Since there is no gene flow between them as far as Y chromosomes are concerned, there could be accurate egg mimics
coexisting
with less accurate egg mimics.
Richard-Dawkins-Unweaving-the-Rainbow
A stick insect lives in a world of twigs, and its body is a representational sculpture of a twig, leaf scars, buds and all.
A fawn's pelage is a painting of the dappled pattern of sunlight filtered through trees on to the woodland floor.
A peppered moth is a model of lichen on the tree bark.
But just as art doesn't have to be literalist and representational, animals can be said to render their world in other ways: impressionistic, say, or symbolic.
An artist seeking a dramatic impression of air speed could hardly do better than the shape of a swift.
Perhaps this is because we have an intuitive understanding of streamlining; perhaps it is because we have grown used to the swept- back beauty of modem jet planes; perhaps it is because we have picked up some knowledge of the physics of turbulence and Reynolds Numbers, in which case we could say that the shape of the swift embodies coded facts about the viscosity of the air in which its ancestors flew.
Whichever is the case, we see a swift as fitting the world of high-speed airflow as a hand fits a glove, an impression enhanced when we contrast it with the floundering clumsiness of a swift stranded on the ground and unable to take off.
A mole is not literally the shape of an underground tunnel. Perhaps it is a kind of negative image of a tunnel, shaped to squeeze through it. Its hands are not literally like soil, but they resemble spades which, through experience or intuition, we can see as the functional complement of soil: spades powered by heavy muscles to work against soil. There are even more striking cases where an animal, or a part of an animal, does not literally resemble its world but fits some part of it, glove-fashion. The coiled abdomen of a hermit crab is a coded representation of the mollusc shells in which its ancestors' genes lived. Or, we could say that the hermit crab's genes contain a coded prediction about an aspect of the world in which the crab will find itself. Because modern snails and
whelks are on average the same as ancient snails and whelks, hermit crabs still fit them and survive - the prediction is fulfilled.
Species of tiny mite are specialized to ride at a precise location on the inside of the pincer-like mandibles of a particular caste of army ant workers. Another species of mite is specialized to ride on the first joint of one antenna of an army ant. Each of these mites is shaped to fit its precise habitat, as a key fits a lock (Professor C. W. Rettenmeyer informs me - to my regret - that there are not mites shaped for left antennae and other mites shaped for right antennae). Just as a key embodies (complementary or negative) information about its own lock (information without which the door cannot be opened), so the mite embodies information about its world, in this case the shape of the insect joint where it lodges. (Parasites are often very specialized keys which fit their hosts' locks in much more detail than predators, presumably because it is unusual for a predator to attack only one species of host. The distinguished biologist Miriam Rothschild has a fund of delightful examples including a 'worm which lives exclusively under the eyelids of the hippopotamus and feeds upon its tears'. )
Sometimes the fit of animal to world is intuitively clear, either to common sense or to the trained eye of the engineer. Anybody can work out why webbed feet are so common among animals that frequently enter the water - ducks, platypuses, frogs, otters and others. If you are in any doubt, put on a pair of rubber frog feet and experience the sense of immediate release when you swim. You might even wish you had been born with frog feet, until you get out of the water and try to walk in your rubber ones. My friend Richard Leakey, paleoanthropologist, conservationist and African hero, lost both his legs in a light aircraft crash. Now he has two pairs of artificial legs: one pair with shoes, extra large for stability and permanently laced for walking, and another pair with flippers for swimming. Feet that are good for one way of life are bad for another. It is hard to design an animal that can do two such different things well.
Anybody can see why otters, seals and other air-breathing animals that live in water often have nostrils that can be closed at will. Again, human swimmers often resort to artifice, in this case a sprung nose-clip like a clothes peg. Anybody watching an ant-eater feeding through a hole in a nest of ants or termites can quickly see why they have been furnished with a long thin snout and sticky tongue. This is true not just of the specialized ant-eaters of South America, but of the unrelated pangolins and aardvark of Africa, and the even less closely related numbat and very distantly related spiny ant-eaters of Australasia. It is less obvious why all mammals that eat ants or termites have a low metabolic rate - a low body
temperature compared with most mammals, and a correspondingly low rate of biochemical turnover.
Our zoologists of the future, in order to reconstruct ancestral worlds and genetic descriptions of them, will need to replace intuitive common sense with systematic research. Here's how they might proceed. Begin by
listing a set of animals which are not particularly closely related to each other but which all share an important aspect of their life. Water- dwelling mammals would be a good test case. On more than a dozen separate occasions, land-dwelling mammals have returned to make their living, either wholly or partly, in water. We know they did so independently of each other because their closer cousins still live on land. The Pyrenean desman is a kind of aquatic mole, closely related to our familiar burrowing moles. Desmans and moles are members of the order Insectivora. Other members of the Insectivora who have independently evolved to live in fresh water include water shrews, one aquatic species of the exclusively Madagascan group of tenrecs, and three species of related otter shrews. That's four separate returnings to water among the Insectivora alone. All four are closer cousins to relatives living on dry
land than they are to the other freshwater species in the list. We have to count the three otter shrews as only a single returning to water because they are related to each other and presumably are all descended from a recent aquatic ancestor.
The surviving whales probably represent at most two separate returnings to water: the toothed whales (including dolphins) and the baleen whales. The surviving dugongs and manatees are close cousins of each other, and certainly their common ancestor also lived in the sea: they too, then, represent only a single returning to the sea. Within the pig family, most live on land but hippopotamuses have partly returned to live in water. Beavers and true otters are other animals whose ancestors returned to the water. They can be directly compared with cousins who have stayed on land, say prairie dogs in the case of beavers, and badgers in the case of otters. Mink are members of the same genus as weasels and stoats (that puts them as close to each other as horses, zebras and donkeys are to each other) but they are semi-aquatic and have partially webbed feet. There is a South American water marsupial, the yapok, which can be directly compared with its land-dwelling cousins among the opossums. Among the egg-laying mammals of Australasia, the duck-billed platypuses live largely in water, the spiny ant-eaters on land. We can make a respectable list of matched pairs: each independently evolved aquatic group opposite the closest cousin we can find that has stayed on the land.
Given the list of matched pairs, we can immediately notice some obvious things. Most of the water-dwellers have at least partially webbed feet;
some have a tail that is modified into the shape of a paddle. These are obvious in the same kind of way as the long sticky tongue shared by ant- eaters. But, like the low metabolic rate shared by ant-eaters, there are probably less obvious characteristics shared by aquatic mammals as distinct from their terrestrial cousins. How shall we discover them? By a systematic statistical analysis; perhaps something like this.
Looking down our table of matched pairs, we make a large set of measurements, the same measurements for all the animals. We measure anything we can think of, with no prior expectations: pelvis width, eye radius, gut length, dozens more, all perhaps scaled as a ratio of total body size. Now throw all the measurements into the computer and invite it to work out which measurements need to be given high weighting in order to discriminate aquatic animals from their terrestrial cousins. We could calculate a number, the 'discrimination number', by summing up contributions from all the measurements, each one having been multiplied by a weighting factor. The computer adjusts the weighting given to each measurement, in order to maximize the difference, in the final sum, between aquatic mammals and their terrestrial opposite numbers. The foot webbing index will presumably emerge from the analysis with a strong weighting. The computer will discover that it pays - if you are trying to maximize the difference between aquatic and terrestrial animals - to multiply the webbing index by a high number before adding it to the discrimination number. Other measurements - things that mammals share without regard to the wetness of their world - will need to be multiplied by zero in order to eliminate their irrelevant and confusing contribution to the weighted sum.
At the end of the analysis we look down the weightings of all our measurements. Those that emerge with high weightings, like the foot webbing index, are the ones that have something to do with the wateriness of the way of life. Webbiness is obvious. What we hope is that the analysis will uncover other important discriminators that are not so obvious. Biochemical measures, for instance. When we have found them, we can then scratch our heads and wonder what connection they have with living in water or on land. This may suggest hypotheses for further research. Even if it doesn't, any measurement that gives us a statistically significant difference between animals that have adopted some way of life and their cousins that have not is very likely to be telling us something important about that way of life.
We can do the same thing with genes. Without any prior hypotheses about what the genes are doing, we make a systematic search for genetic resemblances between unrelated aquatic animals, which are not shared by their terrestrial close cousins. If we find any strong and statistically significant effects, even if we don't understand what those genes are
doing, I would say that what we are looking at might be regarded as a genetic description of watery worlds. Natural selection, to repeat, works as an averaging computer, doing the equivalent of a calculation that is not unlike the calculations we have just programmed our manmade computer to perform. Often a species embraces various ways of life, which may be radically different from each other. A caterpillar, and the butterfly it becomes, are members of the same species, yet our zoologist's reconstruction of their two ways of life would be utterly different. Caterpillar and butterfly contain exactly the same set of genes, and the genes must describe both environments, but separately. Presumably many of them are turned on in the plant-chewing, growing, caterpillar phase, and a largely different set of genes are turned on in the adult, reproductive, nectar-eating phase.
Male and female of most species live in at least somewhat different ways. The differences are pushed to extremes in angler fish, where the male appends himself as a tiny parasitic protuberance on the female's massive body. In most species, including ourselves, both male and female contain most of the genes for being either male or female. The differences lie in which genes are turned on. We all have genes for making penises and genes for making uteruses, regardless of our sex. ('Sex' is correct, by the way, not 'gender'. Gender is a grammatical technical term, applied to words not creatures. In German, a girl's gender is neuter but her sex female. Amerindian languages typically have two genders, animate and inanimate. The association of gender with sex in some groups of languages is incidental. It is quite a good joke that the politically inspired euphemism - saying gender when you mean sex - is consequently a piece of Western Imperialism. ) Our future zoologist reading the body of either a male or a female would get an incomplete picture of the ancestral worlds of the species. On the other hand, the genes of any member of the species would more nearly suffice to reconstruct a complete picture of the range of ways of life that the species has experienced.
Parasitic cuckoos are an oddity, and a fascinating one from the point of view of the Genetic Book of the Dead. As is well known, they are reared by foster parents of a species not their own. They never rear their own young. Not all are reared by the same foster species. In Britain, some are reared by meadow pipits, some by reed warblers, fewer by robins, some by a variety of other species, but the largest number are reared by dunnocks (hedge sparrows). As it happens, our foremost specialist on dunnocks and the author of Dunnock Behaviour and Social Evolution (1992) is also today's leading investigator of cuckoo biology, Nicholas Davies of Cambridge University. I shall base my account on the work of Davies and his colleague Michael Brooke because it lends itself especially well to being cast in the language of species 'experience' of ancestral
worlds. Unless otherwise stated I shall refer to the common cuckoo, Cuculus canorzis, in Britain.
Although they make mistakes on 10 per cent of occasions, a female cuckoo normally lays in the same kind of nest as her mother, her maternal grandmother, her maternal maternal great grandmother, and
so on. Presumably young females learn the characteristics of their foster nest and seek it out when their own time comes to lay. So, as far as females are concerned, there are dunnock cuckoos, reed warbler cuckoos, meadow pipit cuckoos, and so on, and they share this attribute with
their female-line relatives. But these are not separate species, not even separate races in the normal sense of the word. They are called 'gentes' (singular 'gens'). The reason a gens is not a true race or species is that male cuckoos don't belong to a gens. Since males don't lay eggs, they never have to choose a foster nest. And when a male cuckoo comes to mate, he just mates with a female cuckoo irrespective of her gens, and regardless of the foster species that reared either of them. It would follow from this that there is gene flow between the gentes. Males carry genes from one female gens to another. A female's mother, maternal grandmother and maternal maternal great grandmother will all belong to the same gens. But her paternal grandmother, both her paternal great grandmothers, and all her female ancestors to whom she is linked via
any male ancestor, could belong to any gens. From the point of view of gene 'experience', the consequence is very interesting. Recall that, in birds, it is the female sex that has the unequal sex chromosomes, X and Y, while male birds have two X chromosomes. Think what this means for the ancestral experience of genes on a Y chromosome. Since it passes unswervingly down the female line, never straying into the paths of male experience, a Y chromosome stays strictly within one gens. It is a dunnock cuckoo Y chromosome or a meadow pipit cuckoo Y chromosome. Its foster parent 'experience' is the same from generation to generation.
In this respect it differs from all other genes in the cuckoo, for they have all done time in male bodies and have hence shuffled freely around the female gentes, experiencing them all in proportion to their frequency.
In our language of genes as 'descriptions' of ancestral environments, most cuckoo genes will be in a position to describe those features that are shared by the complete range of foster nests that the species has parasitized. Y chromosome genes, uniquely, will describe only one type of foster nest, one species of foster parent. This means that Y chromosome genes, in a way that is not possible for other cuckoo genes, will be in a position to evolve specialized tricks for surviving in their own particular foster species' nest. What sort of tricks? Well, cuckoo eggs show at least some tendency to mimic the eggs of their foster species. Cuckoo eggs laid in meadow pipit nests are like large meadow pipit eggs. Cuckoo eggs laid in reed warbler nests are like large reed warbler eggs. Cuckoo eggs laid in
pied wagtail nests resemble pied wagtail eggs. Presumably this benefits the cuckoo eggs, which might otherwise be rejected by the foster parents. But think what it must mean from the genes' point of view.
If the genes for egg colour were on any chromosomes but the Y chromosome, they would be carried via males into the bodies of females belonging to the full assortment of gentes. This means they would be carried into the full range of host nests and there would be no consistent natural selection pressure to mimic one egg type more than another. It would be difficult for their eggs, in these circumstances, to mimic any but the most generalized features of all host eggs. Although there is no direct evidence, it is therefore reasonable to guess that the specific egg mimicry genes sit on the cuckoo Y chromosome. Females will then carry them, generation after generation, into nests of the same host. Their ancestral 'experience' will all be with the discriminating eyes of the same host, and those eyes will exert the selection pressure that steers their colour and spot pattern towards mimicry of host eggs.
There is a conspicuous exception. Cuckoo eggs laid in dunnock nests do not resemble dunnock eggs. They are no more variable among
themselves than eggs laid in reed warbler or meadow pipit nests; their colour is distinctive of the dunnock gens of cuckoos, and they don't
much resemble the eggs of any other gens, but they don't resemble dunnock eggs either. Why is this? It might be-thought that dunnock eggs, being a uniform pale blue, are harder to mimic than meadow pipit or
reed warbler eggs. Perhaps cuckoos just lack the physiological equipment to make plain blue eggs? I'm always suspicious of such last-resort theories, and in this case there is evidence against it. In Finland there is a gens of cuckoo that parasitizes redstarts, which also have plain blue eggs. These cuckoos, which belong to the same species as our British ones, succeed beautifully in matching redstart eggs. This surely shows that the failure of British cuckoos to mimic dunnock eggs cannot be put down to inherent incapacity to produce the unspeckled blue colour. Davies and Brooke believe that the true explanation lies in the recency of the relationship between dunnocks and cuckoos. Cuckoos run arms races in evolutionary time with each host species and the gens we are looking at has only recently 'invaded' dunnocks. Consequently,
dunnocks haven't yet had time to evolve counter-weapons. And dunnock cuckoos either haven't had time to evolve eggs that mimic dunnocks, or they don't yet need to because dunnocks haven't evolved the habit of discriminating foreign eggs from their own. In the language of this chapter, neither the dunnock gene pool nor the cuckoo gene pool (or rather, the Y chromosome of the dunnock cuckoo gens) has had enough experience of the other to evolve counter-weapons. Perhaps dunnock cuckoos are still adapted to outwit a different foster species, the one that their female ancestor left when she laid the first egg in a dunnock nest.
Meadow pipits, reed warblers and pied wagtails, on this view, are enemies of their respective gentes of cuckoos. There has been plenty of time for a build-up of weaponry on both sides. The hosts have built up keen eyes for an impostor egg and the cuckoos possess correspondingly cunning disguises for their eggs. Robins are an intermediate case. Their cuckoos lay eggs which are slightly robin-like, but not very. Perhaps the arms race between robins and the robin gens of cuckoos is of intermediate antiquity. On this view, the Y chromosomes of robin cuckoos are somewhat experienced, but their description of recent (robin) ancestral environments is still sketchy and contaminated by earlier descriptions of other species, previously 'experienced'.
Davies and Brooke did experiments deliberately putting extra eggs, of various kinds, in nests belonging to different species of birds. They wanted to see which species would accept, or reject, strange eggs. Their hypothesis was that species that have been through an arms race with cuckoos would, as a consequence of their genetic 'experience', be most likely to reject foreign eggs. One way to test this was to look at species which are not even suitable as cuckoo hosts. Baby cuckoos need to eat insects or worms. Species that feed their young on seeds, or species that nest in holes that female cuckoos can't reach, have never been at risk. Davies and Brooke predicted that such birds would not worry if they experimentally introduced strange eggs into their nests. And so it proved. Species that are suitable for cuckoos, however, like chaffinches, song thrushes and blackbirds, showed a stronger tendency to reject the experimental eggs that Davies and Brooke, playing cuckoo, placed in their nests. Flycatchers are potentially vulnerable in that they feed their young on a cuckoo-friendly diet. But whereas spotted flycatchers have open and accessible nests, pied flycatchers nest in holes which female cuckoos are too large to penetrate. Sure enough, when the experimenters dumped foreign eggs in their nests, pied flycatchers, with their 'inexperienced' gene pools, accepted foreign eggs without protest; spotted flycatchers, by contrast, rejected them, suggesting that their gene pools were wise to the cuckoo menace from long ago.
Davies and Brooke did similar experiments with species that cuckoos actually do parasitize. Meadow pipits, reed warblers and pied wagtails usually rejected artificially added eggs. As befits the 'lack of ancestral experience' hypothesis, dunnocks did not; nor did wrens. Robins and sedge warblers were intermediate. At the other extreme, reed buntings, which are suitable for cuckoos but not much parasitized by them, showed total rejection of foreign eggs. No wonder cuckoos don't parasitize them. Davies and Brooke's interpretation would presumably be that reed buntings have come out the other side of a long ancestral arms race with cuckoos, which they eventually won. Dunnocks are near the beginning of
their arms race. Robins are slightly more advanced in theirs. Meadow pipits, reed warblers and pied wagtails are in the middle of theirs. When we say dunnocks have only just begun their arms race with cuckoos, 'only just' has to be interpreted with evolutionary timescales in mind. By human standards the association could still be quite old. The Oxford English Dictionary quotes a 1616 reference to the Heisugge (archaic word for hedge sparrow or dunnock) as 'a bird which hatcheth the Cuckooes egges'. Davies notes the following lines in King Lear I, iv, written a decade earlier:
For, you trow, nuncle,
The hedge-sparrow fed the cuckoo so long,
That its had it head bit off by it young.
And in the fourteenth century Chaucer wrote of the cuckoo's treatment of the dunnock in The Parliament of Fowls:
'Thou mortherere of the hey sage on the braunche That broughte the forth, thow rewthelees glotoun! '
Although dunnock, hedge sparrow and heysoge are all given as synonyms in the dictionary, I can't help wondering how far we should rely on medieval ornithology. Chaucer himself was usually a rather precise user of language, but nevertheless the name sparrow has at times been given to what today is technically called an LBB (little brown bird). This may have been Shakespeare's meaning in the following, from Henry IV Part I, V, i:
And, being fed by us, you used us so
As that ungentle gull the cuckoo's bird,
Useth the sparrow - did oppress our nest
Grew by our feeding to so great a bulk
That even our love durst not come near your sight For fear of swallowing;
Sparrow, on its own, would nowadays mean the house sparrow, Passer domesticus, which is never parasitized by cuckoos. Despite its alternative name hedge sparrow, the dunnock, Prunella modularis, is unrelated; it is a 'sparrow' only in the loose sense of being a little brown bird. But
anyway, even if we take Chaucer's evidence as showing that the arms race between cuckoos and dunnocks really does go back at least to the fourteenth century, Davies and Brooke cite theoretical calculations, taking into account the comparative rarity of cuckoos, suggesting that this is still sufficiently recent in evolutionary terms to account for the apparent naivety of dunnocks when faced with cuckoos.
Before we leave cuckoos, here's an interesting thought. There could be, simultaneously existing, more than one gens of, say, robin cuckoos, who have built up their egg mimicry. ' independently.
Since there is no gene flow between them as far as Y chromosomes are concerned, there could be accurate egg mimics coexisting with less accurate egg mimics. All are capable of mating with the same males but they don't share the same Y chromosomes. The accurate mimics would be descended from a female who moved into parasitizing robins a long time ago. The less accurate ones would be descended from a different female who moved into robins, possibly from a different predecessor host species, more recently.
Ants, termites and other social insect species are odd in a different way. They have sterile workers, often divided into several 'castes' - soldiers, media (middle-sized) workers, minor (small) workers, and so on. Every worker, whatever its caste, contains the genes that could have turned it into any other caste. Different sets of genes are switched on under different rearing conditions. It is by regulating these rearing conditions that the colony engineers a useful balance of different castes. Often the differences among castes are dramatic.
In the Asian ant species Pheidologeton diversus, the large worker caste (specialized for bulldozing smooth paths for other colony members) is 500 times heavier than the small caste, who do all the normal duties of a worker ant. The same set of genes equips a larva to grow up into either a Brobdingnagian or a Lilliputian, depending upon which ones are switched on. Honeypot ants are immobile storage vats, abdomens pumped up with nectar to transparent yellow spheres, hanging from the ceiling of the nest. The normal duties of an ants' nest, defence, foraging and, in this case, filling up the living vats, are done by normal workers whose abdomens are not swollen. The normal workers have genes that equip them to be honeypots, and honeypots, as far as their genes are concerned, could equally well be normal workers. As in the case of male and female, the visible differences in bodily form depend upon which genes are switched on. In this case it is determined by environmental factors, perhaps diet. Once again, the zoologist of the future could read out from the genes, but not the body, of any one member of the species a complete picture of the disparate lives of the different castes.
The European snail Cepaea nemoralis comes in a number of colours and patterns. The background shell colour can be any of six distinct shades (in order of dominance, in the technical genetic sense): brown, dark pink, light pink, very pale pink, dark yellow, light yellow. Overlaying this, there may be any number of stripes from zero to five. Unlike the case of the social insects, it is not true that every individual snail is genetically equipped to assume any of the different forms. Nor are these differences among snails determined by different environments of upbringing. Striped snails have genes that determine their number of stripes, dark pink individuals have genes that make them dark pink. But all the kinds can mate with each other.
The reasons for the persistence of many different types of snail (polymorphism), as well as the detailed genetics of the polymorphism itself, have been exhaustively studied by the English zoologists A. J. Cain and the late P. M. Sheppard with their school. A major part of the evolutionary explanation is that the species ranges over different habitats - woodland, grassland, bare soil - and you need a different colour pattern to be camouflaged against birds in each place. Beechwood snails contain an admixture of genes from grassland because they interbreed at the margins. A chalk downland snail has some genes that previously survived in the bodies of woodland ancestors; and their legacy, depending on the other genes in the snail, may be stripes. Our zoologist of the future would need to look at the gene pool of the species as a whole to reconstruct the full range of its ancestral worlds.
Just as Cepaea snails range over different habitats in space, so the ancestors of any species have changed their way of life from time to time. House mice, Mus musculus, today live almost exclusively in or around human habitations, as unwanted beneficiaries of human agriculture. But by evolutionary standards their way of life is recent. They must have fed on something else before there was human agriculture. Doubtless that something was sufficiently similar for their genetic skills to be pressed into service when the agricultural bonanza came along. Mice and rats have been described as animal weeds (incidentally, a good piece of poetic imagery, genuinely illuminating). They are generalists, opportunists, carrying genes that helped their ancestors to survive through probably a considerable range of ways of life; and pre-agricultural genes are in them yet. Anybody attempting to 'read' their genes may find a confusing palimpsest of ancestral world descriptions.
From earlier still, the DNA of all mammals must describe aspects of very ancient environments as well as more recent ones. The DNA of a camel was once in the sea, but it hasn't been there for a good 300 million years. It has spent most of recent geological history in deserts, programming bodies to withstand dust and conserve water. Like sandbluffs carved into
fantastic shapes by the desert winds, like rocks shaped by ocean waves, camel DNA has been sculpted by survival in ancient deserts, and even more ancient seas, to yield modern camels. Camel DNA speaks - if only we could understand the language - of the changing worlds of camel ancestors. If only we could read the language, the DNA of tuna and starfish would have 'sea' written into the text. The DNA of moles and earthworms would spell 'underground'. Of course all the DNA would spell many other things as well. Shark and cheetah DNA would spell 'hunt', as well as separate messages about sea and land. Monkey and cheetah DNA would spell 'milk'. Monkey and sloth DNA would spell 'trees'. Whale and dugong DNA presumably describes very ancient seas, fairly ancient lands and more recent seas: complicated palimpsests again.
Features of the environment that occur frequently or importantly are heavily emphasized or 'weighted' in the genetic description, compared with rare or trivial features. Environments that lie in the remote past have a different weighting from recent ones, presumably lower, though not in any obvious way. Environments that lasted a long time in the species' history will have a more prominent weighting in the genetic description than environmental events that, however drastic they may have seemed at the time, were geological flashes in the pan.
It has been poetically suggested that the remote marine apprenticeship of all land life is reflected in the biochemistry of the blood, which is said to resemble a primeval salt sea. Or the liquid in a reptile's egg has been described as a private pond, relic of the actual ponds in which the larvae of distant, amphibious ancestors would have grown. To the extent that animals and their genes bear such a stamp of ancient history it will be for good functional reasons. It won't be history for history's sake. Here is the kind of thing I mean by this. When our remote ancestors lived in the sea, many of our biochemical and metabolic processes became geared to the chemistry of the sea - and our genes became a description of marine chemistry - for functional reasons. But (this is an aspect of our 'selfish Cooperator' argument) biochemical processes become geared not only to the external world but to each other. The world to which they became fitted included the other molecules in the body and the chemical processes in which they partook. There after, when remote descendants of these marine animals moved out on to the land and became gradually more and more fitted to a dry airy world, the old mutual adaptation of biochemical processes to each other - and incidentally to the chemical 'memory' of the sea - persisted. Why should it not, when the different kinds of molecules in the cells and blood so greatly outnumber the different kinds of molecules encountered in the outside world? It is only in a very indirect sense that the genes spell out descriptions of ancestral environments. What they directly describe, after being translated into the parallel language of protein molecules, is instructions for individual
embryonic development. It is the gene pool of the species as a whole that becomes carved to fit the environments that its ancestors have encountered - which is why I said that the species is a statistical averaging device. It is in this indirect sense that our DNA is a coded description of the worlds in which our ancestors survived. And isn't it an arresting thought? We are digital archives of the African Pliocene, even of Devonian seas; walking repositories of wisdom out of the old days. You could spend a lifetime reading in this ancient library and die unsated by the wonder of it.
11
REWEAVING THE WORLD
Since my education began I have always had things described to me with their colors and sounds, by one with keen senses and a fine feeling for the significant.
Therefore, I habitually think of things as colored and resonant Habit accounts for part
The soul sense accounts for another part.
The brain with its five-sensed construction asserts its right and accounts for the rest
Inclusive of all, the unity of the world demands that color be kept in it whether I have cognizance of it or not.
Rather than be shut out, I take part in it by discussing it, happy in the happiness of those near to me who gaze at the lovely hues of the sunset or the rainbow.
HELEN KELLER, The Story of My Life (1902)
Where the gene pool or a species is sculpted into a set of models of ancestral worlds, the brain of an individual houses a parallel set of models of the animal's own world.
Both are equivalent to descriptions of the past, and both are used to aid survival into the future. The difference is one of timescale and of relative privacy. The genetic description is a collective memory belonging to the species as a whole, going back into the indefinite past. The memory of the brain is private and contains the individual's experiences since it was born.
Our subjective knowledge of a familiar place does indeed feel to us like a model of the place. Not an accurate scale model, certainly less accurate
than we think it is, but a serviceable model for the purposes required. One way to approach this idea was proposed some years ago by the Cambridge physiologist Horace Barlow, incidentally a direct descendant of Charles Darwin. Barlow is especially interested in vision and his argument starts from the realization that to recognize an object is a much more difficult problem than we, who seem to see so effortlessly, ordinarily understand.
For we are blissfully unaware of what a formidably clever thing we do every second of our waking lives when we see and recognize objects. The sense organs' task of unweaving the physical stimuli that bombard them is easy compared with the brain's task of reweaving an internal model of the world that it can then make use of. The argument holds for all our sensory systems, but I'll stick mostly to vision because that is the one that means the most to us. Think what a problem our brain solves when it recognizes something, say a letter A. Or think of the problem of recognizing a particular person's face. By long in-group convention, the hypothetical face we are talking about is assumed to belong to the grandmother of the distinguished neurobiologist J. Lettvin, but substitute any face you know, or indeed any object you can recognize. We are not concerned here with subjective consciousness, with the philosophically hard problem of what it means to be aware of your grandmother's face. Just a cell in the brain which fires if and only if the grandmother's face appears on the retina will do nicely for a start, and it is very difficult to arrange. It would be easy if we could assume that the face would always fall exactly on a particular part of the retina. There could be a keyhole arrangement, with a grandmother-shaped region of cells on the retina wired up to a grandmother-signalling cell in the brain. Other cells - members of the 'anti-keyhole' - would have to be wired up in inhibitory-fashion, otherwise the central nervous cell would respond to a white sheet just as strongly as to the grandmother's face which - together with all other conceivable images - it would necessarily 'contain'. The essence of responding to a key image is to avoid responding to everything else.
The keyhole strategy is ruled out by sheer force of numbers.
Even if Lettvin needed to recognize nothing but his grandmother, how could he cope when her image falls on a different part of the retina? How cope with her image's changing size and shape as she approaches or recedes, as she turns sideways, or cants to the rear, as she smiles or as she frowns? If we add up all possible combinations of keyholes and anti- keyholes, the number enters the astronomical range. When you realize that Lettvin can recognize not only his grandmother's face but hundreds of other faces, the other bits of his grandmother and of other people, all the letters of the alphabet, all the thousands of objects to which a normal person can instantly give a name, in all possible orientations and
apparent sizes, the explosion of triggering cells gets rapidly out of hand. The American psychologist Fred Attneave, who had come up with the same general idea as Barlow, dramatized the point by the following calculation: if there were just one brain cell to cope, keyhole fashion, with each image that we can distinguish in all its presentations, the volume of the brain would have to be measured in cubic light years.
How then, with a brain capacity measured only in hundreds of cubic centimetres, do we do it? The answer was proposed in the 1950s by Barlow and Attneave independently. They suggested that nervous systems exploit the massive redundancy in all sensory information. Redundancy is jargon from the world of information theory, originally developed by engineers concerned with the economics of telephone line capacity. Information, in the technical sense, is surprise value, measured as the inverse of expected probability. Redundancy is the opposite of information, a measure of unsurprisingness, of old-hatitude. Redundant messages or parts of messages are not informative because the receiver, in some sense, already knows what is coming. Newspapers do not carry headlines saying, 'The sun rose this morning'. That would convey almost zero information. But if a morning came when the sun did not rise, headline writers would, if any survived, make much of it. The information content would be high, measured as the surprise value of the message. Much of spoken and written language is redundant - hence possible condense telegraphese: redundancy lost, information preserved.
Everything that we know about the world outside our skulls comes to us via nerve cells whose impulses chatter like machine guns. What passes along a nerve cell is a volleying of 'spikes', impulses whose voltage is
fixed (or at least irrelevant) but whose rate of arriving varies meaningfully. Now let's think about coding principles. How would you translate information from the outside world, say, the sound of an oboe or the temperature of a bath, into a pulse code? A first thought is a simple rate code: the hotter the bath, the faster the machine gun should fire. The brain, in other words, would have a thermometer calibrated in pulse rates. Actually, this is not a good code because it is uneconomical with pulses. By exploiting redundancy, it is possible to devise codes that convey the same information at a cost of fewer pulses. Temperatures in the world mostly stay the same for long periods at a time. To signal 'It is hot, it is hot, it is still hot. . . ' by a continuously high rate of machine-gun pulses is wasteful; it is better to say, 'It has suddenly become hot' (now you can assume that it will stay the same until further notice).
And, satisfyingly, this is what nerve cells mostly do, not just for signalling temperature but for signalling almost everything about the world. Most nerve cells are biased to signal changes in the world. If a trumpet plays a long sustained note, a typical nerve cell telling the brain
about it would show the following pattern of impulses: Before the trumpet starts, low firing rate; immediately after the trumpet starts, high firing rate; as the trumpet carries on sustaining its note, the firing rate dies away to an infrequent mutter; at the moment when the trumpet stops, high firing rate, dying away to a resting mutter again. Or there might be one class of nerve cells that fire only at the onset of sounds and a different class of cells that fire only when sounds go off. Similar exploitation of redundancy - screening out of the sameness in the world - goes on in cells that tell the brain about changes in light, changes in temperature, changes in pressure. Everything about the world is signalled as change, and this is a major economy.
But you and I don't seem to hear the trumpet die away. To us the trumpet seems to carry on at the same volume and then to stop abruptly. Yes, of course. That's what you'd expect because the coding system is ingenious. It doesn't throw away information, it only throws away redundancy. The brain is told only about changes, and it is then in a position to reconstruct the rest. Barlow doesn't put it like this, but we could say that the brain constructs a virtual sound, using the messages supplied by the nerves coming from the ears. The reconstructed virtual sound is complete and unabridged, even though the messages
themselves are economically stripped down to information about changes. The system works because the state of the world at a given time is
usually not greatly different from the preceding second. Only if the world changed capriciously, randomly and frequently, would it be economical for sense organs to signal continuously the state of the world. As it is, sense organs are set up to signal, economically, the discontinuities in the worlds and the brain, assuming correctly that the world doesn't change capriciously and at random, uses the information to construct an
internal virtual reality in which the continuity is restored.
The world presents an equivalent kind of redundancy in space, and the nervous system uses the corresponding trick. Sense organs tell the brain about edges and the brain fills in the boring bits between. Suppose you are looking at a black rectangle on a white background. The whole scene is projected on to your retina - you can think of the retina as a screen covered with a dense carpet of tiny photocells, the rods and cones. In theory, each photocell could report to the brain the exact state of the light falling upon it. But the scene we are looking at is massively redundant. Cells registering black are overwhelmingly likely to be surrounded by other cells registering black. Cells registering white are nearly all surrounded by other white-signalling cells. The important exceptions are cells on edges. Those on the white side of an edge signal white themselves and so do their neighbours that sit further into the white area. But their neighbours on the other side are in the black area. The brain can theoretically reconstruct the whole scene if just the retinal
cells on edges fire. If this could be achieved there would be massive savings in nerve impulses. Once again, redundancy is removed and only information gets through.
Elegantly, the economy is achieved in practice by the mechanism known as lateral inhibition'. Here's a simplified version of the principle, using our analogy of the screen of photocells. Each photocell sends one long wire to the central computer (brain) and also short wires to its immediate neighbours in the photocell screen. The short connections to the neighbours inhibit them, that is, turn down their firing rate. It is easy to see that maximal firing will come only from cells that lie along edges, for they are inhibited from one side only. Lateral inhibition of this kind is common among the low-level units of both vertebrate and invertebrate eyes.
Once again, we could say that the brain constructs a virtual world which is more complete than the picture relayed to it by the senses. The information which the senses supply to the brain is mostly information about edges. But the model in the brain is able to reconstruct the bits between the edges. As in the case of discontinuities in time, an economy is achieved by the elimination - and later reconstruction in the brain - of redundancy. This economy is possible only because uniform patches exist in the world. If the shades and colours in the world were randomly dotted about, no economical remodeling would be possible.
Another kind of redundancy stems from the fact that many lines in the real world are straight, or curved in smooth and therefore predictable (or mathematically reconstructable), ways. If the ends of a line are specified, the middle can be filled in using a simple rule that the brain already 'knows'. Among the nerve cells that have been discovered in the brains of mammals are the so-called 'line-detectors', neurones that fire whenever a straight line, aligned in a particular direction, falls on a particular place in the retina, the so-called 'retinal field' of the brain cell. Each of these line-detector cells has its own preferred direction. In the cat brain, there are only two preferred directions, horizontal and vertical, with an approximately equal number favouring each direction; however, in monkeys other angles are accommodated. From the point of view of the redundancy argument, what is going on here is as follows. In the retina, all the cells along a straight line fire and most of these impulses are redundant. The nervous system economizes by using a single cell to register the line, labelled with its angle. Straight lines are economically specified by their position and direction alone, or by their ends, not by the light value of every point along their length. The brain reweaves a virtual line in which the points along the line are reconstructed.
However, if a part of a scene suddenly detaches itself from the rest and starts to crawl over the background, it is news and should be signalled. Biologists have indeed discovered nerve cells that are silent until something moves against a still background. These cells don't respond when the entire scene moves - that would correspond to the sort of apparent movement the animal would see when it itself moves. But movement of a small object against a still background is information-rich and there are nerve cells tuned to detect it. The most famous of these are the so-called 'bug-detectors' discovered in frogs by Lettvin (he of the grandmother) and his colleagues. A bug-detector is a cell which is apparently blind to everything except the movement of small objects against their background. As soon as an insect moves in the field covered by a bug-detector, the cell immediately initiates massive signalling and the frog's tongue is likely to shoot out to catch the insect. To a sufficiently sophisticated nervous system, though, even the movement of a bug is redundant if it is movement in a straight line. Once you've been told that a bug is moving steadily in a northerly direction, you can assume that it will continue to move in this direction until further notice. Carrying the logic a step further, we should expect to find higher-order movement detector cells in the brain that are especially sensitive to change in movement, say, change in direction or change in speed. Lettvin and his colleagues found a cell that seems to do this, again in the frog. In their paper in Sensory Communication (1961) they describe a particular experiment as follows:
Let us begin with an empty gray hemisphere for the visual field-There is usually no response of the cell to turning on and off the illumination. It is silent. We bring in a small dark object say 1 to 2 degrees in diameter, and at a certain point in its travel, almost anywhere in the field, the cell suddenly 'notices' it. Thereafter, wherever that object is moved it is tracked by the cell. Every time it moves, with even the faintest jerk, there is a burst of impulses that dies down to a mutter that continues as long as the object is visible. If the object is kept moving, the bursts signal discontinuities in the movement, such as the turning of corners, reversals, and so forth, and these bursts occur against a continuous background mutter that tells us the object is visible to the cell.
A mole is not literally the shape of an underground tunnel. Perhaps it is a kind of negative image of a tunnel, shaped to squeeze through it. Its hands are not literally like soil, but they resemble spades which, through experience or intuition, we can see as the functional complement of soil: spades powered by heavy muscles to work against soil. There are even more striking cases where an animal, or a part of an animal, does not literally resemble its world but fits some part of it, glove-fashion. The coiled abdomen of a hermit crab is a coded representation of the mollusc shells in which its ancestors' genes lived. Or, we could say that the hermit crab's genes contain a coded prediction about an aspect of the world in which the crab will find itself. Because modern snails and
whelks are on average the same as ancient snails and whelks, hermit crabs still fit them and survive - the prediction is fulfilled.
Species of tiny mite are specialized to ride at a precise location on the inside of the pincer-like mandibles of a particular caste of army ant workers. Another species of mite is specialized to ride on the first joint of one antenna of an army ant. Each of these mites is shaped to fit its precise habitat, as a key fits a lock (Professor C. W. Rettenmeyer informs me - to my regret - that there are not mites shaped for left antennae and other mites shaped for right antennae). Just as a key embodies (complementary or negative) information about its own lock (information without which the door cannot be opened), so the mite embodies information about its world, in this case the shape of the insect joint where it lodges. (Parasites are often very specialized keys which fit their hosts' locks in much more detail than predators, presumably because it is unusual for a predator to attack only one species of host. The distinguished biologist Miriam Rothschild has a fund of delightful examples including a 'worm which lives exclusively under the eyelids of the hippopotamus and feeds upon its tears'. )
Sometimes the fit of animal to world is intuitively clear, either to common sense or to the trained eye of the engineer. Anybody can work out why webbed feet are so common among animals that frequently enter the water - ducks, platypuses, frogs, otters and others. If you are in any doubt, put on a pair of rubber frog feet and experience the sense of immediate release when you swim. You might even wish you had been born with frog feet, until you get out of the water and try to walk in your rubber ones. My friend Richard Leakey, paleoanthropologist, conservationist and African hero, lost both his legs in a light aircraft crash. Now he has two pairs of artificial legs: one pair with shoes, extra large for stability and permanently laced for walking, and another pair with flippers for swimming. Feet that are good for one way of life are bad for another. It is hard to design an animal that can do two such different things well.
Anybody can see why otters, seals and other air-breathing animals that live in water often have nostrils that can be closed at will. Again, human swimmers often resort to artifice, in this case a sprung nose-clip like a clothes peg. Anybody watching an ant-eater feeding through a hole in a nest of ants or termites can quickly see why they have been furnished with a long thin snout and sticky tongue. This is true not just of the specialized ant-eaters of South America, but of the unrelated pangolins and aardvark of Africa, and the even less closely related numbat and very distantly related spiny ant-eaters of Australasia. It is less obvious why all mammals that eat ants or termites have a low metabolic rate - a low body
temperature compared with most mammals, and a correspondingly low rate of biochemical turnover.
Our zoologists of the future, in order to reconstruct ancestral worlds and genetic descriptions of them, will need to replace intuitive common sense with systematic research. Here's how they might proceed. Begin by
listing a set of animals which are not particularly closely related to each other but which all share an important aspect of their life. Water- dwelling mammals would be a good test case. On more than a dozen separate occasions, land-dwelling mammals have returned to make their living, either wholly or partly, in water. We know they did so independently of each other because their closer cousins still live on land. The Pyrenean desman is a kind of aquatic mole, closely related to our familiar burrowing moles. Desmans and moles are members of the order Insectivora. Other members of the Insectivora who have independently evolved to live in fresh water include water shrews, one aquatic species of the exclusively Madagascan group of tenrecs, and three species of related otter shrews. That's four separate returnings to water among the Insectivora alone. All four are closer cousins to relatives living on dry
land than they are to the other freshwater species in the list. We have to count the three otter shrews as only a single returning to water because they are related to each other and presumably are all descended from a recent aquatic ancestor.
The surviving whales probably represent at most two separate returnings to water: the toothed whales (including dolphins) and the baleen whales. The surviving dugongs and manatees are close cousins of each other, and certainly their common ancestor also lived in the sea: they too, then, represent only a single returning to the sea. Within the pig family, most live on land but hippopotamuses have partly returned to live in water. Beavers and true otters are other animals whose ancestors returned to the water. They can be directly compared with cousins who have stayed on land, say prairie dogs in the case of beavers, and badgers in the case of otters. Mink are members of the same genus as weasels and stoats (that puts them as close to each other as horses, zebras and donkeys are to each other) but they are semi-aquatic and have partially webbed feet. There is a South American water marsupial, the yapok, which can be directly compared with its land-dwelling cousins among the opossums. Among the egg-laying mammals of Australasia, the duck-billed platypuses live largely in water, the spiny ant-eaters on land. We can make a respectable list of matched pairs: each independently evolved aquatic group opposite the closest cousin we can find that has stayed on the land.
Given the list of matched pairs, we can immediately notice some obvious things. Most of the water-dwellers have at least partially webbed feet;
some have a tail that is modified into the shape of a paddle. These are obvious in the same kind of way as the long sticky tongue shared by ant- eaters. But, like the low metabolic rate shared by ant-eaters, there are probably less obvious characteristics shared by aquatic mammals as distinct from their terrestrial cousins. How shall we discover them? By a systematic statistical analysis; perhaps something like this.
Looking down our table of matched pairs, we make a large set of measurements, the same measurements for all the animals. We measure anything we can think of, with no prior expectations: pelvis width, eye radius, gut length, dozens more, all perhaps scaled as a ratio of total body size. Now throw all the measurements into the computer and invite it to work out which measurements need to be given high weighting in order to discriminate aquatic animals from their terrestrial cousins. We could calculate a number, the 'discrimination number', by summing up contributions from all the measurements, each one having been multiplied by a weighting factor. The computer adjusts the weighting given to each measurement, in order to maximize the difference, in the final sum, between aquatic mammals and their terrestrial opposite numbers. The foot webbing index will presumably emerge from the analysis with a strong weighting. The computer will discover that it pays - if you are trying to maximize the difference between aquatic and terrestrial animals - to multiply the webbing index by a high number before adding it to the discrimination number. Other measurements - things that mammals share without regard to the wetness of their world - will need to be multiplied by zero in order to eliminate their irrelevant and confusing contribution to the weighted sum.
At the end of the analysis we look down the weightings of all our measurements. Those that emerge with high weightings, like the foot webbing index, are the ones that have something to do with the wateriness of the way of life. Webbiness is obvious. What we hope is that the analysis will uncover other important discriminators that are not so obvious. Biochemical measures, for instance. When we have found them, we can then scratch our heads and wonder what connection they have with living in water or on land. This may suggest hypotheses for further research. Even if it doesn't, any measurement that gives us a statistically significant difference between animals that have adopted some way of life and their cousins that have not is very likely to be telling us something important about that way of life.
We can do the same thing with genes. Without any prior hypotheses about what the genes are doing, we make a systematic search for genetic resemblances between unrelated aquatic animals, which are not shared by their terrestrial close cousins. If we find any strong and statistically significant effects, even if we don't understand what those genes are
doing, I would say that what we are looking at might be regarded as a genetic description of watery worlds. Natural selection, to repeat, works as an averaging computer, doing the equivalent of a calculation that is not unlike the calculations we have just programmed our manmade computer to perform. Often a species embraces various ways of life, which may be radically different from each other. A caterpillar, and the butterfly it becomes, are members of the same species, yet our zoologist's reconstruction of their two ways of life would be utterly different. Caterpillar and butterfly contain exactly the same set of genes, and the genes must describe both environments, but separately. Presumably many of them are turned on in the plant-chewing, growing, caterpillar phase, and a largely different set of genes are turned on in the adult, reproductive, nectar-eating phase.
Male and female of most species live in at least somewhat different ways. The differences are pushed to extremes in angler fish, where the male appends himself as a tiny parasitic protuberance on the female's massive body. In most species, including ourselves, both male and female contain most of the genes for being either male or female. The differences lie in which genes are turned on. We all have genes for making penises and genes for making uteruses, regardless of our sex. ('Sex' is correct, by the way, not 'gender'. Gender is a grammatical technical term, applied to words not creatures. In German, a girl's gender is neuter but her sex female. Amerindian languages typically have two genders, animate and inanimate. The association of gender with sex in some groups of languages is incidental. It is quite a good joke that the politically inspired euphemism - saying gender when you mean sex - is consequently a piece of Western Imperialism. ) Our future zoologist reading the body of either a male or a female would get an incomplete picture of the ancestral worlds of the species. On the other hand, the genes of any member of the species would more nearly suffice to reconstruct a complete picture of the range of ways of life that the species has experienced.
Parasitic cuckoos are an oddity, and a fascinating one from the point of view of the Genetic Book of the Dead. As is well known, they are reared by foster parents of a species not their own. They never rear their own young. Not all are reared by the same foster species. In Britain, some are reared by meadow pipits, some by reed warblers, fewer by robins, some by a variety of other species, but the largest number are reared by dunnocks (hedge sparrows). As it happens, our foremost specialist on dunnocks and the author of Dunnock Behaviour and Social Evolution (1992) is also today's leading investigator of cuckoo biology, Nicholas Davies of Cambridge University. I shall base my account on the work of Davies and his colleague Michael Brooke because it lends itself especially well to being cast in the language of species 'experience' of ancestral
worlds. Unless otherwise stated I shall refer to the common cuckoo, Cuculus canorzis, in Britain.
Although they make mistakes on 10 per cent of occasions, a female cuckoo normally lays in the same kind of nest as her mother, her maternal grandmother, her maternal maternal great grandmother, and
so on. Presumably young females learn the characteristics of their foster nest and seek it out when their own time comes to lay. So, as far as females are concerned, there are dunnock cuckoos, reed warbler cuckoos, meadow pipit cuckoos, and so on, and they share this attribute with
their female-line relatives. But these are not separate species, not even separate races in the normal sense of the word. They are called 'gentes' (singular 'gens'). The reason a gens is not a true race or species is that male cuckoos don't belong to a gens. Since males don't lay eggs, they never have to choose a foster nest. And when a male cuckoo comes to mate, he just mates with a female cuckoo irrespective of her gens, and regardless of the foster species that reared either of them. It would follow from this that there is gene flow between the gentes. Males carry genes from one female gens to another. A female's mother, maternal grandmother and maternal maternal great grandmother will all belong to the same gens. But her paternal grandmother, both her paternal great grandmothers, and all her female ancestors to whom she is linked via
any male ancestor, could belong to any gens. From the point of view of gene 'experience', the consequence is very interesting. Recall that, in birds, it is the female sex that has the unequal sex chromosomes, X and Y, while male birds have two X chromosomes. Think what this means for the ancestral experience of genes on a Y chromosome. Since it passes unswervingly down the female line, never straying into the paths of male experience, a Y chromosome stays strictly within one gens. It is a dunnock cuckoo Y chromosome or a meadow pipit cuckoo Y chromosome. Its foster parent 'experience' is the same from generation to generation.
In this respect it differs from all other genes in the cuckoo, for they have all done time in male bodies and have hence shuffled freely around the female gentes, experiencing them all in proportion to their frequency.
In our language of genes as 'descriptions' of ancestral environments, most cuckoo genes will be in a position to describe those features that are shared by the complete range of foster nests that the species has parasitized. Y chromosome genes, uniquely, will describe only one type of foster nest, one species of foster parent. This means that Y chromosome genes, in a way that is not possible for other cuckoo genes, will be in a position to evolve specialized tricks for surviving in their own particular foster species' nest. What sort of tricks? Well, cuckoo eggs show at least some tendency to mimic the eggs of their foster species. Cuckoo eggs laid in meadow pipit nests are like large meadow pipit eggs. Cuckoo eggs laid in reed warbler nests are like large reed warbler eggs. Cuckoo eggs laid in
pied wagtail nests resemble pied wagtail eggs. Presumably this benefits the cuckoo eggs, which might otherwise be rejected by the foster parents. But think what it must mean from the genes' point of view.
If the genes for egg colour were on any chromosomes but the Y chromosome, they would be carried via males into the bodies of females belonging to the full assortment of gentes. This means they would be carried into the full range of host nests and there would be no consistent natural selection pressure to mimic one egg type more than another. It would be difficult for their eggs, in these circumstances, to mimic any but the most generalized features of all host eggs. Although there is no direct evidence, it is therefore reasonable to guess that the specific egg mimicry genes sit on the cuckoo Y chromosome. Females will then carry them, generation after generation, into nests of the same host. Their ancestral 'experience' will all be with the discriminating eyes of the same host, and those eyes will exert the selection pressure that steers their colour and spot pattern towards mimicry of host eggs.
There is a conspicuous exception. Cuckoo eggs laid in dunnock nests do not resemble dunnock eggs. They are no more variable among
themselves than eggs laid in reed warbler or meadow pipit nests; their colour is distinctive of the dunnock gens of cuckoos, and they don't
much resemble the eggs of any other gens, but they don't resemble dunnock eggs either. Why is this? It might be-thought that dunnock eggs, being a uniform pale blue, are harder to mimic than meadow pipit or
reed warbler eggs. Perhaps cuckoos just lack the physiological equipment to make plain blue eggs? I'm always suspicious of such last-resort theories, and in this case there is evidence against it. In Finland there is a gens of cuckoo that parasitizes redstarts, which also have plain blue eggs. These cuckoos, which belong to the same species as our British ones, succeed beautifully in matching redstart eggs. This surely shows that the failure of British cuckoos to mimic dunnock eggs cannot be put down to inherent incapacity to produce the unspeckled blue colour. Davies and Brooke believe that the true explanation lies in the recency of the relationship between dunnocks and cuckoos. Cuckoos run arms races in evolutionary time with each host species and the gens we are looking at has only recently 'invaded' dunnocks. Consequently,
dunnocks haven't yet had time to evolve counter-weapons. And dunnock cuckoos either haven't had time to evolve eggs that mimic dunnocks, or they don't yet need to because dunnocks haven't evolved the habit of discriminating foreign eggs from their own. In the language of this chapter, neither the dunnock gene pool nor the cuckoo gene pool (or rather, the Y chromosome of the dunnock cuckoo gens) has had enough experience of the other to evolve counter-weapons. Perhaps dunnock cuckoos are still adapted to outwit a different foster species, the one that their female ancestor left when she laid the first egg in a dunnock nest.
Meadow pipits, reed warblers and pied wagtails, on this view, are enemies of their respective gentes of cuckoos. There has been plenty of time for a build-up of weaponry on both sides. The hosts have built up keen eyes for an impostor egg and the cuckoos possess correspondingly cunning disguises for their eggs. Robins are an intermediate case. Their cuckoos lay eggs which are slightly robin-like, but not very. Perhaps the arms race between robins and the robin gens of cuckoos is of intermediate antiquity. On this view, the Y chromosomes of robin cuckoos are somewhat experienced, but their description of recent (robin) ancestral environments is still sketchy and contaminated by earlier descriptions of other species, previously 'experienced'.
Davies and Brooke did experiments deliberately putting extra eggs, of various kinds, in nests belonging to different species of birds. They wanted to see which species would accept, or reject, strange eggs. Their hypothesis was that species that have been through an arms race with cuckoos would, as a consequence of their genetic 'experience', be most likely to reject foreign eggs. One way to test this was to look at species which are not even suitable as cuckoo hosts. Baby cuckoos need to eat insects or worms. Species that feed their young on seeds, or species that nest in holes that female cuckoos can't reach, have never been at risk. Davies and Brooke predicted that such birds would not worry if they experimentally introduced strange eggs into their nests. And so it proved. Species that are suitable for cuckoos, however, like chaffinches, song thrushes and blackbirds, showed a stronger tendency to reject the experimental eggs that Davies and Brooke, playing cuckoo, placed in their nests. Flycatchers are potentially vulnerable in that they feed their young on a cuckoo-friendly diet. But whereas spotted flycatchers have open and accessible nests, pied flycatchers nest in holes which female cuckoos are too large to penetrate. Sure enough, when the experimenters dumped foreign eggs in their nests, pied flycatchers, with their 'inexperienced' gene pools, accepted foreign eggs without protest; spotted flycatchers, by contrast, rejected them, suggesting that their gene pools were wise to the cuckoo menace from long ago.
Davies and Brooke did similar experiments with species that cuckoos actually do parasitize. Meadow pipits, reed warblers and pied wagtails usually rejected artificially added eggs. As befits the 'lack of ancestral experience' hypothesis, dunnocks did not; nor did wrens. Robins and sedge warblers were intermediate. At the other extreme, reed buntings, which are suitable for cuckoos but not much parasitized by them, showed total rejection of foreign eggs. No wonder cuckoos don't parasitize them. Davies and Brooke's interpretation would presumably be that reed buntings have come out the other side of a long ancestral arms race with cuckoos, which they eventually won. Dunnocks are near the beginning of
their arms race. Robins are slightly more advanced in theirs. Meadow pipits, reed warblers and pied wagtails are in the middle of theirs. When we say dunnocks have only just begun their arms race with cuckoos, 'only just' has to be interpreted with evolutionary timescales in mind. By human standards the association could still be quite old. The Oxford English Dictionary quotes a 1616 reference to the Heisugge (archaic word for hedge sparrow or dunnock) as 'a bird which hatcheth the Cuckooes egges'. Davies notes the following lines in King Lear I, iv, written a decade earlier:
For, you trow, nuncle,
The hedge-sparrow fed the cuckoo so long,
That its had it head bit off by it young.
And in the fourteenth century Chaucer wrote of the cuckoo's treatment of the dunnock in The Parliament of Fowls:
'Thou mortherere of the hey sage on the braunche That broughte the forth, thow rewthelees glotoun! '
Although dunnock, hedge sparrow and heysoge are all given as synonyms in the dictionary, I can't help wondering how far we should rely on medieval ornithology. Chaucer himself was usually a rather precise user of language, but nevertheless the name sparrow has at times been given to what today is technically called an LBB (little brown bird). This may have been Shakespeare's meaning in the following, from Henry IV Part I, V, i:
And, being fed by us, you used us so
As that ungentle gull the cuckoo's bird,
Useth the sparrow - did oppress our nest
Grew by our feeding to so great a bulk
That even our love durst not come near your sight For fear of swallowing;
Sparrow, on its own, would nowadays mean the house sparrow, Passer domesticus, which is never parasitized by cuckoos. Despite its alternative name hedge sparrow, the dunnock, Prunella modularis, is unrelated; it is a 'sparrow' only in the loose sense of being a little brown bird. But
anyway, even if we take Chaucer's evidence as showing that the arms race between cuckoos and dunnocks really does go back at least to the fourteenth century, Davies and Brooke cite theoretical calculations, taking into account the comparative rarity of cuckoos, suggesting that this is still sufficiently recent in evolutionary terms to account for the apparent naivety of dunnocks when faced with cuckoos.
Before we leave cuckoos, here's an interesting thought. There could be, simultaneously existing, more than one gens of, say, robin cuckoos, who have built up their egg mimicry. ' independently.
Since there is no gene flow between them as far as Y chromosomes are concerned, there could be accurate egg mimics coexisting with less accurate egg mimics. All are capable of mating with the same males but they don't share the same Y chromosomes. The accurate mimics would be descended from a female who moved into parasitizing robins a long time ago. The less accurate ones would be descended from a different female who moved into robins, possibly from a different predecessor host species, more recently.
Ants, termites and other social insect species are odd in a different way. They have sterile workers, often divided into several 'castes' - soldiers, media (middle-sized) workers, minor (small) workers, and so on. Every worker, whatever its caste, contains the genes that could have turned it into any other caste. Different sets of genes are switched on under different rearing conditions. It is by regulating these rearing conditions that the colony engineers a useful balance of different castes. Often the differences among castes are dramatic.
In the Asian ant species Pheidologeton diversus, the large worker caste (specialized for bulldozing smooth paths for other colony members) is 500 times heavier than the small caste, who do all the normal duties of a worker ant. The same set of genes equips a larva to grow up into either a Brobdingnagian or a Lilliputian, depending upon which ones are switched on. Honeypot ants are immobile storage vats, abdomens pumped up with nectar to transparent yellow spheres, hanging from the ceiling of the nest. The normal duties of an ants' nest, defence, foraging and, in this case, filling up the living vats, are done by normal workers whose abdomens are not swollen. The normal workers have genes that equip them to be honeypots, and honeypots, as far as their genes are concerned, could equally well be normal workers. As in the case of male and female, the visible differences in bodily form depend upon which genes are switched on. In this case it is determined by environmental factors, perhaps diet. Once again, the zoologist of the future could read out from the genes, but not the body, of any one member of the species a complete picture of the disparate lives of the different castes.
The European snail Cepaea nemoralis comes in a number of colours and patterns. The background shell colour can be any of six distinct shades (in order of dominance, in the technical genetic sense): brown, dark pink, light pink, very pale pink, dark yellow, light yellow. Overlaying this, there may be any number of stripes from zero to five. Unlike the case of the social insects, it is not true that every individual snail is genetically equipped to assume any of the different forms. Nor are these differences among snails determined by different environments of upbringing. Striped snails have genes that determine their number of stripes, dark pink individuals have genes that make them dark pink. But all the kinds can mate with each other.
The reasons for the persistence of many different types of snail (polymorphism), as well as the detailed genetics of the polymorphism itself, have been exhaustively studied by the English zoologists A. J. Cain and the late P. M. Sheppard with their school. A major part of the evolutionary explanation is that the species ranges over different habitats - woodland, grassland, bare soil - and you need a different colour pattern to be camouflaged against birds in each place. Beechwood snails contain an admixture of genes from grassland because they interbreed at the margins. A chalk downland snail has some genes that previously survived in the bodies of woodland ancestors; and their legacy, depending on the other genes in the snail, may be stripes. Our zoologist of the future would need to look at the gene pool of the species as a whole to reconstruct the full range of its ancestral worlds.
Just as Cepaea snails range over different habitats in space, so the ancestors of any species have changed their way of life from time to time. House mice, Mus musculus, today live almost exclusively in or around human habitations, as unwanted beneficiaries of human agriculture. But by evolutionary standards their way of life is recent. They must have fed on something else before there was human agriculture. Doubtless that something was sufficiently similar for their genetic skills to be pressed into service when the agricultural bonanza came along. Mice and rats have been described as animal weeds (incidentally, a good piece of poetic imagery, genuinely illuminating). They are generalists, opportunists, carrying genes that helped their ancestors to survive through probably a considerable range of ways of life; and pre-agricultural genes are in them yet. Anybody attempting to 'read' their genes may find a confusing palimpsest of ancestral world descriptions.
From earlier still, the DNA of all mammals must describe aspects of very ancient environments as well as more recent ones. The DNA of a camel was once in the sea, but it hasn't been there for a good 300 million years. It has spent most of recent geological history in deserts, programming bodies to withstand dust and conserve water. Like sandbluffs carved into
fantastic shapes by the desert winds, like rocks shaped by ocean waves, camel DNA has been sculpted by survival in ancient deserts, and even more ancient seas, to yield modern camels. Camel DNA speaks - if only we could understand the language - of the changing worlds of camel ancestors. If only we could read the language, the DNA of tuna and starfish would have 'sea' written into the text. The DNA of moles and earthworms would spell 'underground'. Of course all the DNA would spell many other things as well. Shark and cheetah DNA would spell 'hunt', as well as separate messages about sea and land. Monkey and cheetah DNA would spell 'milk'. Monkey and sloth DNA would spell 'trees'. Whale and dugong DNA presumably describes very ancient seas, fairly ancient lands and more recent seas: complicated palimpsests again.
Features of the environment that occur frequently or importantly are heavily emphasized or 'weighted' in the genetic description, compared with rare or trivial features. Environments that lie in the remote past have a different weighting from recent ones, presumably lower, though not in any obvious way. Environments that lasted a long time in the species' history will have a more prominent weighting in the genetic description than environmental events that, however drastic they may have seemed at the time, were geological flashes in the pan.
It has been poetically suggested that the remote marine apprenticeship of all land life is reflected in the biochemistry of the blood, which is said to resemble a primeval salt sea. Or the liquid in a reptile's egg has been described as a private pond, relic of the actual ponds in which the larvae of distant, amphibious ancestors would have grown. To the extent that animals and their genes bear such a stamp of ancient history it will be for good functional reasons. It won't be history for history's sake. Here is the kind of thing I mean by this. When our remote ancestors lived in the sea, many of our biochemical and metabolic processes became geared to the chemistry of the sea - and our genes became a description of marine chemistry - for functional reasons. But (this is an aspect of our 'selfish Cooperator' argument) biochemical processes become geared not only to the external world but to each other. The world to which they became fitted included the other molecules in the body and the chemical processes in which they partook. There after, when remote descendants of these marine animals moved out on to the land and became gradually more and more fitted to a dry airy world, the old mutual adaptation of biochemical processes to each other - and incidentally to the chemical 'memory' of the sea - persisted. Why should it not, when the different kinds of molecules in the cells and blood so greatly outnumber the different kinds of molecules encountered in the outside world? It is only in a very indirect sense that the genes spell out descriptions of ancestral environments. What they directly describe, after being translated into the parallel language of protein molecules, is instructions for individual
embryonic development. It is the gene pool of the species as a whole that becomes carved to fit the environments that its ancestors have encountered - which is why I said that the species is a statistical averaging device. It is in this indirect sense that our DNA is a coded description of the worlds in which our ancestors survived. And isn't it an arresting thought? We are digital archives of the African Pliocene, even of Devonian seas; walking repositories of wisdom out of the old days. You could spend a lifetime reading in this ancient library and die unsated by the wonder of it.
11
REWEAVING THE WORLD
Since my education began I have always had things described to me with their colors and sounds, by one with keen senses and a fine feeling for the significant.
Therefore, I habitually think of things as colored and resonant Habit accounts for part
The soul sense accounts for another part.
The brain with its five-sensed construction asserts its right and accounts for the rest
Inclusive of all, the unity of the world demands that color be kept in it whether I have cognizance of it or not.
Rather than be shut out, I take part in it by discussing it, happy in the happiness of those near to me who gaze at the lovely hues of the sunset or the rainbow.
HELEN KELLER, The Story of My Life (1902)
Where the gene pool or a species is sculpted into a set of models of ancestral worlds, the brain of an individual houses a parallel set of models of the animal's own world.
Both are equivalent to descriptions of the past, and both are used to aid survival into the future. The difference is one of timescale and of relative privacy. The genetic description is a collective memory belonging to the species as a whole, going back into the indefinite past. The memory of the brain is private and contains the individual's experiences since it was born.
Our subjective knowledge of a familiar place does indeed feel to us like a model of the place. Not an accurate scale model, certainly less accurate
than we think it is, but a serviceable model for the purposes required. One way to approach this idea was proposed some years ago by the Cambridge physiologist Horace Barlow, incidentally a direct descendant of Charles Darwin. Barlow is especially interested in vision and his argument starts from the realization that to recognize an object is a much more difficult problem than we, who seem to see so effortlessly, ordinarily understand.
For we are blissfully unaware of what a formidably clever thing we do every second of our waking lives when we see and recognize objects. The sense organs' task of unweaving the physical stimuli that bombard them is easy compared with the brain's task of reweaving an internal model of the world that it can then make use of. The argument holds for all our sensory systems, but I'll stick mostly to vision because that is the one that means the most to us. Think what a problem our brain solves when it recognizes something, say a letter A. Or think of the problem of recognizing a particular person's face. By long in-group convention, the hypothetical face we are talking about is assumed to belong to the grandmother of the distinguished neurobiologist J. Lettvin, but substitute any face you know, or indeed any object you can recognize. We are not concerned here with subjective consciousness, with the philosophically hard problem of what it means to be aware of your grandmother's face. Just a cell in the brain which fires if and only if the grandmother's face appears on the retina will do nicely for a start, and it is very difficult to arrange. It would be easy if we could assume that the face would always fall exactly on a particular part of the retina. There could be a keyhole arrangement, with a grandmother-shaped region of cells on the retina wired up to a grandmother-signalling cell in the brain. Other cells - members of the 'anti-keyhole' - would have to be wired up in inhibitory-fashion, otherwise the central nervous cell would respond to a white sheet just as strongly as to the grandmother's face which - together with all other conceivable images - it would necessarily 'contain'. The essence of responding to a key image is to avoid responding to everything else.
The keyhole strategy is ruled out by sheer force of numbers.
Even if Lettvin needed to recognize nothing but his grandmother, how could he cope when her image falls on a different part of the retina? How cope with her image's changing size and shape as she approaches or recedes, as she turns sideways, or cants to the rear, as she smiles or as she frowns? If we add up all possible combinations of keyholes and anti- keyholes, the number enters the astronomical range. When you realize that Lettvin can recognize not only his grandmother's face but hundreds of other faces, the other bits of his grandmother and of other people, all the letters of the alphabet, all the thousands of objects to which a normal person can instantly give a name, in all possible orientations and
apparent sizes, the explosion of triggering cells gets rapidly out of hand. The American psychologist Fred Attneave, who had come up with the same general idea as Barlow, dramatized the point by the following calculation: if there were just one brain cell to cope, keyhole fashion, with each image that we can distinguish in all its presentations, the volume of the brain would have to be measured in cubic light years.
How then, with a brain capacity measured only in hundreds of cubic centimetres, do we do it? The answer was proposed in the 1950s by Barlow and Attneave independently. They suggested that nervous systems exploit the massive redundancy in all sensory information. Redundancy is jargon from the world of information theory, originally developed by engineers concerned with the economics of telephone line capacity. Information, in the technical sense, is surprise value, measured as the inverse of expected probability. Redundancy is the opposite of information, a measure of unsurprisingness, of old-hatitude. Redundant messages or parts of messages are not informative because the receiver, in some sense, already knows what is coming. Newspapers do not carry headlines saying, 'The sun rose this morning'. That would convey almost zero information. But if a morning came when the sun did not rise, headline writers would, if any survived, make much of it. The information content would be high, measured as the surprise value of the message. Much of spoken and written language is redundant - hence possible condense telegraphese: redundancy lost, information preserved.
Everything that we know about the world outside our skulls comes to us via nerve cells whose impulses chatter like machine guns. What passes along a nerve cell is a volleying of 'spikes', impulses whose voltage is
fixed (or at least irrelevant) but whose rate of arriving varies meaningfully. Now let's think about coding principles. How would you translate information from the outside world, say, the sound of an oboe or the temperature of a bath, into a pulse code? A first thought is a simple rate code: the hotter the bath, the faster the machine gun should fire. The brain, in other words, would have a thermometer calibrated in pulse rates. Actually, this is not a good code because it is uneconomical with pulses. By exploiting redundancy, it is possible to devise codes that convey the same information at a cost of fewer pulses. Temperatures in the world mostly stay the same for long periods at a time. To signal 'It is hot, it is hot, it is still hot. . . ' by a continuously high rate of machine-gun pulses is wasteful; it is better to say, 'It has suddenly become hot' (now you can assume that it will stay the same until further notice).
And, satisfyingly, this is what nerve cells mostly do, not just for signalling temperature but for signalling almost everything about the world. Most nerve cells are biased to signal changes in the world. If a trumpet plays a long sustained note, a typical nerve cell telling the brain
about it would show the following pattern of impulses: Before the trumpet starts, low firing rate; immediately after the trumpet starts, high firing rate; as the trumpet carries on sustaining its note, the firing rate dies away to an infrequent mutter; at the moment when the trumpet stops, high firing rate, dying away to a resting mutter again. Or there might be one class of nerve cells that fire only at the onset of sounds and a different class of cells that fire only when sounds go off. Similar exploitation of redundancy - screening out of the sameness in the world - goes on in cells that tell the brain about changes in light, changes in temperature, changes in pressure. Everything about the world is signalled as change, and this is a major economy.
But you and I don't seem to hear the trumpet die away. To us the trumpet seems to carry on at the same volume and then to stop abruptly. Yes, of course. That's what you'd expect because the coding system is ingenious. It doesn't throw away information, it only throws away redundancy. The brain is told only about changes, and it is then in a position to reconstruct the rest. Barlow doesn't put it like this, but we could say that the brain constructs a virtual sound, using the messages supplied by the nerves coming from the ears. The reconstructed virtual sound is complete and unabridged, even though the messages
themselves are economically stripped down to information about changes. The system works because the state of the world at a given time is
usually not greatly different from the preceding second. Only if the world changed capriciously, randomly and frequently, would it be economical for sense organs to signal continuously the state of the world. As it is, sense organs are set up to signal, economically, the discontinuities in the worlds and the brain, assuming correctly that the world doesn't change capriciously and at random, uses the information to construct an
internal virtual reality in which the continuity is restored.
The world presents an equivalent kind of redundancy in space, and the nervous system uses the corresponding trick. Sense organs tell the brain about edges and the brain fills in the boring bits between. Suppose you are looking at a black rectangle on a white background. The whole scene is projected on to your retina - you can think of the retina as a screen covered with a dense carpet of tiny photocells, the rods and cones. In theory, each photocell could report to the brain the exact state of the light falling upon it. But the scene we are looking at is massively redundant. Cells registering black are overwhelmingly likely to be surrounded by other cells registering black. Cells registering white are nearly all surrounded by other white-signalling cells. The important exceptions are cells on edges. Those on the white side of an edge signal white themselves and so do their neighbours that sit further into the white area. But their neighbours on the other side are in the black area. The brain can theoretically reconstruct the whole scene if just the retinal
cells on edges fire. If this could be achieved there would be massive savings in nerve impulses. Once again, redundancy is removed and only information gets through.
Elegantly, the economy is achieved in practice by the mechanism known as lateral inhibition'. Here's a simplified version of the principle, using our analogy of the screen of photocells. Each photocell sends one long wire to the central computer (brain) and also short wires to its immediate neighbours in the photocell screen. The short connections to the neighbours inhibit them, that is, turn down their firing rate. It is easy to see that maximal firing will come only from cells that lie along edges, for they are inhibited from one side only. Lateral inhibition of this kind is common among the low-level units of both vertebrate and invertebrate eyes.
Once again, we could say that the brain constructs a virtual world which is more complete than the picture relayed to it by the senses. The information which the senses supply to the brain is mostly information about edges. But the model in the brain is able to reconstruct the bits between the edges. As in the case of discontinuities in time, an economy is achieved by the elimination - and later reconstruction in the brain - of redundancy. This economy is possible only because uniform patches exist in the world. If the shades and colours in the world were randomly dotted about, no economical remodeling would be possible.
Another kind of redundancy stems from the fact that many lines in the real world are straight, or curved in smooth and therefore predictable (or mathematically reconstructable), ways. If the ends of a line are specified, the middle can be filled in using a simple rule that the brain already 'knows'. Among the nerve cells that have been discovered in the brains of mammals are the so-called 'line-detectors', neurones that fire whenever a straight line, aligned in a particular direction, falls on a particular place in the retina, the so-called 'retinal field' of the brain cell. Each of these line-detector cells has its own preferred direction. In the cat brain, there are only two preferred directions, horizontal and vertical, with an approximately equal number favouring each direction; however, in monkeys other angles are accommodated. From the point of view of the redundancy argument, what is going on here is as follows. In the retina, all the cells along a straight line fire and most of these impulses are redundant. The nervous system economizes by using a single cell to register the line, labelled with its angle. Straight lines are economically specified by their position and direction alone, or by their ends, not by the light value of every point along their length. The brain reweaves a virtual line in which the points along the line are reconstructed.
However, if a part of a scene suddenly detaches itself from the rest and starts to crawl over the background, it is news and should be signalled. Biologists have indeed discovered nerve cells that are silent until something moves against a still background. These cells don't respond when the entire scene moves - that would correspond to the sort of apparent movement the animal would see when it itself moves. But movement of a small object against a still background is information-rich and there are nerve cells tuned to detect it. The most famous of these are the so-called 'bug-detectors' discovered in frogs by Lettvin (he of the grandmother) and his colleagues. A bug-detector is a cell which is apparently blind to everything except the movement of small objects against their background. As soon as an insect moves in the field covered by a bug-detector, the cell immediately initiates massive signalling and the frog's tongue is likely to shoot out to catch the insect. To a sufficiently sophisticated nervous system, though, even the movement of a bug is redundant if it is movement in a straight line. Once you've been told that a bug is moving steadily in a northerly direction, you can assume that it will continue to move in this direction until further notice. Carrying the logic a step further, we should expect to find higher-order movement detector cells in the brain that are especially sensitive to change in movement, say, change in direction or change in speed. Lettvin and his colleagues found a cell that seems to do this, again in the frog. In their paper in Sensory Communication (1961) they describe a particular experiment as follows:
Let us begin with an empty gray hemisphere for the visual field-There is usually no response of the cell to turning on and off the illumination. It is silent. We bring in a small dark object say 1 to 2 degrees in diameter, and at a certain point in its travel, almost anywhere in the field, the cell suddenly 'notices' it. Thereafter, wherever that object is moved it is tracked by the cell. Every time it moves, with even the faintest jerk, there is a burst of impulses that dies down to a mutter that continues as long as the object is visible. If the object is kept moving, the bursts signal discontinuities in the movement, such as the turning of corners, reversals, and so forth, and these bursts occur against a continuous background mutter that tells us the object is visible to the cell.
