Sniffing out the brothers

This behaviour implies that workers can distinguish between their male and female siblings. How can they do this? They certainly appear to be unable to recognize the sex of eggs. However, when males grow into larvae or pupae, it becomes easier to identify them: they are larger than females and their morphologies are different. At that stage, workers can tell them apart by sight. Or perhaps by smell. To tell the truth, we are unsure how they do it, but they can make the distinction. Evidence for this is supplied by Formica exsecta, a species in which, though the queen lays equal numbers of eggs of both sexes, by the time they have become pupae, there is a large majority of females. This shows that the workers have intervened during the development of the brood to kill off the males and alter the sex ratio to their own advantage.

A very different problem is how the workers decide whether to eliminate their brothers or not. In other words, how do they work out how often their mother mated? They weren't playing gooseberry; they weren't even thought of during the mating flight. The answer lies in their sense of smell. There is a genetic component in the smell of insects, as has been shown by studies made of bees and several species of ant. When they sniff their nestmates, workers must be able to detect the diversity of odours, which depends on the number of times their mother mated. In this indirect way, they are aware of the genetic diversity within their colony: if it is extensive, it means the queen has had various mates and the workers will not alter the sex ratio, thus protecting the males from their sisters' mandibles.

Whenever fratricidal conflicts do emerge within such matriarchal societies, the males always come off second best, a plight which might make one feel sorry for them. But they have a trick that can help them avoid the fate that their sisters have in store for them: they survive by 'hiding' their sex. Over the course of evolution, they have developed a mode of disguise, which consists either of smelling like workers or queens, or of being the same size as the females. This idea may sound far-fetched; but observation of parasitical ants has shown that it is perfectly possible. Once these gate-crashers have established themselves in another colony's nest, their queen gives birth to sexual offspring even at times of the year when the resident monarch is only producing workers. This means that if the intruders want to avoid being evicted, they must not draw attention to themselves. This they do, male and female, by growing to a size which is similar to that of the workers whose nest they have occupied. This has been suggested by Peter Nonacs of the University of Los Angeles; and we have confirmed his findings in studies of the tiny Plagiolepis xene ants in the south of France. Among this parasite, sexual individuals, whether male or female, are all of a size with the workers which they exploit. If they grew any larger, they would be detected and eliminated; and if they were any smaller, they would have less chance of ever founding new colonies. So natural selection sometimes works in mysterious ways; and it is highly possible that some males have benefited from this to escape their sisters' clutch.

Males that do not resort to this survival ploy may be able to count on the protection of their mother. For queens also know a trick or two. They can, for instance, give the workers less room for manœuvre by varying the number of males and females in the eggs they lay. Red imported fire ants do this, as demonstrated by Luc Passera and Serge Aron working with our own team as well as with Edward L. Vargo, then at the University of Austin (Texas). There are colonies in which the queen gives herself complete control of the situation by producing almost exclusively male eggs, which means that since there are not enough females, the workers have no choice but to tend to the males—a second best no doubt from their point of view, but better than nothing.

It appears that, in general, queens have greater control over colony sex ratio in monogynous than in polygynous nests. When there are several queens in a colony, they compete with each other. Even if most of them produced a majority of males, it would require only one or two of the others to produce females for the workers to favour them. When there are conflicts within a dominant class, the dominated can take advantage of the situation to promote their own interests. To this general rule of societies ants are no exception.

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