty, prudence — Thorley added chastity. Ignoring virtually all that had been discovered over the last century and a quarter, he referred back to Butler's claim that bees do not copulate as do other creatures: "Another Virtue," he noted, "that should not be passed over in silence, being a Pattern to all, especially the Female Sex, …particularly those whose Province it is to discharge the Offices of the Kitchen, etc. is their Cleanness and decency." Their hive is always spotless and their dress always "neat to a proverb."

Thorley also believed that bees are naturally social creatures (like angels and men), living under the original and most natural form of government, a monarchy. However, he was somewhat dismayed by how the system operated:

Why must the female be Crowned with Honor and regal Dignities, and all the Ensigns of Royalty; when at the same time the Males are degraded, treated with the utmost Contempt, triumphed over, and trampled upon by the Populace and Commonality; expelled and banished, and, in a word, slain without mercy? Have previous authors quite forgot what they were taught when school-boys, that the Masculine Gender is more worthy than the female?

On the other hand, Thorley noted that if the drones are given their due and are, in fact, all consorts of the queen (i.e., the "Kings" and "Princes" of the hive), then one faces an even more embarrassing dilemma: No monarchy could exist with scores of pretenders to the crown all proclaiming their royal authority, and desirous of the queen. Certainly, if just a single queen can produce an entire colony, she does not need hundreds of males with which to mate. This idea, in Thorley's opinion, denigrates the queen, making her majesty "the most hateful and abominable whore, with Gallants by Hundreds"; if the drones are the male reproductives, he asked, then "What has become of her so much boasted, admired chastity, wherein she appears such an eminent Pattern to the human Species?” Thorley solved this dilemma in the only way he could. He claimed that the drones are of neither sex, and must have been created for some purpose other than reproduction. By similar reasoning he argued that since the queen can produce all of the hive's inhabitants on her own, there is no need for additional females. So, like the drones, the worker bees must be neuter, too!

Thorley had one more reason for arguing that the common bees are neither male nor female: The drones could not possibly be both male and under the domination of female bees. In support of this contention, he cited Aristotle, whose argument had been eloquently paraphrased by Charles Butler:

Natur' hat armed no' femal' for fight and forc' against de mal': But de Bee's are armed wit weapons and power, to chastis' de weaponles Dron': v. and der' for' de bee's cannot bee de femal's, and de Dron's de Mal's.

In the same year that Thorley's book was published, an English translation of Gilles Bazin's Historie naturelle des abeilles became available in Britain. In this very popular and widely read book, Bazin explained the bees’ sex and gender roles through a dialogue between two main characters, Clarissa and Eugenio. In the story, Eugenio explains to Clarissa that the hive consists of a single “Queen Mother” (the only female in the hive), up to one thousand drones who are the royal consorts to the queen, and fifteen thousand or more worker bees of no sex.

However, by claiming that all the males are potential consorts to the queen, Eugenio was faced with the same problem that Thorley was so anxious to avoid — namely, if the queen has gallants by the hundred, how can she maintain the virtue and dignity befitting a woman, especially a woman of her social rank?

Eugenio claimed to have solved this problem with a simple experiment: When a queen and a single drone were placed together in a glass bottle, he observed that the queen maintained an appropriate, feminine demeanor at all times. When she thought it best, the queen “chose” to caress the indolent, insensitive male into the act of love. Once aroused by the queen, he obeyed until he died, exhausted by his passion. Hence, by choosing only one husband at a time, the queen maintains her virtue.

Eugenio also discovered, much to his astonishment, that when a second drone was introduced into the same bottle, the queen did not behave like a "brute" but rather like a virtuous wife. Remaining fixed to the body of her deceased spouse; she did not take a new husband until the next day. Although, at first, this may not seem like a long enough period of mourning for a respectable woman, Eugenio defended her actions. She should not be chastised, he explained, because, given the short life of a bee, a single day is likely a proper period of mourning, as is a year for "one of our young widows."

Although Clarissa was taken aback by much of this, Eugenio assured her that the natural order was not violated: 

For when it has been once established, that a female should cohabit with a thousand males, the consequence ought to be, that these males should be sleepy, and to be awakened only by her; that she should be free to choose among them all him, whom she would honor with her favors. You easily conceive what confusion, what a terrible situation it would be for a woman, to find herself in the midst and at the mercy of a crowd of active, petulant husbands, who would all be masters the same moment.

Bazin's book was the last of its type. With the exception of a single (somewhat reactionary and vitriolic) book published in the early nineteenth century (Robert Huish, A Treatise on the Economy and Practical Management of Bees), beekeeping books written after 1750 stopped using the hive as a model for English social life. Two major factors were responsible for this change. The most important was the publication of two influential papers about bees in the Philosophical Transactions of the Royal Society in 1750 and 1777. The first was Arthur Dobbs's accurate explanation of the function of the queen bee's spermatheca. The knowledge that the queen mates in the summer and stores the sperm over the winter made the drones' role in reproduction, and the timing of their emergence understandable. The second was an article by John Debraw that popularized and replicated the amazing discovery of A. M. Schirach, that a single, fertilized egg will yield either a worker or a queen bee depending solely on the diet of the larva. The fact that a single egg could yield either a queen or a commoner, meant that the hive could no longer serve as a metaphor for class distinctions based on birthright. Together, these discoveries put to rest debates about bee biology revolving around the rigidity of social class — such as who might be the "royal" mate to the queen, or whether the queen lays only "royal" eggs — and halted the bickering about whether the common bees are male, female, or neuter.

The second factor was a new sophistication on the part of the beekeeping public. Rapid dissemination of accurate, experimentally derived scientific information made it increasingly difficult to distort biological fact in the service of social ideology. Beekeeping books, with progressively fewer exceptions, came to contain the best of that information and its practical application, rather than the social and political ideologies of their authors.

So, what have we learned about bees… I mean people?

Well, we have come full circle. We’ve returned to the hypothetical argument rhetorically posed in the article with which I began — Could it be that the worker bees have no sex at all? It’s an echo of the argument that began over three centuries ago, and a suggestion just shades away from any number of similar arguments that I’ve read ad nauseam in the popular press — written even by those who should know better.

In its crudest form, the argument goes like this: “Let’s find the most unusual and fascinating animal that we can, and use it to explain all of human behavior — especially that stuff related to evolution, sex and gender — and let’s do it in terms of our preferred ideology rather than the biology, itself.”

Have we become more intellectually sophisticated over the last three centuries?

That’s your call.

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This essay is based on the original books, most of which I actually held in my hands and read in the rare book room at The University of Chicago. In some cases, I used facsimiles of the original texts (which are more readily available now). All of the detailed references can be found in my original article, “Can Females Rule the Hive? The Controversy over Honey Bee Gender Roles in British Beekeeping Texts of the Sixteenth-Eighteenth Centuries.” Journal of the History of Biology, Vol. 24, No. 1 (Spring, 1991), pp. 113-144.

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