To take just one particular example, many ground-nesting birds perform a so-called ‘distraction display’ when a predator such as a fox approaches. The parent bird limps away from the nest, holding out one wing as though it were broken. The predator, sensing easy prey, is lured away from the nest containing the chicks. Finally the parent bird gives up its pretence and leaps into the air just in time to escape the fox’s jaws. It has probably saved the life of its nestlings, but at some risk to itself. […]

Honey bees suffer from an infectious disease called foul brood. This attacks the grubs in their cells. Of the domestic breeds used by beekeepers, some are more at risk from foul brood than others, and it turns out that the difference between strains is, at least in some cases, a behavioural one. There are so-called hygienic strains which quickly stamp out epidemics by locating infected grubs, pulling them from their cells and throwing them out of the hive. The susceptible strains are susceptible because they do not practise this hygienic infanticide. The behaviour actually involved in hygiene is quite complicated. The workers have to locate the cell of each diseased grub, remove the wax cap from the cell, pull out the larva, drag it through the door of the hive, and throw it on the rubbish tip. Doing genetic experiments with bees is quite a complicated business for various reasons. Worker bees themselves do not ordinarily reproduce, and so you have to cross a queen of one strain with a drone (= male) of the other, and then look at the behaviour of the daughter workers. This is what W. C. Rothenbuhler did. He found that all first-generation hybrid daughter hives were non-hygienic: the behaviour of their hygienic parent seemed to have been lost, although as things turned out the hygienic genes were still there but were recessive, like human genes for blue eyes. When Rothenbuhler ‘back-crossed’ first-generation hybrids with a pure hygienic strain (again of course using queens and drones), he obtained a most beautiful result. The daughter hives fell into three groups. One group showed perfect hygienic behaviour, a second showed no hygienic behaviour at all, and the third went half way. This last group uncapped the wax cells of diseased grubs, but they did not follow through and throw out the larvae. Rothenbuhler surmised that there might be two separate genes, one gene for uncapping, and one gene for throwing-out. Normal hygienic strains possess both genes, susceptible strains possess the alleles—rivals—of both genes instead. The hybrids who only went half way presumably possessed the uncapping gene (in double dose) but not the throwing-out gene. Rothenbuhler guessed that his experimental group of apparently totally non-hygienic bees might conceal a subgroup possessing the throwing-out gene, but unable to show it because they lacked the uncapping gene. He confirmed this most elegantly by removing caps himself. Sure enough, half of the apparently non-hygienic bees thereupon showed perfectly normal throwing-out behaviour.*

Hygienic bees

If the original book had had footnotes, one of them would have been devoted to explaining—as Rothenbuhler himself scrupulously did—that the bee results were not quite so neat and tidy. Out of the many colonies that, according to theory, should not have shown hygienic behaviour, one nevertheless did. In Rothenbuhler’s own words, ‘We cannot disregard this result, regardless of how much we would like to, but we are basing the genetic hypothesis on the other data.’ A mutation in the anomalous colony is a possible explanation, though it is not very likely.

Mole-crickets amplify their song to stentorian loudness by singing down in a burrow which they carefully dig in the shape of a double exponential horn, or megaphone. […]

In the course of their experiments they had occasion to introduce into magpie nests the eggs and chicks of cuckoos, and, for comparison, eggs and chicks of other species such as swallows. On one occasion they introduced a baby swallow into a magpie’s nest. The next day they noticed one of the magpie eggs lying on the ground under the nest. It had not broken, so they picked it up, replaced it, and watched. What they saw is utterly remarkable. The baby swallow, behaving exactly as if it was a baby cuckoo, threw the egg out. They replaced the egg again, and exactly the same thing happened. The baby swallow used the cuckoo method of balancing the egg on its back between its wing-stubs, and walking backwards up the side of the nest until the egg toppled out. Perhaps wisely, Alvarez and his colleagues made no attempt to explain their astonishing observation. How could such behaviour evolve in the swallow gene pool? It must correspond to something in the normal life of a swallow. Baby swallows are not accustomed to finding themselves in magpie nests. They are never normally found in any nest except their own. Could the behaviour represent an evolved anti-cuckoo adaptation? Has the natural selection been favouring a policy of counter-attack in the swallow gene pool, genes for hitting the cuckoo with his own weapons? It seems to be a fact that swallows’ nests are not normally parasitized by cuckoos. Perhaps this is why. According to this theory, the magpie eggs of the experiment would be incidentally getting the same treatment, perhaps because, like cuckoo eggs, they are bigger than swallow eggs. But if baby swallows can tell the difference between a large egg and a normal swallow egg, surely the mother should be able to as well. In this case why is it not the mother who ejects the cuckoo egg, since it would be so much easier for her to do so than the baby? The same objection applies to the theory that the baby swallow’s behaviour normally functions to remove addled eggs or other debris from the nest. Once again, this task could be—and is—performed better by the parent. The fact that the difficult and skilled egg-rejecting operation was seen to be performed by a weak and helpless baby swallow, whereas an adult swallow could surely do it much more easily, compels me to the conclusion that, from the parent’s point of view, the baby is up to no good. It seems to me just conceivable that the true explanation has nothing to do with cuckoos at all. The blood may chill at the thought, but could this be what baby swallows do to each other? Since the firstborn is going to compete with his yet unhatched brothers and sisters for parental investment, it could be to his advantage to […]. The chief objection to this theory is that it is very difficult to believe that nobody would have seen this diabolical behaviour if it really occurred. I have no convincing explanation for this. There are different races of swallow in different parts of the world. It is known that the Spanish race differs from, for example, the British one, in certain respects. The Spanish race has not been subjected to the same degree of intensive observation as the British one, and I suppose it is just conceivable that fratricide occurs but has been overlooked. […]

The physical characteristics of the calls seem to be ideally shaped to be difficult to locate. If an acoustic engineer were asked to design a sound that a predator would find it hard to approach, he would produce something very like the real alarm calls of many small songbirds. […]

Unfortunately, we know too little at present to assign realistic numbers to the costs and benefits of various outcomes in nature.

We now have some good field measurements of costs and benefits in nature, which have been plugged into particular ESS models. One of the best examples comes from great golden digger wasps in North America. Digger wasps are not the familiar social wasps of our autumn jam-pots, which are neuter females working for a colony. Each female digger wasp is on her own, and she devotes her life to providing shelter and food for a succession of her larvae. Typically, a female begins by digging a long bore-hole into the earth, at the bottom of which is a hollowed-out chamber. She then sets off to hunt prey (katydids or longhorned grasshoppers in the case of the great golden digger wasp). When she finds one she stings it to paralyse it, and drags it back into her burrow. Having accumulated four or five katydids she lays an egg on the top of the pile and seals up the burrow. The egg hatches into a larva, which feeds on the katydids. The point about the prey being paralysed rather than killed, by the way, is that they don’t decay but are eaten alive and are therefore fresh. It was this macabre habit, in the related Ichneumon wasps, that provoked Darwin to write: ‘I cannot persuade myself that a beneficent and omnipotent God would have designedly created the Ichneumonidae with the express intention of their feeding within the living bodies of Caterpillars . . .” He might as well have used the example of a French chef boiling lobsters alive to preserve the flavour. Returning to the life of the female digger wasp, it is a solitary one except that other females are working independently in the same area, and sometimes they occupy one another’s burrows rather than go to the trouble of digging a new one. Dr Jane Brockmann is a sort of wasp equivalent of Jane Goodall. She came from America to work with me at Oxford, bringing her copious records of almost every event in the life of two entire populations of individually identified female wasps. These records were so complete that individual wasp time-budgets could be drawn up. Time is an economic commodity: the more time spent on one part of life, the less is available for other parts. Alan Grafen joined the two of us and taught us how to think correctly about time-costs and reproductive benefits. We found evidence for a true mixed ESS in a game played between female wasps in a population in New Hampshire, though we failed to find such evidence in another population in Michigan. Briefly, the New Hampshire wasps either Dig their own nests or Enter a nest that another wasp has dug. According to our interpretation, wasps can benefit by entering because some nests are abandoned by their original diggers and are reusable. It does not pay to enter a nest that is occupied, but an enterer has no way of knowing which nests are occupied and which abandoned. She runs the risk of going for days in double-occupation, at the end of which she may come home to find the burrow sealed up, and all her efforts in vain—the other occupant has laid her egg and will reap the benefits. If too much entering is going on in a population, available burrows become scarce, the chance of double-occupation goes up, and it therefore pays to dig. Conversely, if plenty of wasps are digging, the high availability of burrows favours entering. There is a critical frequency of entering in the population at which digging and entering are equally profitable. If the actual frequency is below the critical frequency, natural selection favours entering, because there is a good supply of available abandoned burrows. If the actual frequency is higher than the critical frequency, there is a shortage of available burrows and natural selection favours digging. So a balance is maintained in the population. The detailed, quantitative evidence suggests that this is a true mixed ESS, each individual wasp having a probability of digging or entering, rather than the population containing a mixture of digging and entering specialists.


p. 173 . . . it seems to be only in the social insects that [the evolution of sterile workers] has actually happened.

That is what we all thought. We had reckoned without naked mole rats. Naked mole rats live in extensive networks of underground burrows. Colonies typically number 70 or 80 individuals, but they can increase into the hundreds. The network of burrows occupied by one colony can be two or three miles in total length, and one colony may excavate three or four tons of soil annually. Tunnelling is a communal activity. A face worker digs at the front with its teeth, passing the soil back through a living conveyor belt, a seething, scuffling line of half a dozen little pink animals. From time to time the face-worker is relieved by one of the workers behind. Only one female in the colony breeds, over a period of several years. Jarvis, in my opinion legitimately, adopts social insect terminology and calls her the queen. The queen is mated by two or three males only. All the other individuals of both sexes are nonbreeding, like insect workers. And, as in many social insect species, if the queen is removed some previously sterile females start to come into breeding condition and then fight each other for the position of queen. The sterile individuals are called ‘workers’, and again this is fair enough. Workers are of both sexes, as in termites (but not ants, bees and wasps, among which they are females only). What mole rat workers actually do depends on their size. The smallest ones, whom Jarvis calls ‘frequent workers’, dig and transport soil, feed the young, and presumably free the queen to concentrate on childbearing. She has larger litters than is normal for rodents of her size, again reminiscent of social insect queens. The largest nonbreeders seem to do little except sleep and eat, while intermediate-sized nonbreeders behave in an intermediate manner: there is a continuum as in bees, rather than discrete castes as in many ants. Jarvis originally called the largest nonbreeders nonworkers. But could they really be doing nothing? There is now some suggestion, both from laboratory and field observations, that they are soldiers, defending the colony if it is threatened; snakes are the main predators. There is also a possibility that they act as ‘food vats’ like ‘honeypot ants’ (see p. 171). Mole rats are homocoprophagous, which is a polite way of saying that they eat one another’s faeces (not exclusively: that would run foul of the laws of the universe). Perhaps the large individuals perform a valuable role by storing up their faeces in the body when food is plentiful, so that they can act as an emergency larder when food is scarce—a sort of constipated commissariat. To me, the most puzzling feature of naked mole rats is that, although they are like social insects in so many ways, they seem to have no equivalent caste to the young winged reproductives of ants and termites. They have reproductive individuals, of course, but these don’t start their careers by taking wing and dispersing their genes to new lands. As far as anyone knows, naked mole rat colonies just grow at the margins by expanding the subterranean burrow system. Apparently they don’t throw off long-distance dispersing individuals, the equivalent of winged reproductives. This is so surprising to my Darwinian intuition that it is tempting to speculate. My hunch is that one day we shall discover a dispersal phase which has hitherto, for some reason, been overlooked. It is too much to hope that the dispersing individuals will literally sprout wings! But they might in various ways be equipped for life above ground rather than underground. They could be hairy instead of naked, for instance. Naked mole rats don’t regulate their individual body temperatures in the way that normal mammals do; they are more like ‘cold-blooded’ reptiles. Perhaps they control temperature socially—another resemblance to termites and bees. Or could they be exploiting the well-known constant temperature of any good cellar? At all events, my hypothetical dispersing individuals might well, unlike the underground workers, be conventionally ‘warm-blooded’. Is it conceivable that some already known hairy rodent, hitherto classified as an entirely different species, might turn out to be the lost caste of the naked mole rat? There are, after all, precedents for this kind of thing. Locusts, for instance. Locusts are modified grasshoppers, and they normally live the solitary, cryptic, retiring life typical of a grasshopper. But under certain special conditions they change utterly—and terribly. They lose their camouflage and become vividly striped. One could almost fancy it a warning. If so, it is no idle one, for their behaviour changes too. They abandon their solitary ways and gang together, with menacing results. From the legendary biblical plagues to the present day, no animal has been so feared as a destroyer of human prosperity. They swarm in their millions, a combined harvester thrashing a path tens of miles wide, sometimes travelling at hundreds of miles per day, engulfing 2,000 tons of crops per day, and leaving a wake of starvation and ruin. And now we come to the possible analogy with mole rats. The difference between a solitary individual and its gregarious incarnation is as great as the difference between two ant castes. Moreover, just as we were postulating for the ‘lost caste’ of the mole rats, until 1921 the grasshopper Jekylls and their locust Hydes were classified as belonging to different species. But alas, it doesn’t seem terribly likely that mammal experts could have been so misled right up to the present day. I should say, incidentally, that ordinary, untransformed naked mole rats are sometimes seen above ground and perhaps travel farther than is generally thought. But before we abandon the ‘transformed reproductive’ speculation completely, the locust analogy does suggest another possibility. Perhaps naked mole rats do produce transformed reproductives, but only under certain conditions—conditions that have not arisen in recent decades. In Africa and the Middle East, locust plagues are still a menace, just as they were in biblical times. But in North America, things are different. Some grasshopper species there have the potential to turn into gregarious locusts. But, apparently because conditions haven’t been right, no locust plagues have occurred in North America this century (although cicadas, a totally different kind of plague insect, still erupt regularly and, confusingly, they are called ‘locusts’ in colloquial American speech). Nevertheless, if a true locust plague were to occur in America today, it would not be particularly surprising: the volcano is not extinct; it is merely dormant. But if we didn’t have written historical records and information from other parts of the world it mould be a nasty surprise because the animals would be, as far as anyone knew, just ordinary, solitary, harmless grasshoppers. What if naked mole rats are like American grasshoppers, primed to produce a distinct, dispersing caste, but only under conditions which, for some reason, have not been realized this century? Nineteenth-century East Africa could have suffered swarming plagues of hairy mole rats migrating like lemmings above ground, without any records surviving to us. Or perhaps they are recorded in the legends and sagas of local tribes?

Richard Dawkins, The Selfish Gene, 30th Anniversary Edition, 2006

Footnotes (1989 edition) are doubly indented.

Added to diary 27 June 2018