Saturday, October 05, 2019

The Biopolitical Science of the Imperfect Honey Bee

Aristotle thought the political animals could be identified as those animals who cooperate for some common work or function (koinon ergon). This suggests that the best political order serves the common good of all its members.  And yet the evolutionary science of animal politics indicates that such perfect harmony in a political order is impossible, because the individual diversity of animals must always create conflicts of interest both within and between their social groups, and therefore there can never be a perfect animal society in which every member works for the common interest of all the members of the society.  This must be true even for those social insects, such as honey bees, that might appear to be perfectly cooperative.

As examples of political animals, Aristotle identified bees, ants, wasps, cranes, and humans.  Today, bees, ants, and wasps are classified as belonging to the Hymenoptera order of insects, which includes over 150,000 living species.  Of these, the honey bees are the best studied insects, because for thousands of years beekeepers have managed them for the production of honey.  Aristotle wrote extensively about honey bees (in The History of Animals and The Generation of Animals), and clearly much of his knowledge came from beekeepers.

Today, we know that most of the bee species are solitary or only weakly social.  The 380 bee species showing well-structured colonies are only 1.3% of all bee species.  The 11 living species of honey bees are only 3% of all eusocial bee species.  The honey bee species found generally in Europe and North America is Apis mellifera.

                                                    Queen Bees Fighting to the Death

Beginning in ancient Greece and Rome, political thinkers have pointed to honey bee colonies as models of political justice in which members do different jobs in a complex division of labor under the monarchic rule of the queen bee for the common good of all (see Morley 2007 and Van Overmeire 2011).  Actually, though, most political philosophers--including Plato and Aristotle--thought the ruler was a king bee, and it wasn't until the 16th and 17th centuries that it became clear that the ruler was really a female bee, which confirmed Xenophon, the one ancient philosopher who suggested that the ruler of the bees was a queen.  In 1609, an English beekeeper Charles Butler published The Feminine Monarchy, Or A Treatise Concerning Bees, which surveyed the scientific knowledge of bees beginning with Aristotle and presented bee society as displaying the best form of government: "For the Bees abhorre as well Polyarchie, as Anarchie, God having shewed in them unto men, an expresse patterne of A Perfect Monarchic, The Most Natural And Absolute Forme of Government" (1.7).  Since this was only six years after the death of Queen Elizabeth, Butler's readers could see this as a tribute to her rule.

This looking to the bees as showing the natural pattern for the best form of government began with Plato.  In his Statesman, the Eleatic Stranger lamented that "no king is produced in our cities who is, like the ruler of the bees in their hives, by natural birth pre-eminently fitted from the beginning in body and mind" (301d-e).  In The Republic, Socrates claimed that in his most just city, philosophers would be reared from birth to rule for the common good just like the king bees in hives (520b).

Aristotle agreed with Plato in recognizing that some bees were political animals by nature, although he also saw that some species of bees were solitary animals (HA, 487b32-488a14, 623b5-15). But Aristotle disagreed with Plato's assumption that the political life of bees was perfectly harmonious.  Aristotle thought there were often several leaders in a bee colony, that they would fight with one another, and that the worker bees would kill the most disruptive leaders (553b14-20, 625a15-18, 626a29-32).  He also thought that bees had to fight against robber bees who would steal their honey (625a15-b7).  And despite the reputation of bees as industrious workers, he observed that some bees were remarkably lazy, which was one of the many traits showing individual variability in their personalities (626a1-b20, 627a12-22).  Indeed, he thought that all animals showed individual differences in their character traits (487a10-14, 629b6-8).  As indicated in some previous posts here and here, the recent biological studies of animal personalities support Aristotle's point here.

Against Aristotle, Thomas Hobbes argued, in both De Cive (5.5) and the Leviathan (ch. 17) that, unlike human beings, the truly political animals like bees and ants lived in harmonious societies without conflict, where there was no conflict between the private good and the common good, because the natural instincts of the social insects inclined them as individuals to do what was good for all members of the society.  Consequently, the social insects do not need the coercive power of the Leviathan to enforce social order, as is the case for human beings.  Hobbes was mistaken about this, because the social insects show many possible lines of conflict--between colonies, between queens, between workers, and between queens and workers.  I have written about this here.

Those biologists who speak of bees and other social insects as "superorganisms" stress the apparent harmony and perfect cooperation in an insect colony in a way that seems to support Hobbes's understanding (Holldobler and Wilson 2008; Moritz and Southwick 1991).  But in their recent book--The Dark Side of the Hive: The Evolution of the Imperfect Honey Bee--Robin Moritz and Robin Crewe show that the imperfection of a bee colony becomes clear as soon as one looks at its individual members.  They write:
"As with any complex social system, honey bee societies are prone to error, robbery, cheating, and social parasitism.  The honey bee colony is thus far from being a harmonious, cooperative whole.  It is full of individual mistakes, obvious maladaptations, and evolutionary dead ends.  Conflict, cheating, worker inefficiency, and curious reproduction strategies all occur.  The perfection that is perceived to exist in their social organization is a function of a particular experimental focus on the colony as a whole rather than exploring the idiosyncrasies of its individual members" (vii).
Bees are individuals with variable temperaments as shaped by their genetic endowment and their life experience.  So, for example, most workers respond to the queen's pheromonal signals by suppressing their ovaries, so that only the queen lays eggs, but some workers activate their ovaries and lay eggs even in the presence of the queen.  To counter this rebellion, some workers police the colony by destroying the eggs laid by workers.

Despite their reputation for industrious devotion to whatever task they undertake in the colony, many bees are remarkably lazy.  If one observes individual bees throughout their lives, many will be seen loafing most of the time.

There is also great individual variation in intelligence. One illustration of this is in their famous "waggle dance," which was observed by Aristotle (624b5-8), although he could not understand the signals.  Karl von Frisch explained this dance as a communication by foraging bees of the direction and distance of good foraging sites.  But he observed that some bees were not as accurate and precise in their dance communication as others.  There was a lot of sloppy dance language showing that there were a lot of stupid individuals (von Frisch 1967: 149, 212).

The primary reason why honey bee societies appear to be harmoniously cooperative is that most of the individual bees give up reproduction in order to raise the offspring of the queen, and thus the workers appear to sacrifice their individual fitness to serve the fitness of the queen.  William Hamilton thought he could explain this self-sacrificing altruism as a product of the close relatedness of the females in a haplodiploid system of sex determination.  In this system, males develop from unfertilized eggs and are haploid (having only one set of chromosomes), while females develop from fertilized eggs and are diploid (having two sets of chromosomes).  Consequently, if the queen mates with one male, her daughters will be more closely related to one another (sharing 3/4 of their genes on average) than to their own offspring (sharing 1/2 of their genes on average); and therefore these super-sisters enhance their inclusive fitness by foregoing their personal reproduction and rearing their sisters.

The problem with this explanation, however, is that honey bee queens are polyandrous in their mating, which reduces intracolonial relatedness.  A virgin queen flies out of her hive to attract a swarm of males, and as many as one hundred of them will fertilize her eggs.  As a result, the colony of offspring that she produces will have many subfamilies, and so her daughters are more likely to meet half-sisters (with a relatedness of 1/4) than super-sisters (with a relatedness of 3/4).  And since the workers are unable to discriminate between half-sisters and super-sisters, they are unable to favor the reproduction of their own subfamilies.

This and other problems with Hamilton's theory has provoked a debate over whether kin-selection is or is not necessary for explaining social cooperation.  Edward O. Wilson has changed his mind about this--switching from supporting Hamilton's theory to doubting it.  I have written about this here.

The "imperfect honey bee" illustrates an often overlooked fact about evolution--that far from providing optimal solutions to problems, it only provides feasible solutions that are good enough for somewhat stable systems but not perfect.  That's the theme of a new book by David Milo--Good Enough: The Tolerance for Mediocrity in Nature and Society.


Butler, Charles. 1609. The Feminine Monarchie. Oxford: Joseph Barnes.

Milo, David. Good Enough: The Tolerance for Mediocrity in Nature and Society. Cambridge: Harvard University Press.

Morley, Neville. 2007. "Civil War and Succession Crisis in Roman Beekeeping." Historia 56: 462-70.

Moritz, Robin, and Robin Crewe. 2018. The Dark Side of the Hive: The Evolution of the Imperfect Honey Bee. Oxford: Oxford University Press.

Van Overmeire, S. 2011. "The Perfect King Bee: Visions of Kingship in Classical Antiquity." Akroterion 56: 31-46.

von Frisch, Karl. 1967. The Dance Language and Orientation of Bees. Cambridge: Harvard University Press.


Roger Sweeny said...

The problem with this explanation, however, is that honey bee queens are polyandrous in their mating, which reduces intercolonial relatedness.

I think you mean inTRAcolonial (within colonies) rather than inTERcolonial (between colonies).

If I'm right, feel free to change the text and never publish this.

Larry Arnhart said...

Roger, thanks for spotting this. I've made the correction.