A game of drones: why some bees kill their queens

In a palace intrigue worthy of George R R Martin, a new study has shown that some bee workers are queen slayers who will rise up and kill their queen if she produces the wrong sort of male offspring. The throne can then be seized by one of her daughters, who will produce the right kind of male heirs – ensuring the survival of the bloodline.

Why would bees favour some queens over others based on their sons? To understand this, we need to know a bit about the difference between male and female bees. The sons of queen bees, ants, and wasps (insects collectively known as Hymenoptera) come in two kinds.

The difference is all to do with their genetics. Humans are “diploid” organisms, meaning they have two copies (alleles) of each gene, one from each parent. Bees, however, work a little differently.

Female bees, like us, are diploid, coming from fertilised eggs with two sets of alleles. A queen must mate to produce females, because the father contributes half of the daughter’s genome.

But male bees, known as drones, are normally “haploid”, produced from the queen’s unfertilised eggs and carrying one set of alleles. The queen can produce them without ever mating.

The queen mates only once, but stores the sperm for the rest of her life. After mating, she can choose whether to fertilise any given egg, and so can control how many male and female offspring she has.

Occasionally, though, a rarer and more sinister kind of male appears, over which the queen has no control. These males are diploid, and usually sterile. They are formed when a diploid (and so rightfully female) bee’s body is fooled into becoming male. They spell disaster for a colony’s survival because they consume resources, cannot contribute to reproduction, and, like all Hymenopteran males, refuse to work.

When deciding whether to become male or female, a developing bee’s body looks at just a single gene called the “complementary sex determination” (CSD) gene. If this gene has two different alleles because it comes from a fertilised egg, the bee becomes female. But if it has only one allele because it comes from an unfertilised egg, the bee becomes male.

Normally this sex determination system works fine. But if by random chance the queen has mated with a male that carries a CSD allele identical to hers, then half her diploid offspring will only have one kind of CSD allele and become male instead of female, effectively halving the workforce of the new generation.

Existing workers are, understandably, not at all down with that.

Queens with sterile male offspring get assassinated

The researchers in the new study looked at the species Scaptotrigona depilis, a member of the stingless bees (Meliponini) native to Brazil. They identified colonies with developing sterile diploid males, as well as normal colonies to compare them with.

They introduced a new, normal, healthy queen to each nest and tracked its activity. Queens in colonies containing sterile males mysteriously died about 10 days after those males emerged.

The introduced queens in the two kinds of colony were otherwise no different from each other. This means we can rule out genetic factors that might have made them more likely to die, or might have made them inherently smell different to workers.

They weren’t the mothers of any offspring in either the experimental or control colonies, so there was no reason to think that workers in control colonies were more likely to favour their new queen than workers in experimental colonies.

Sterile males are both lazy and smelly

So why did the experimental colonies rise up and kill their new queens? The simplest explanation is that the presence of sterile diploid males, rather than anything about the queen herself, is what causes the workers to assassinate her.

In a normally functioning colony (one that hasn’t been manipulated for an experiment), this response would be extremely advantageous. If the queen is producing hungry, lazy, sterile males, then killing her allows one of her daughters to become a new queen, producing genuinely reproductive male heirs. The workers can then help the new queen perpetuate their collective genetic legacy.

How do the workers detect sterile males? The researchers showed that, to workers, normal haploid males and sterile diploid males smell different. The two distinct smells develop a short while after the males emerge. How long afterwards, do you suppose? About 10 days – precisely the point at which the queens in the experiment began “mysteriously” dying off. The smoking gun.

Why aren’t these males rooted out earlier? In honey bees (Apis mellifera), they are. Worker bees attend eggs and larvae and can easily “smell” a diploid male and kill it. But in stingless bees, eggs are sealed off in cells early in development, and workers have no contact with them until they emerge as good-for-nothing layabout males.

Ants and wasps are queen-killers too

This kind of behaviour isn’t unique; queen slaying is known in many Hymenopteran species. One example is in colonies of fire ants (Solenopsis invicta), whose workers form gangs. Each gang has its own “gang sign”, an odour produced by the combination of alleles of a particular gene, which allows the ants to identify who is in their gang. Workers from one gang will kill queens showing the wrong gang sign.

In yellowjacket wasps, which have annual lifecycles, workers will commonly slay their queen at the end of the year as she ages and her power wanes. In her prime, she produces chemical signals that suppress the workers’ ability to reproduce (even workers can produce males by laying unfertilised eggs).

Workers are OK with this, as long as the queen continues to mass-produce their brothers and sisters. But once her baby-making ability starts to decline, the sums don’t add up. They do better genetically by ending the season with a bang and laying vast numbers of their own males – and for that they need freedom from mother. One only hopes they make it quick.

Oddly, workers only kill faithful queens that mate with only one male. In species with more promiscuous queens, workers are less bloodthirsty because they are typically half siblings, not full siblings. Here, workers do not share enough genes to favour giving a leg-up to each other’s children over the queen’s offspring – however decrepit she is.

But in both these cases, the queen is slain because of her genetics, rather than her life choices. Uniquely, stingless bee workers instead exert gruesome revenge on their queen because of her actions: her unfortunate choice of mate.

The authors of the new study also suggest that the queen is unlikely to be able to distinguish good from bad mates, that is, whether or not a potential suitor shares her CSD allele. So there is no reason to suppose the queen would know she is marked for death until the moment she is assassinated in a “Red Wedding”-style ambush.

James Gilbert is a lecturer in zoology at the University of Hull. This article first appeared on The Conversation (theconversation.com)