How to bee a queen
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Castes: the sorting hat of societies
Imagine a society where female reproductive rights are a matter of state concern. Where working class females are actively suppressed from having their own children, and only the nobility are allowed to reproduce. It’s also a police state, where everyone is spying on their neighbours, their family even, and if you’re found to have broken the rules, your children will be taken away from you and executed. There is no social mobility; if you’re born working class, you stay working class, and you’re forced to spend your life feeding, tending to and defending the very rulers who subjugate you. Yet even still, outsiders looking in praise the system, holding it up as the pinnacle of cooperation and altruism.
This is a very real situation, one that’s happening right now, all over the world, and if you haven’t guessed yet, I am of course talking about honeybees. It’s a tough lot being a worker honeybee. So why do these different hierarchies of workers and queens even exist?
When it comes to societies, as with most things in evolution, it all comes down to sex and reproduction.
Many animals are cooperative breeders, where adults look after the offspring of others, not just their own. Long tailed tits do this all the time; if you’re an adult long tailed tit and all your chicks were eaten by a predator, why not help look after your nieces and nephews instead? Your brother or sister could certainly do with an extra pair of hands - or wings - to feed all those hungry mouths. And so we can split adult long tailed tits into two groups; breeders and helpers. One year you might be a helper, the next year you might be a breeder, but in a given year, one group reproduces more than the other.
Some species take this further. Truly social species - or eusocial species to use the fancy Greek term - have specialised castes. Gone is the mantra of “you can be anything you want to be when you grow up”. Instead, before you go through puberty, you are essentially put through a sorting hat and assigned to a Hogwarts house, or caste. Much like the different Harry Potter houses, members of each caste behave very differently to one another.
Honey, I’m home
Honeypot ant workers can swell up with food and hang from the ceiling as a living larder.
Image by Greg Hume, via Wikimedia
Far less like the Harry Potter houses however, members of each caste often start to look very different from other castes, growing much bigger or smaller, developing exaggerated body parts that help them perform their duties. Someone from a soldier caste might develop huge weapons, while someone from a defender caste might contort their body into a living door able to seal up the entrance to the nest. A larder caste individual might swell up into a balloon able to store vast quantities of food. And no, I’m not just making these up - these are very real castes in the well-named army ants, turtle ants and honeypot ants respectively. I’ve put photos in the show notes which I highly recommend viewing because these things look weird.
Societies with this caste system have evolved multiple times across the animal kingdom. Most famously, we see these eusocial societies in bees, wasps and ants, a grouping called the Hymenoptera because their front and back wings or ‘ptera’ are paired up during flight, as if married by the Greek god of marriage, Hymen. You probably already know the names of the different castes in bees; you have the queen bees - females that reproduce, drone bees - males that reproduce, and the worker bees - females that instead of reproducing do pretty much every other task you can imagine, from collecting nectar to building the hive to defending the colony.
Hold the door
Turtle ant soldiers have large, flattened heads that fit perfectly into the round entrance holes for their nests so they can act as a living door.
Image by Katja Schulz via Flickr
But these aren’t the only animals with eusocial societies. We also see them in termites (which are much more closely related to cockroaches than they are to ants), beetles, aphids and shrimps, as well as Damaraland molerats and naked molerats. Yes, as if being a mammal without fur that changes its body temperature as the surrounding temperature changes, a rodent that lives for 30 years but basically never get cancers, and an animal that can survive for hours with barely little oxygen,wasn’t already weird enough, naked mole rats also live in eusocial societies where a single queen and a handful of breeding males are tended to by workers.
In naked mole rat societies, only one female is capable of breeding at a time - that’s the queen. Not only is the queen much bigger than the other females, she also prevents them from going through puberty so their ovaries don’t fully develop. But when the queen dies, the workers’ hormones kick in and they become sexually mature within a week. As you might expect, a bloody battle ensues as each female fights to be the heir to the throne until one, usually the largest, establishes dominance. The queen is dead, long live the queen.
Things get really interesting though when individuals can’t shift between castes. Each caste becomes so specialised and so good at the one job it does that they’re useless at doing any of the other jobs. Once you’re a worker, you’re always a worker. You’ve lost the potential to become a reproductive member of society.
Hello, soldier
Army ant soldiers grow huge mandibles and are much larger than other workers, allowing them to defend the colony from threats.
Image by Axel Rouvin via Flickr
We call this obligate eusociality because individuals are obligated to play their part in the society, and it’s the case in honeybees. A queen bee is totally dependent on workers to reproduce as she no longer has the capacity to raise offspring on her own, just as the worker bees are totally dependent on the queen to reproduce as they no longer have the capacity to breed.
All of this specialisation is a big deal. The reason eusociality has evolved multiple times is because, as the Victorian industrialists found out, division of labour is highly efficient. Why have a thousand jack-of-all-trades when you can have masters of each trade working together?
You’re probably more familiar with this concept than you realise, especially if we replace ‘bee caste’ with ‘cell type’. Lots of single celled individuals are going about their business, feeding and moving and reproducing all on their own, until one day they decide to be social and form a multicellular organism. Now they’re a society or colony of cells if you like, and they realise it’s much more efficient if each cell type specialises. Some cells become the immune system, the fighting caste. Some cells produce bone and connective tissue, the nest-building caste. And just one cell type is responsible for producing the next generation. The ovary cells are the queen bees of the body.
Let them eat bee bread! The making of a queen
It’s clear that castes can look and behave wildly different from each other, and in the case of the honeybee, it’s impossible for an individual to switch between castes. A worker bee can’t have a midlife crisis, become a queen bee and start producing several hundred eggs a day. But at birth, a bee has the potential to become any caste, just as a stem cell has the potential to become any cell type. All female eggs contain the genes needed to become a queen, as well as all the genes needed to become a worker. So what makes the expression of these genes so different?
Let’s say you’re a female egg that’s just hatched into a little larva. How do you become a queen bee? Firstly, you’ve got to be in the right place at the right time. Oddly enough, it’s the workers that decide which eggs get to become queens. When the current queen is dying or preparing to swarm, the levels of queen pheromone in the hive drop and this tells the workers to start producing future queens.
Regal snot
A larva sits in an opened queen cell on top of a bed of royal jelly.
Image by L. Rusert, via Wikimedia
Lucky for you, you’ve been born at just the right time, and the workers tending to the brood - the nurses - have decided to bestow upon you this royal fate. And here’s the important bit. You’re fed a special diet consisting of royal jelly and nothing but royal jelly. Yes, this is the exact same royal jelly you get in fancy soap and supplements. It’s basically worker bee snot - a milky white liquid that nurses secrete from their heads that’s packed full of all the proteins, sugars and nutrients that a young princess needs.
For a long time, geneticists studied this royal jelly to see how it was able to switch a bee’s genome into queen mode. There must be something in this regal cocktail activating royal genes. After decades of searching, in 2011 researcher Masaki Kamakura found one protein that looked like a likely candidate, which he called royalactin. It was an ideal finding - feed bee larvae a diet with royalactin and they turn into queens, feed them a diet without royalactin and they turn into workers. Finally geneticists could get to work looking at exactly how royalactin altered gene expression.
Sadly though, this finding was too good to be true. Just 5 years later, a team of German researchers tried to replicate Kamakura’s findings and were able to produce queens without feeding them any royalactin. There goes that hypothesis.
At around the same time, developmental biologist May Berenbaum was also interested in why bee larvae become queens. But by teaming up with Wenfu Mao and Mary Schuler, they soon realised they were asking the wrong question. Rather than asking why some bees become queens, they should instead be asking why some bees become workers.
If you’re destined to become a worker bee, you’re not fed anything as fancy as royal jelly. Instead, you’re fed honey, a concentrated form of nectar, and beebread, a special pollen-saliva mix that has been fermented by bacteria and looks like tiny yellow pebbles.
At risk of stating the obvious, nectar and pollen come from plants, unlike royal jelly which is secreted by the bees. And this means that a diet of beebread and honey is going to contain whatever compounds the plant produces. One of these compounds is p-coumaric acid. Now p coumaric acid is everywhere in the plant kingdom, and as a known antioxidant and anti-inflammatory it’s sometimes added to cosmetics and is even being studied as a chemotherapy drug. But that’s in humans.
Let them eat bread!
A pot of bee bread, aka bee pollen, which despite its humble origins is often used as a food supplement
Berenbaum wanted to know what effect eating this plant compound had on bee larvae. Her team fed the larvae a diet with or without p coumaric acid, and watched the larvae grow up. Bees that had eaten this compound grew smaller ovaries than those that didn’t, making them much more like sterile workers than hyper-fertile queens.
She went a step further and sequenced the RNA to see which genes were switched on by the compound. And you guessed it, the plant compound was changing the genes for being either a queen or a worker, and in particular the genes that control how big your organs are.
This completely changed how we think about how queen bees are made. You don’t become a queen because of the presence of royal jelly, but because of the absence of bee bread and the plant compounds it contains, as royal jelly itself doesn’t contain these plant compounds.
When told that the starving workers had run out of bread, legend says that French queen Marie Antoinette decreed “Let them eat cake”. Now, it’s highly unlikely that she ever actually said that, but every day in hives all across the world, honeybee queens say “let them eat bread” as a way to stop her workers from turning into queens themselves.
Sons of anarchy: the workers are revolting
It’s at this point in the story that I have to come clean and admit I lied. Or at least, I didn’t tell you the whole truth. You see, although the vast majority of worker bees do not reproduce, that’s not to say that they can not reproduce, at least, to a limited extent under certain circumstances.
Bees, and in fact all the Hymenoptera, have weird genomes. Humans, like most other animals, are diploid. That means that we have two copies of each chromosome. When we want to reproduce however, we can’t just combine a male and female cell otherwise the resulting kid would have four copies of every chromosome, which is why our egg and sperm cells are haploid - they have half the genome, or one copy of every chromosome.
The bees, wasps and ants, however, do things slightly differently. They’re what we call haplodiploid. Females are diploid, like us, and have two copies of each chromosome. Males on the other hand, are haploid; they have half the number of chromosomes of females.
When a female produces eggs, she only puts half of her genome into each egg cell - exactly the same as humans. If that egg gets fertilised by a sperm cell, that offspring now has two copies of each chromosome; congratulations, it’s a girl. However, if the egg doesn’t get fertilised, it can still hatch and develop into an adult, but it can only become a male.
This leads to some incredibly weird relationships between bee families. Male bees can only have daughters, not sons. A female is more related to her brothers than she is to her sisters. A mother is more related to her son than she is to her brother. Like I say, it gets incredibly weird.
Why all this matters though, is it means that females don’t need to have sex with a male to be able to produce sons. Any female with sufficiently developed ovaries can produce sons, whether they’re the queen or a worker. And this means conflict. The queen wants her sons to become drones, whereas each worker would rather have their own sons become drones. So, stalemate?
Not quite. While there is only one queen, there are thousands of workers. And although each worker wants her own sons to become drones, she really doesn’t want another worker’s sons - her nephews - to become drones. It’s very much the mindset of “I’m allowed to break the rules but nobody should be allowed to”. And so, a police state forms. Workers will surreptitiously lay unfertilised, male eggs in the hope that they will go unseen and will one day become a drone, while at the same time locating and destroying any eggs laid by another worker.
This conflict and policing happens in beehives all around the world, but around the Cape of Good Hope in South Africa, a much more devious uprising is taking place. The Cape honey bee is its own subspecies, and its workers aren’t just revolting, they’re mutating.
Normally when a female produces an egg, the cell has to split the number of chromosomes in half through the process of meiosis. That’s how you get two haploid egg cells, destined to either be fertilised or become male. But a new mutation has snuck into Cape honey bees that allows those two haploid cells to fuse together and form a diploid egg cell which will develop into a female. Worker bees that never have sex with males are able to produce both males and females through virgin birth.
And it gets even sneakier. Compared to normal workers, Cape honey bee workers can activate their ovaries much faster in response to dropping queen pheromone levels, and they can produce their own secretions that make them smell like a queen. Perfect adaptations to stage a coup.
The coup looks like this. If the queen dies, the level of queen pheromones in the hive drops, and that tells the workers to start making royal jelly and preparing new queens to replace her. The mutant worker takes advantage of the political instability, and gives off a whiff of royalty, producing her own queen-like pheromones, encouraging other workers to feed her enough protein to start churning out both male and female eggs that are tended to by the rest of the hive. And there you have it, the virgin queen.
But as anyone who has watched a royal drama knows, it’s not enough to establish yourself as queen. You also have to ensure the future of your daughters too. And her daughters - who are of course clones of their mother - are more than capable of finding their way in the world. These females, who remember, are unmated, fly off and find another bee hive. There they head straight for the incumbent queen and kill her, taking her place. She plays her part well; she smells like a queen, and she is able to produce female eggs like a queen, so the workers don’t realise anything is amiss. They dedicate their working lives to rearing the offspring of a completely unrelated bee, a completely different subspecies even, tending to a queen they mistakenly think is their mother.
The life of a queen may seem far better than the life of a worker, but the queen still has duties that she must perform to keep the colony alive and functioning. Her main role, is of course, to produce hundreds of eggs a day in order to maintain the number of workers and replace any that die. And although Cape honey bee workers smell like queens, and can produce daughters like queens, they are at the end of the day, still workers, and they simply don’t have the reproductive capacity of a queen. The number of workers in the hive dwindles, and without enough eggs to replace them, the colony slowly ceases to function and dies, but not before any remaining Cape honey bees fly off, ready to seize the throne in another hive.
And thus, this one mutant created a highly successful clonal dynasty - the Cape honey bee subspecies - that in a single year, 2011, managed to parasitise nearly half of all managed honey bee colonies in South Africa.
In the season 4, Kat talked about contagious cancers, such as the transmissible tumours in tasmanian devils where a single mutated cell is able to jump from one devil to another, co-opting the rest of the body to help it grow and spread. We’ve already seen the similarities between the bees in a colony and the cells in a body, and the Cape honey bee just goes to show that even societies are vulnerable to cancers from within.
References:
After a Murderous Rise to the Top, a Naked Mole-Rat Queen Reigns Supreme | Smart News
Royal Jelly Isn't What Makes a Queen Bee a Queen Bee | WIRED
Kamakura (2011) Royalactin induces queen differentiation in honeybees
Buttstedt et al. (2016) Royalactin is not a royal making of a queen
Cape honey bee - Apis mellifera capensis | University of Florida
Davies, Krebs & West (2012) An Introduction to Behavioural Ecology 4th ed.
