A Sting in the Tale (16 page)

To explain this dark side, it is first essential to look into why bees are normally so sociable, and this is a little complicated. In most creatures, parents look after their offspring because their offspring carry their genes into the next generation. Parents that leave lots of offspring behind pass on many genes, so any gene which makes a parent good at producing and rearing offspring will become more and more common in successive generations. Self-evidently, the genes of parents that leave few offspring will quickly disappear. This is the basis of evolution by natural selection (of course you do not need to know or understand this to be a good parent). Some evolutionary biologists even argue that we are simply vehicles manufactured by our genes as mechanisms to help them multiply – a somewhat disconcerting thought.

At the risk of this sounding a little like a textbook, I need to explain a bit about genes and inheritance. These two words strike fear into the hearts of biology undergraduates, for they associate them with fiendishly complex exam questions such as, ‘Calculate the probability that the child of a left-handed colour-blind woman from Cardiff married to a one-legged Glaswegian with sickle-cell anaemia will have brown eyes and a limp.' I will keep this as simple as possible and there is no exam at the end. Genes are carried in chains (called chromosomes), contained within the nucleus of almost every cell in our body. Most animals, including ourselves and female bees, are diploid, meaning that we have two copies of each chromosome, and hence two copies of each gene. In humans, we happen to have twenty-three pairs of chromosomes. Female bumblebees have between twelve and nineteen pairs, depending on the species. Oddly enough, adder's-tongue fern holds the record at over 1,200 pairs, although why this rather nondescript little plant needs so many is unknown. These chromosome chains contain all the information needed to build a fully functioning human, bee or fern, a bit like a vast instruction manual.

Each gene can be seen as a recipe – they provide the information required to build a particular protein needed in the body. It is handy that we have two copies of each gene, for some are duds – the recipe contains a mistake, and so does not work. For example, roughly one in twenty-five Caucasians has a mistake in the gene which provides the recipe for a protein with the snappy name of cystic fibrosis transmembrane conductance regulator, or CFTCR. So long as we also have a good copy of this gene, we are fine. If by chance we have two duff copies, we have cystic fibrosis.

When we produce offspring, we pass to them one of each pair of chromosomes, and hence one copy of each gene, good or bad; they obtain the other copy from their other parent. To do this, we have a special type of cell division (known as meiosis), which takes place in our gonads whereby normal, diploid cells divide to produce gametes – sperm or eggs – which are haploid, meaning they have just one copy of each of the twenty-three chromosomes. During sexual reproduction, gametes from each parent fuse to produce a diploid cell, a zygote, which then divides and grows to produce a new organism. It follows from this process that each of your offspring carries 50 per cent of your genes (the remaining 50 per cent coming from their other parent). In evolutionary terms, your genes have broken even if you have two children, for on average each of your genes will have been passed on once. More than two children, and your genes might consider that they have done well for themselves. Fewer than two, and your genes might rightfully be disappointed in your performance.

In humans, one of the pairs of chromosomes determines sex; the sex chromosome comes in two types, X and Y. Your mother had two X chromosomes. Your father had an X and a Y, and your sex depends solely on whether he passed on to you his X chromosome or his Y chromosome. Under this common genetic system, you are not only 50 per cent related to your offspring, but you are also 50 per cent related to your parents and to your siblings. By extrapolation, you are 25 per cent related to your grandchildren, grandparents, aunts, uncles, nephews and nieces, and so on. The same applies to most animals, but not to bees. In bees, it is much more complicated.

Bees belong to the Hymenoptera, a huge and very successful insect group that also contains ants and wasps. It is not by coincidence that the Hymenoptera includes most of the known social insects. It is because of their rather weird genetics. In bees, sex is determined by a single gene. If an individual has two different copies of this gene, it is female. If it has two identical copies, or just one copy, it is male. Female bees, like us, have two copies of each chromosome. Male bees, typically, have just one. To produce a son, a female bee has just to lay an unfertilised egg; the haploid gamete develops into a healthy son. Sons have no father (male bees are bastards). To produce a daughter, she fertilises her egg using sperm from a male; in bumblebees this sperm had been stored inside the queen since the previous summer. So long as the copy of the sex-determining gene in the sperm is different from each of the two different copies held by the mother, then these diploid offspring will all be female. In a normal, healthy bee population there are dozens (perhaps hundreds) of different versions of this gene, so it is unlikely that the gene of the father will match either of the versions held by the mother.

One odd consequence of males being haploid is that they do not need the process of meiosis to produce haploid gametes; all of their cells are haploid, and hence all of their sperm carry exactly the same set of genes.

My apologies if you are on the verge of falling asleep. I teach this stuff every year to the third-year students at Stirling, and every year I notice that at least half the class have tuned out within five minutes, no matter how much I jump about and try to make it sound exciting. The importance of all this is that it results in some very odd patterns of relatedness. Daughters get one copy of each chromosome from their mother and one from their father, so they are 50 per cent related to their mother, and she to them. Sons get one copy of each of their mother's chromosomes, so they carry 50 per cent of her genes. Sisters must share identical genes from their father's side, and on average share 50 per cent of the genes they get from their mother; hence overall they are 75 per cent related. This is a crucial point – sister bees are more closely related to each other than they are to either their mother or their own offspring. Another strange quirk of this system is that a father is 100 per cent related to his daughters (she has all of his genes), but she is only 50 per cent related to him (half of her genes came from her mother).

If by now you are utterly confused, as I was when I first tried to get to grips with this, don't worry. All that you really need to remember is this: a female bumblebee is 50 per cent related to her daughters and sons, but 75 per cent related to her sisters. Now, why does any of this matter?

I started this slightly tedious discourse on bumblebee genetics by saying that parents look after their offspring because their offspring carry their genes. Now, put yourself in the (six very small) shoes of a worker bee in a bumblebee nest. She could try to lay her own eggs. Because she has not mated, these will be sons, which carry 50 per cent of her genes. Even supposing she had been able to mate and could produce daughters, they will also carry only 50 per cent of her genes. Alternatively, she could help to rear sisters, which carry 75 per cent of her genes. So all else being equal, the best way to increase the number of copies of her genes is to rear sisters rather than her own offspring. This, in essence, is why highly social behaviour has become common in the Hymenoptera, but is rather rare in most other organisms; their odd genetics have predisposed daughters to help their mother rear their sisters rather than trying to reproduce themselves. An ant, wasp or bee nest is a vast, tightly knit group of closely related sisters helping their mother to produce more and more sisters.

This, hopefully, explains why a bumblebee nest is so harmonious; so long as they are rearing their sisters, the worker bees should be content. They have no incentive to try to have their own offspring. The problem comes when it is time to produce sons. Somebody has to produce them; in bumblebees, the nest will die in the winter, so the only option is to make new queens and for the males to mate with them before summer's end, so that the mated queens can survive the winter. Hence, in high summer, the queen bee starts laying both fertilised (female) and unfertilised (male) eggs. Up to this point she has been releasing a pheromone signal, instructing her female offspring to develop as workers rather than queens. At about the time that she starts laying male eggs, she switches off this signal. The goal of the queen through the spring and early summer has been to build up a big workforce. Now, her aim is to use this workforce to produce as many new daughter queens and sons as she can, in the hope of ensuring that she leaves descendants in the following year (I should stress that I am not implying that the queen has actually thought this all through).

This is all very well for the queen: she is equally related to her sons and to her daughters (50 per cent), so she is content to produce both. But rearing brothers is not such an attractive proposition for her daughter workers. Since their brothers have no father, they are equivalent to half-brothers, and so they have only 25 per cent of their sisters' genes. If the nest must produce males, the workers would rather rear their own sons (to which they are 50 per cent related) than their brothers. Although the worker bees are physically unable to mate, they have perfectly functional ovaries, and can lay unfertilised eggs – which will develop into sons.

This conflict over who produces the male offspring leads to chaos. It takes a few days for the workers to detect that there are male grubs in the nest, at which point they start trying to lay their own eggs. The queen cannot tolerate this treachery, and so she sets about eating all of the workers' eggs as quickly as they are laid, thereby consuming her own grandchildren. The queen would much prefer the nest to rear her sons, to whom she is 50 per cent related, rather than her grandsons, to whom she is 25 per cent related. If she catches one of her daughters in the act of laying eggs she will attack and bite her repeatedly; being larger and stronger than her worker daughters she wins the fight easily enough, and then consumes the eggs. However, she is heavily outnumbered. She may win the first fight, and the second and third, but her nest may contain hundreds of daughters, and she cannot bully them all. Now the daughters retaliate, eating the queen's eggs – their baby brothers – and anarchy ensues.

Until recently it would have been difficult to work out who won these battles, but these days it is straightforward to use genetic markers to identify the mothers of males in a nest. Steph has done this with some of her buff-tail nests, spending hours in the lab genotyping thousands of male bees, and she has found that the vast majority of the males are sons of the queen. Other researchers have looked at other bumblebee species and generally found that workers manage to produce at most 10 per cent of males. It seems that, despite being heavily outnumbered, the queen is able to hang on to power for long enough to ensure her own reproductive success.
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Nevertheless, the running battles between the queen and her many workers take their toll, and her condition deteriorates – her wings become frayed and her fur thins as she accumulates injuries. From this stage on the nest's days are numbered, for no new workers are being produced, and with some of the existing workers battling over laying eggs in the nest, the incoming food supply dwindles. Sometimes the queen is even killed by her daughters, whilst at other times the food supply runs out and the remaining workers simply wander off, leaving their listless mother to expire amongst the ruins of her nest.

This inexorable process is not as sad as it seems. From the point of view of the queen and the genes that constructed her, even if she is finally killed by the daughters that she patiently reared, her life will have been a success if her genes persist in new queens, by now safely hibernating underground, or as sperm stored inside such queens.

CHAPTER TEN

Cuckoo Bumblebees

The Cuckoo comes in April

She kills a Queen in May

She enslaves her brood

To gather up food

And in July she dies away.

Anon.

Most people are familiar with the cuckoo's nefarious habits. Much as it may seem anthropomorphic to impose human values on a bird, it is hard not to find the cuckoo's habit of laying eggs in the nests of others rather underhand and distasteful, particularly since the baby cuckoo goes on to slaughter its nest-mates, pushing the helpless chicks out.

Far less well known, however, is the fact that many other birds, such as moorhens and various ducks, will also routinely sneak their own eggs into the nests of other birds. They behave much like a cuckoo, waiting until the nest owner is absent before swiftly depositing one or two eggs. The unsuspecting owner returns and subsequently spends time and energy looking after extra offspring not its own. This sneaky strategy's advantage is that it enables the interloper to produce more offspring than it could look after by itself.

Remarkable recent work by Carlos Lopez-Vaamonde at the Institute of Zoology in Regent's Park, London, has shown that bumblebee workers do something very similar. Lopez-Vaamonde was using DNA markers to measure how many males within the nests of buff-tailed bumblebees were produced by workers versus their queen. These nests were housed in a laboratory high up in a building, but the bees were allowed to forage freely through tubes connecting them to the outside world. He found that workers produced only 2.2 per cent of all males within their nest, with the queen producing 95.7 per cent of males. The really interesting result was that 2.1 per cent of males in these nests were not genetically related to either the queen or her daughters, but were the sons of workers from other nests. As most of the egg-laying workers in the experiment were from other experimental nests, it was easy enough to deduce that bees might have become confused and accidentally flown down the wrong tube and hence ended up in the wrong nest. After all, the nests in the experiment were all very close together, and the entrance tubes probably all looked very similar. So far, so good, but what was really remarkable was that some of the workers laying eggs in these nests had come from wild nests somewhere out in Regent's Park or in the gardens nearby. That these worker bees had somehow found their way up to the top of a building and into the experimental nests could surely not have happened by chance.