The Ancestor's Tale Part 13

Rendezvous 24.

SEA SQUIRTS.

The sea squirts seem, at first, unlikely recruits to our human-centred pilgrimage. Previous arrivals have not been too dramatically different from those already on the march. Even the lancelet can plausibly be regarded as a stripped-down fish: lacking major features, to be sure, but you can easily sketch a pathway along which something like a lancelet could evolve into a fish. A sea squirt is something else. It doesn't swim like a fish. It doesn't swim like anything. It doesn't swim. It is far from clear why it deserves the ill.u.s.trious name of chordate at all. A typical sea squirt is a bag filled with sea water, plus a gut and reproductive organs, anch.o.r.ed to a rock. The bag is topped by two siphons one for drawing water in, the other for exhaling it. Day and night, water streams in through one siphon and out again through the other. On the way, it pa.s.ses through the pharyngeal basket, a filtering net that strains out particles of food. Some sea squirts are packed together in colonies, but each member does essentially the same thing. No sea squirt is even faintly reminiscent of a fish, or of any vertebrate, or of the lancelet (see plate 31) (see plate 31).

No adult sea squirt, that is. However unchordate-like an adult sea squirt might be, it has a larva that looks like ... a tadpole. Or like the larva of a lamprey, the ammocoete of Garstang's rhyme on page 374. Like many larvae of sedentary, bottom-dwelling, filter-feeding animals, the tadpole larva of the sea squirt swims in the plankton. It propels itself like a fish by a post-a.n.a.l tail that undulates from side to side. It has a notochord and a dorsal nerve tube. The larva, though not the adult sea squirt, has the appearance of at least a rudimentary chordate. When it is ready to metamorphose into an adult, the larva fastens itself onto a rock (or whatever is to be its adult resting place) head first, loses its tail, its notochord and most of its nervous system, and settles down for life.

It is even called a 'tadpole larva', and the significance of this was known to Darwin. He gave the sea squirts the following unpromising introduction, under their scientific name of ascidians: [image]

Sea squirts join. Animals with a stiff cartilaginous 'notochord' are cla.s.sified together as chordates (in humans, remnants of this rod linger as the discs between our vertebrae). It has long been accepted that, among the chordates, the sea squirts and their allies (of which there are about 2,000 described species) are the most distantly related to all the others. This has also been substantiated by recent molecular data. Animals with a stiff cartilaginous 'notochord' are cla.s.sified together as chordates (in humans, remnants of this rod linger as the discs between our vertebrae). It has long been accepted that, among the chordates, the sea squirts and their allies (of which there are about 2,000 described species) are the most distantly related to all the others. This has also been substantiated by recent molecular data.

Image: blue sea squirt ( blue sea squirt (Rhopalaea cra.s.sa).

They hardly appear like animals, and consist of a simple, tough, leathery sack, with two small projecting orifices. They belong to the Molluscoidea of Huxley a lower division of the great kingdom of the Mollusca; but they have recently been placed by some naturalists amongst the Vermes or worms. Their larvae somewhat resemble tadpoles in shape, and have the power of swimming freely about.

I should say that neither Molluscoidea nor Vermes are any longer recognised, and sea squirts are no longer placed close to molluscs or worms. Darwin goes on to mention his own satisfaction in discovering such a larva in the Falkland Islands in 1833, and he continues as follows: M. Kovalevsky has lately observed that the larvae of Ascidians are related to the Vertebrata, in their manner of development, in the relative position of the nervous system, and in possessing a structure closely like the chorda dorsalis chorda dorsalis of vertebrate animals ... We should then be justified in believing that at an extremely remote period a group of animals existed, resembling in many respects the larvae of our present Ascidians, which diverged into two great branches the one retrograding in development and producing the present cla.s.s of Ascidians, the other rising to the crown and summit of the animal kingdom by giving birth to the Vertebrata. of vertebrate animals ... We should then be justified in believing that at an extremely remote period a group of animals existed, resembling in many respects the larvae of our present Ascidians, which diverged into two great branches the one retrograding in development and producing the present cla.s.s of Ascidians, the other rising to the crown and summit of the animal kingdom by giving birth to the Vertebrata.

But now we have a division of opinion among experts. There are two theories of what happened: the one Darwin voiced, and a later one, which the Axolotl's Tale has already attributed to Walter Garstang. You remember the message of the axolotl, the message of neoteny. Sometimes the juvenile stage in a life-cycle can develop s.e.x organs and reproduce: it becomes s.e.xually mature, while remaining immature in other aspects of its being. We have previously applied the axolotl's message to Pekinese dogs, to ostriches and to ourselves: we humans appear to some scientists to be juvenile apes who have accelerated their reproductive development and chopped off the adult phase of the life cycle.

Garstang applied the same theory to sea squirts at this much older juncture in our history. The adult phase of our remote ancestor, he suggested, was a sedentary sea squirt, which evolved the tadpole larva as an adaptation to disperse, in the same way as a dandelion seed has a little parachute to carry the next generation far away from the site of its parent. We vertebrates, Garstang suggested, are descended from sea squirt larvae larvae larvae that never grew up: or rather larvae whose reproductive organs grew up but who never turned into sea squirt adults. larvae that never grew up: or rather larvae whose reproductive organs grew up but who never turned into sea squirt adults.

A second Aldous Huxley might project fictional human longevity to the point where some super-Methuselah finally settles down on his head and metamorphoses into a giant sea squirt, fastened permanently to the sofa in front of a television. The plot would gain added satirical punch from the popular myth that a sea squirt larva, when it abandons pelagic activity for sedentary adulthood, 'eats its own brain'. Somebody must once have colourfully expressed the more mundane fact that, like a caterpillar in its chrysalis, the metamorphosing sea squirt larva breaks down its larval tissues and recycles them into the adult body. This includes breaking down the head ganglion, which was useful when it was an active swimmer in the plankton. Mundane or not, a literary metaphor as promising as that was never going to pa.s.s unnoticed a meme as fecund would not go unspread. More than once I have seen a reference to the larval sea squirt which, when the time comes, settles down to a sedentary life and 'eats its brain, like an a.s.sociate professor getting tenure'.

There is a group of modern animals within the sea squirt subphylum called the Larvaceae, which are reproductively adult but resemble sea squirt larvae. Garstang pounced on them, seeing them as a more recent rerun of his ancient evolutionary script. In his view, the larvaceans had ancestors that were bottom-dwelling, sedentary sea squirts, with a planktonic larval phase. They evolved the capacity to reproduce in the larval stage, and then chopped the old adult stage off the end of their life cycle. This could all have transpired rather recently, giving us a fascinating glimpse of what perhaps happened to our ancestors half a billion years ago.

Garstang's theory is certainly an attractive one, and it was much in favour for many years, especially in Oxford under the influence of Garstang's persuasive son-in-law, Alister Hardy. Unfortunately, recent DNA evidence has swung the pendulum in favour of Darwin's original theory. If the larvaceans const.i.tute a recent re-enactment of an ancient Garstang scenario, they should find closer kins.h.i.+p with some modern sea squirts than with others. Alas, this is not so. The oldest split in the entire phylum is that between the larvaceans on the one hand, and all the rest of the phylum on the other. This doesn't conclusively prove that Garstang was wrong but, as the current holder of Alister Hardy's Chair, Peter Holland, has pointed out to me, it weakens his case and in a way that neither Garstang nor Hardy could possibly have foreseen.

The estimate I have adopted for the date of Concestor 24 is 565 million years ago, which would put it around our 275-million-greats-grandparent, but such estimates are now getting increasingly strained. It may well have looked something like a sea squirt larva. But, contra contra Garstang, it now seems probable that the adult sea squirt evolved later, as Darwin suggested. Darwin tacitly a.s.sumed that the adult of that remote species looked like a tadpole. One branch of its descendants stayed tadpole-shaped and evolved into fish. The other branch got tenure, settled down on the sea bottom and became a sedentary filter-feeder, retaining its former adult form only in the larval stage. Garstang, it now seems probable that the adult sea squirt evolved later, as Darwin suggested. Darwin tacitly a.s.sumed that the adult of that remote species looked like a tadpole. One branch of its descendants stayed tadpole-shaped and evolved into fish. The other branch got tenure, settled down on the sea bottom and became a sedentary filter-feeder, retaining its former adult form only in the larval stage.

Rendezvous 25.

AMBULACRARIANS.

Our pilgrimage is now a milling horde, having ama.s.sed all the vertebrates, together with their primitive chordate cousins, amphioxus and the sea squirts. It comes as quite a surprise that the next pilgrims to join us, our closest relatives among the invertebrates, include those strange creatures I shall soon refer to them as 'Martians' the starfish, sea urchins, brittle stars and sea cuc.u.mbers. These, together with a largely extinct group called the crinoids or sea lilies, comprise the phylum Echinodermata, the spiny-skinned ones. 'Before' the echinoderms join us, they link arms with a few miscellaneous worm-like groups which, in the absence of molecular evidence, had been placed elsewhere in the animal kingdom. The acorn worms and their kind (Enteropneusta and Pterobranchia) had previously been cla.s.sified with the sea squirts as protochordates. Molecular evidence now links them, not so very far away, with the echinoderms in a super-phylum called Ambulacraria.

Also now placed in the ambulacrarians is a curious little worm called Xenoturbella Xenoturbella. n.o.body knew where to put little Xenoturbella Xenoturbella it seems to lack most of the things that a respectable worm ought to have, like a proper excretory system and a through-flow gut. Zoologists shuffled this obscure little worm from phylum to phylum, and had pretty well given up on it when, in 1997, somebody announced that, despite all appearances, it was a highly degenerate bivalve mollusc, with affinities to c.o.c.kles. This confident statement came from molecular evidence. it seems to lack most of the things that a respectable worm ought to have, like a proper excretory system and a through-flow gut. Zoologists shuffled this obscure little worm from phylum to phylum, and had pretty well given up on it when, in 1997, somebody announced that, despite all appearances, it was a highly degenerate bivalve mollusc, with affinities to c.o.c.kles. This confident statement came from molecular evidence. Xenoturbella Xenoturbella's DNA closely resembled that of a c.o.c.kle and, as if to clinch it, Xenoturbella Xenoturbella specimens were found to contain mollusc-type eggs. Terrible warning! In what looks like the cla.s.sic nightmare of the modern forensic detective contamination of the suspect's DNA by that of the murder victim it has now turned out that the reason specimens were found to contain mollusc-type eggs. Terrible warning! In what looks like the cla.s.sic nightmare of the modern forensic detective contamination of the suspect's DNA by that of the murder victim it has now turned out that the reason Xenoturbella Xenoturbella contained mollusc DNA and mollusc eggs is that it eats molluscs! The residue of genuine contained mollusc DNA and mollusc eggs is that it eats molluscs! The residue of genuine Xenoturbella Xenoturbella that is left when the mollusc DNA is removed reveals an even more surprising affinity: that is left when the mollusc DNA is removed reveals an even more surprising affinity: Xenoturbella Xenoturbella is a member of the Ambulacraria, possibly the last member to join them 'before' we greet them at is a member of the Ambulacraria, possibly the last member to join them 'before' we greet them at Rendezvous 25 Rendezvous 25. Other molecular evidence places this rendezvous somewhere in the late Precambrian, maybe about 570 million years ago. I am guessing that Concestor 25 was approximately our 280-million-greats-grandparent. We have no idea what it looked like, but it surely was more worm-like than starfish-like. There is every indication that the echinoderms evolved their radial symmetry secondarily from left-right symmetrical ancestors 'Bilateria'.

[image]

Starfish and their kin join. We chordates belong to the major branch of animals known as the deuterostomes. Recent molecular studies suggest that all the other 8,100 or so deuterostome species group together. This new group, given the name of Ambulacraria, is quite strongly supported, although there is uncertainty in the position of the distressingly amorphous pair of species in the Xenoturbellida. We chordates belong to the major branch of animals known as the deuterostomes. Recent molecular studies suggest that all the other 8,100 or so deuterostome species group together. This new group, given the name of Ambulacraria, is quite strongly supported, although there is uncertainty in the position of the distressingly amorphous pair of species in the Xenoturbellida.

Images, left to right: sea apple ( sea apple (Pseudo-colochirus violaceus); edible sea urchin (Echinus esculentus); common starfish (Asterias rubens); brittle star (Ophiothrix sp.); feather star ( sp.); feather star (Cenometra bella); acorn worm (Enteropneusta).

Echinoderms are a large phylum, with about 6,000 living species and a very respectable fossil record going back to early Cambrian times. Those ancient fossils include some weirdly asymmetrical creatures. Indeed, weird is perhaps the adjective that first occurs to one contemplating the echinoderms. A colleague once described the cephalopod molluscs (octopuses, squids and cuttlefish) as 'Martians'. He made a good point, but I think my candidate for the role might be a starfish. A 'Martian', in this sense, is a creature whose very strangeness helps us to see ourselves more clearly by showing us what we are not.

Earth's animals are mainly bilaterally symmetrical: they have a front end and a rear end, a left side and a right side. Starfish are radially symmetrical, with the mouth right in the middle of the lower surface, and the a.n.u.s right in the middle of the top surface. Most echinoderms are similar, but heart urchins and sand dollars have rediscovered a modest degree of bilateral symmetry with a front and a rear for purposes of burrowing through the sand. If 'Martian' starfish have sides at all, they have five sides (or, in a few cases, some larger number), not two like most of the rest of us on Earth. Earth's animals mostly have blood. Starfish have piped sea water instead. Earth's animals mostly move about by means of muscles, pulling on bones or other skeletal elements. Starfish move about by means of a unique hydraulic system, using pumped sea water. Their actual propulsive organs are hundreds of small 'tube feet' on their under surface, arrayed in avenues along the five axes of symmetry. Each tube foot looks like a thin tentacle with a little round sucker on the end. On its own it is too small to move the animal, but the whole array pulling together can do it, slowly but powerfully. A tube foot is extended by hydraulic pressure, exerted by a little squeezed bulb at its near end. Each individual tube foot has a cycle of activity rather like a tiny leg. Having exerted its pull, it releases its sucker, picks itself up and swings forward to take a new grip with the sucker, and pull again.

Sea urchins get around by the same method. Sea cuc.u.mbers, which are shaped like warty sausages, can move this way too, but burrowing ones move the whole body as earthworms do, by alternately squeezing the body so it elongates forward, then pulling the rear up behind. Brittle stars, which have (usually) five slender, waving arms radiating out from a nearly circular central disc, move by rowing with whole arms, rather than dragging themselves along by tube feet. Starfish too have muscles that swing whole arms about. They use them, for example, to engulf prey and pull mussel sh.e.l.ls apart.

'Forward' is arbitrary for these 'Martians', and that includes brittle stars and most urchins as well as starfish. Unlike most Earth life forms, who have a definite front end with a head, a starfish can 'lead' with any one of its five arms. The hundreds of tube feet somehow manage to 'agree' to follow the lead arm at any one time, but the lead role can change from arm to arm. The co-ordination is achieved by a nervous system, but it is a different pattern of nervous system from any others we are accustomed to on this planet. Most nervous systems are based upon a long trunk cable running from front to rear, either along the dorsal side (like our spinal cord) or along the ventral side, in which case it is often double, with a ladder of connections between the left and right sides (as in worms and all arthropods). In a typical Earth creature, the main longitudinal trunk cable has side nerves, often paired in segments repeated serially from front to rear. And it usually has ganglia, local swellings which, when sufficiently large, are dignified with the name of brain. The starfish nervous system is utterly different. As we have come to expect by now, it is radially arranged. There is a complete ring going right round the mouth, from which five (or however many arms there are) cables radiate out, one along each arm. As you would expect, the tube feet along each arm are controlled by the trunk nerve running along it.

In addition to the tube feet, some species also have hundreds of so-called pedicellariae (singular pedicellaria), scattered over the lower surface of the five arms. These have tiny pincers, and are used for catching food, or in defence against small parasites.

Alien 'Martians' though they may appear, starfish and their kind are still our relatively close cousins. Less than four per cent of all animal species are closer cousins to us than starfish are. By far the greater part of the animal kingdom is yet to join our pilgrimage. And they mostly arrive all together, at Rendezvous 26 Rendezvous 26, in one gigantic influx of pilgrims. The protostomes are about to overwhelm even the mult.i.tude of pilgrims who are already on the march.

Rendezvous 26.

PROTOSTOMES.

In the deeps of geological time, and increasingly deprived of the hard support of fossils, we are now entirely reliant on the technique that I referred to in the General Prologue as molecular rangefinding. The upside is that the technique is getting ever more sophisticated. Molecular rangefinding confirms a belief long held by comparative anatomists, or more strictly comparative embryologists, that the greater part of the animal kingdom is deeply divided into two great subkingdoms, the Deuterostomia and the Protostomia.

Here's how embryology comes in. Animals typically pa.s.s through a watershed event in their early life called gastrulation. The distinguished embryologist and scientific iconoclast Lewis Wolpert said: It is not birth, marriage or death, but gastrulation, which is truly the most important time in your life.

Gastrulation is something that all animals do early in their life. Typically, before gastrulation, an animal embryo consists of a hollow ball of cells, the blastula, whose wall is one cell thick. During gastrulation the ball indents to form a cup with two layers. The opening of the cup closes in to form a small hole called the blastopore. Almost all animal embryos go through this stage, which presumably means it is a very ancient feature indeed. You might expect that so fundamental an opening would become one of the two deep holes in the body, and you'd be right. But now comes the big divide in the animal kingdom, between the Deuterostomia (every pilgrim who arrived before Rendezvous 26 Rendezvous 26, including us) and the Protostomia (the huge throng who are now joining at Rendezvous 26 Rendezvous 26).

In deuterostome embryology, the eventual fate of the blastopore is to become the a.n.u.s (or at least the a.n.u.s develops close to the blastopore). The mouth appears later as a separate perforation at the other end of the gut. The protostomes do it differently: in some, the blastopore becomes the mouth, and the a.n.u.s appears later; in others, the blastopore is a slit that subsequently zippers up in the middle, with the mouth at one end and the a.n.u.s at the other. Protostome means 'mouth first'. Deuterostome means 'mouth second'.

[image]

Protostomes join. At this rendezvous the 60,000 or so known deuterostome species join well over a million described protostomes. This protostome phylogeny represents another recent and radical rearrangement brought about by genetics. The two major groupings are now generally accepted, but the order of branching within them is extremely uncertain. The order within the seven lineages on the left ('Lophotrochozoa') is particularly unsure. At this rendezvous the 60,000 or so known deuterostome species join well over a million described protostomes. This protostome phylogeny represents another recent and radical rearrangement brought about by genetics. The two major groupings are now generally accepted, but the order of branching within them is extremely uncertain. The order within the seven lineages on the left ('Lophotrochozoa') is particularly unsure.

Images, left to right: lugworm ( lugworm (Arenicola sp.); garden snail ( sp.); garden snail (Helix aspersa); unknown bryozoan, gastrotrich (Chaetonotus simrothi); zebra polyclad flatworm (Pseudoceros dimidiatus); Antarctic bdelloid rotifer (Philodina gregaria); unknown nematode, leaf-cutter ant (Atta sp.); velvet worm ( sp.); velvet worm (Peripatopsis moseleyi); unknown tardigrade.

This traditional embryological cla.s.sification of the animal kingdom has been upheld by modern molecular data. There are indeed two main kinds of animal, the deuterostomes (our lot) and the protostomes (them over there). However, some phyla that used to be included in the deuterostomes have now been moved by molecular revisionists, whom I shall follow, to the protostomes. These are the three so-called lophophorate phyla the phoronids, brachiopods and bryozoans now grouped together with the molluscs and annelid worms in the 'Lophotrochozoa' division of the protostomes. For goodness' sake don't bother to remember the 'lophophorates' I need to mention them here only because zoologists of a certain age might be surprised not to find them among the deuterostomes. There are also some animals that don't belong to either the protostomes or the deuterostomes, but we'll come to them later.

Rendezvous 26 is the biggest of all, more of a gigantic rally of pilgrims than a rendezvous. When does it happen? Such ancient dates are hard to estimate. My attempt of 590 million years is plus or minus a large margin of error. The same goes for the estimate that Concestor 26 is our 300-million-greats-grandparent. The protostomes const.i.tute the great bulk of the pilgrimage of animals. Because our own species is of the deuterostome persuasion, I have given them special attention in this book, and I am portraying the protostomes as joining the pilgrimage all together, at one major rendezvous. Not only the protostomes themselves would see it the other way around a dispa.s.sionate observer would too. is the biggest of all, more of a gigantic rally of pilgrims than a rendezvous. When does it happen? Such ancient dates are hard to estimate. My attempt of 590 million years is plus or minus a large margin of error. The same goes for the estimate that Concestor 26 is our 300-million-greats-grandparent. The protostomes const.i.tute the great bulk of the pilgrimage of animals. Because our own species is of the deuterostome persuasion, I have given them special attention in this book, and I am portraying the protostomes as joining the pilgrimage all together, at one major rendezvous. Not only the protostomes themselves would see it the other way around a dispa.s.sionate observer would too.

The protostomes have a much greater number of animal phyla than the deuterostomes, including the largest phyla of all. They include the molluscs, with twice as many species as the vertebrates. They include the three great worm phyla: flatworms, roundworms and annelid worms, whose species together outnumber the mammal species perhaps thirtyfold. Above all, the protostome pilgrims include the arthropods: insects, crustaceans, spiders, scorpions, centipedes, millipedes and several other smaller groups. The insects alone const.i.tute at least three-quarters of all animal species, and probably more. As Robert May, the current President of the Royal Society has said, to a first approximation all species are insects.

Before the days of molecular taxonomy, we grouped and divided animals by looking at their anatomy and embryology. Of all the cla.s.sificatory levels species, genus, order, cla.s.s, etc. phylum had a special, almost mystical status. Animals within one phylum were clearly related to one another. Animals in different phyla were too distinct for any relations.h.i.+ps to be taken seriously. The phyla were separated by an all but unbridgeable gulf. Molecular comparison now suggests that the phyla are much more connected than we ever thought they were. In a sense that was always obvious n.o.body believed the animal phyla arose separately from primordial slime. They had to be connected to each other, in the same sort of hierarchical patterns as their const.i.tuent parts. It was just that the connections were hard to see, lost in deep time.

There were exceptions. The protostomedeuterostome grouping above the phylum level was admitted, based on embryology. And within the protostomes it was widely accepted that the annelid worms (segmented earthworms, leeches and bristle worms) were related to arthropods, both having a segmented body plan. That particular connection now seems to be wrong, as we shall see: nowadays the annelids are partnered with the molluscs. Actually, it was always a bit worrying that marine annelids had a kind of larva that was so similar to the larvae of many marine molluscs that they were given the same name, the 'trochoph.o.r.e' larva. If the annelidmollusc grouping is right, it means that the segmented body plan was invented twice (by annelids and arthropods), rather than the trochoph.o.r.e larva being invented twice (by annelids and molluscs). The a.s.sociation of annelids with molluscs, and their separation from arthropods, is one of the bigger surprises that molecular genetics has dealt those zoologists brought up on morphologically based taxonomy.

Molecular evidence divides the protostome phyla into two, or perhaps three, main groups: super-phyla, I suppose we could call them. Some authorities have yet to accept this cla.s.sification, but I shall go along with it while recognising that it could still be wrong. The two super-phyla are called the Ecdysozoa and the Lophotrochozoa. The third super-phylum, which is less widely acknowledged, but which I shall accept rather than lumping them in with the Lophotrochozoa as some prefer, is the Platyzoa.

The Ecdysozoa are named after their characteristic habit of moulting, or ecdysis (from a Greek word meaning roughly to get your kit off). That gives an immediate hint that the insects, crustaceans, spiders, millipedes, centipedes, trilobites and other arthropods are ecdysozoans, and this means that the ecdysozoan faction of the protostome pilgrimage is very large indeed, far more than three-quarters of the animal kingdom.

The arthropods dominate both the land (especially insects and spiders) and the sea (crustaceans and, in earlier times, trilobites). With the exception of the eurypterids, those Palaeozoic sea scorpions1 which, we conjectured, terrorised the Palaeozoic fishes, arthropods have not achieved the enormous body size of some extreme vertebrates. This is often attributed to limits set by their method of encasing themselves in an armour-plated exoskeleton, with their limbs in hard jointed tubes. This means they can grow only by ecdysis: casting their outer casing aside at regular intervals and hardening a new, larger one. How the eurypterids managed to exempt themselves from this alleged size limitation is not entirely clear to me. which, we conjectured, terrorised the Palaeozoic fishes, arthropods have not achieved the enormous body size of some extreme vertebrates. This is often attributed to limits set by their method of encasing themselves in an armour-plated exoskeleton, with their limbs in hard jointed tubes. This means they can grow only by ecdysis: casting their outer casing aside at regular intervals and hardening a new, larger one. How the eurypterids managed to exempt themselves from this alleged size limitation is not entirely clear to me.

There is lingering dispute about how the sub-contingents of arthropods are arranged. Some zoologists uphold the earlier view that the insects belong with the myriapods (centipedes, millipedes and their kind), separated off from the crustaceans. The majority now bracket the insects with the crustaceans, pus.h.i.+ng the myriapods and spiders off as outgroups. Everyone agrees that spiders and scorpions, together with the terrifying eurypterids, belong together in the group called chelicerates. Limulus Limulus, the living fossil known, unfortunately, as the horseshoe crab, is also placed in the chelicerates, despite its superficial resemblance to the extinct trilobites, which are separated off in their own group.

Allied to the arthropods within the Ecdysozoa, and sometimes called panarthropods, are two small contingents of pilgrims, the onychophorans and the tardigrades. Onychophorans or velvet worms, such as Peripatus Peripatus, are now cla.s.sified in the phylum Lobopodia, which has an important fossil contingent, as we shall see in the Velvet Worm's Tale. Peripatus Peripatus itself looks a bit like a caterpillar of rather endearing mien, although in this respect it is outdone by the tardigrades. Whenever I see a tardigrade I want to keep it as a pet. Tardigrades are sometimes called water bears, and they have the cuddly appearance of a baby bear. A very baby bear indeed: you can only just see them without a microscope, waving their eight stubby legs with a charming air of infantile inept.i.tude. itself looks a bit like a caterpillar of rather endearing mien, although in this respect it is outdone by the tardigrades. Whenever I see a tardigrade I want to keep it as a pet. Tardigrades are sometimes called water bears, and they have the cuddly appearance of a baby bear. A very baby bear indeed: you can only just see them without a microscope, waving their eight stubby legs with a charming air of infantile inept.i.tude.

The other major phylum in the superphylum Ecdysozoa is that of the nematode worms. They too are extremely numerous, a fact made memorable long ago by the American zoologist Ralph Buchsbaum: If all the matter in the universe except the nematodes were swept away, our world would still be dimly recognisable ... we should find its mountains, hills, vales, rivers, lakes, and oceans represented by a film of nematodes ... Trees would still stand in ghostly rows representing our streets and highways. The location of the various plants and animals would still be decipherable, and, had we sufficient knowledge, in many cases even their species could be determined by an examination of their erstwhile nematode parasites.

I was delighted by this image when I first read Buchsbaum's book, but I must confess, returning to reread it now, I find myself sceptical. Let's just say that nematode worms are extremely numerous and ubiquitous.

Smaller phyla in the Ecdysozoa include various other kinds of worms, including the priapulid or p.e.n.i.s worms. These are quite aptly named, although the champion in this vein is the fungus whose Latin name is Phallus Phallus (wait for (wait for Rendezvous 34 Rendezvous 34). It is superficially surprising that the priapulids are now cla.s.sified so far from the annelid worms.

The lophotrochozoan pilgrims may be outnumbered by the Ecdysozoa, but even they decisively outnumber our own deuterostome pilgrims. The two big lophotrochozoan phyla are the molluscs and the annelids. The annelid worms are not long confusible with the nematode worms, for the annelids are segmented like the arthropods, as we have seen. This means that their body is arranged as a series of segments fore and aft, like the trucks of a train. Many body parts, for example nerve ganglia and blood vessels running around the gut, are repeated in every segment along the length of the body. The same is true of arthropods, most obviously millipedes and centipedes because their segments are all pretty much the same as each other. In a lobster or, even more, a crab, many of the segments are different from each other, but you can still clearly see that the body is segmented in the fore-and-aft direction. Their ancestors surely had more uniform segments like a woodlouse or a millipede.2 Annelid worms are like millipedes or woodlice in this respect, although the worms are more closely related to the non-segmented molluscs. The most familiar annelid worms are common or garden (for once the phrase is strictly apt) earthworms. I am privileged to have seen giant earthworms ( Annelid worms are like millipedes or woodlice in this respect, although the worms are more closely related to the non-segmented molluscs. The most familiar annelid worms are common or garden (for once the phrase is strictly apt) earthworms. I am privileged to have seen giant earthworms (Megascolides australis), in Australia, said to be capable of growing to four metres long.

The Lophotrochozoa include other worm-like phyla, for instance the nemertine worms, not to be confused with the nematodes. The similarity of name is unfortunate and unhelpful, compounded by further confusion with two other worm phyla, the Nematomorpha and the Nemertodermatida. Nema (nematos) in Greek means 'thread', while Nemertes was the name of a sea nymph. Unfortunate coincidence, that. On a school marine biology field trip to the Scottish coast with our inspiring zoology teacher Mr I. F. Thomas, we found a bootlace worm, Lineus longissimus Lineus longissimus, a species of nemertine legendarily capable of growing to 50 metres. Our specimen was at least 10 metres long, but I don't remember the exact measurement, and Mr Thomas has sadly lost his photograph of this unforgettable occasion, so it will have to remain as a nemertean version of a fisherman's tall tale.

There are various other more-or-less worm-like phyla, but the biggest and most important phylum of the Lophotrochozoa is the Mollusca: the snails, oysters, ammonites, octopuses and their kind. The mollusc contingent of the pilgrimage mostly creeps at snail's pace, but squids are among the fastest swimmers in the sea, using a form of jet propulsion. They, and their cousins the octupuses, are the most spectacularly proficient colour-changers in the animal kingdom, streets better than the proverbial chameleons, not least because they change in quick time. The ammonites were relatives of the squids who lived in coiled sh.e.l.ls that served them as flotation organs, as with the still surviving Nautilus Nautilus. Ammonites once thronged the seas but went finally extinct at the same time as the dinosaurs. I hope they changed colour too.

Another major group of molluscs is the bivalves: oysters, mussels, clams and scallops, with two sh.e.l.ls or valves. Bivalves have a single extremely powerful muscle, the adductor, whose function is to close the valves and lock in the closed position against predators. Don't put your foot in a giant clam (Tridacna) you'll never get it back. The bivalves include Teredo Teredo, the s.h.i.+pworm, which uses its valves as cutting tools to bore through driftwood, wooden s.h.i.+ps and the pilings of piers and quays. You will probably have seen their holes, of cleanly circular cross-section. Piddocks do something similar through rock.

Superficially like bivalve molluscs are the brachiopods, the lamp sh.e.l.ls. They are also part of the great lophotrochozoan contingent of the protostome pilgrimage, but are not closely related to the bivalve molluscs. We have already met one of them, Lingula Lingula, in the Lungfish's Tale, as a famous 'living fossil'. There are now only about 350 species of brachiopod, but in the Palaeozoic Era they rivalled the bivalve molluscs.3 The resemblance between them is superficial: the bivalve molluscs' two sh.e.l.ls are left and right, where the two brachiopod sh.e.l.ls are top and bottom. The status of the brachiopod pilgrims, and two allied 'lophophorate' groups called phoronids and bryozoans, is still disputed. As already mentioned, I am following the dominant contemporary school of thought in placing them in the Lophotrochozoa (to which name, indeed, they have contributed). Some zoologists leave them where they used to be, outside the protostomes altogether and in the deuterostomes, but I suspect theirs is a losing battle. The resemblance between them is superficial: the bivalve molluscs' two sh.e.l.ls are left and right, where the two brachiopod sh.e.l.ls are top and bottom. The status of the brachiopod pilgrims, and two allied 'lophophorate' groups called phoronids and bryozoans, is still disputed. As already mentioned, I am following the dominant contemporary school of thought in placing them in the Lophotrochozoa (to which name, indeed, they have contributed). Some zoologists leave them where they used to be, outside the protostomes altogether and in the deuterostomes, but I suspect theirs is a losing battle.

The third major branch of the protostome super-phylum, the Platyzoa, would be joined by some authorities to the Lophotrochozoa. 'Platy' means 'flat', and the name Platyzoa comes from one of the component phyla, the flatworms or Platyhelminthes. 'Helminth' means 'intestinal worm', and while some flatworms are parasitic (tapeworms and flukes), there is also a large group of freeliving flatworms, the turbellarians, which are often extremely beautiful. Recently, some of the animals traditionally cla.s.sified as flatworms, for example the acoels, have been removed by molecular taxonomists out of the protostomes altogether. We shall meet them presently.

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Ceci n'est pas une coquille. Fossil brachiopod ( Fossil brachiopod (Doleorthis) from the Silurian.

Other phyla are provisionally placed in the Platyzoa, but for the moment it is for want of anywhere more certain to put them, and they are mostly not flat. Belonging to the so-called 'minor phyla', they are fascinating in their own right and each deserves a whole chapter in a textbook of invertebrate zoology. Unfortunately, however, we have a pilgrimage to complete and must press on. Of these minor phyla I shall just mention the rotifers, because they have a tale to tell.

Rotifers are so small that they were originally grouped with single-celled protozoan 'animalcules'. They are actually multicellular and quite complicated in miniature. One group of them, the bdelloid rotifers, are remarkable because no male has ever been seen. This is what their tale is about, and we shall come to it soon.

So this vast flood of protostome pilgrims, composite of tributaries far and wide, truly the dominant stream of animal pilgrims, converges on its rendezvous with the deuterostomes, the junior (by comparison) contingent, whose progress we have hitherto followed for the sufficient reason that it is our own. The grand ancestor of both, Concestor 26 from our human point of view, is extremely hard to reconstruct at such a remote distance of time.

It seems very likely that Concestor 26 was some kind of worm. But that is only to say a long thing, bilaterally symmetrical, with a left and a right side, a dorsal and a ventral side, and a head and a tail end. Indeed, some scientists have given the name Bilateria to all the animals descended from Concestor 26, and I shall use this word. Why is this pattern, the worm form, so common? The most primitive members of all three protostome subgroups, and the most primitive deuterostomes, are all of the form that we should generally call worm-shaped. So let's have a tale about what it means to be a worm.

I wanted to put the worm's tale into the grey and muddy mouth of the lugworm.4 Unfortunately, the lugworm spends most of its time in a U-shaped burrow, which is just what we don't need for the tale, as will soon become apparent. We need a more typical worm, which actively crawls or swims in a forward direction: for whom front and rear, left and right, and up and down have a clear meaning. So the lugworm's close cousin, Unfortunately, the lugworm spends most of its time in a U-shaped burrow, which is just what we don't need for the tale, as will soon become apparent. We need a more typical worm, which actively crawls or swims in a forward direction: for whom front and rear, left and right, and up and down have a clear meaning. So the lugworm's close cousin, Nereis Nereis the ragworm, shall take over the role. An 1884 magazine article for anglers said, 'The bait used is that damp kind of centipede called a ragworm.' It is not a centipede, of course, but a polychaete worm. It lives in the sea, where it normally crawls over the bottom but is capable of swimming if necessary. the ragworm, shall take over the role. An 1884 magazine article for anglers said, 'The bait used is that damp kind of centipede called a ragworm.' It is not a centipede, of course, but a polychaete worm. It lives in the sea, where it normally crawls over the bottom but is capable of swimming if necessary.

THE RAGWORM'S TALE.

Any animal that moves, in the sense of covering the ground from A to B rather than just sitting in one place and waving its arms or pumping water through itself, is likely to need a specialised front end. It might as well have a name, so let's call it the head. The head hits novelty first. It makes sense to take in food at the end that encounters it first, and to concentrate the sense organs there too eyes perhaps, some kind of feelers, organs of taste and smell. Then the main concentration of nervous tissue the brain had best be near the sense organs, and near the action at the front end, where the food-catching apparatus is. So we can define the head end as the leading end, the one with the mouth, the main sense organs and the brain, if there is one. Another good idea is to void wastes somewhere near the back end, far from the mouth, to avoid re-imbibing what has just been pa.s.sed out. By the way, although all this makes sense if we think worm, I should remind you that the argument evidently does not apply to radially symmetrical animals such as starfish. I am genuinely puzzled why starfish and their kind opt out of this argument, which is one reason why I referred to them as 'Martians'.

To return to our primeval worm, having dealt with its fore and aft asymmetry, how about up-down asymmetry? Why is there a dorsal side and a ventral side? The argument is similar, and this one applies to starfish just as much as to worms. Gravity being what it is, there are lots of inevitable differences between up and down. Down is where the sea bottom is, down is where the friction is, up is where the sunlight comes from, up is the direction from which things fall on you. It is unlikely that dangers will threaten equally from below and above, and in any case those dangers are likely to be qualitatively different. So our primitive worm should have a specialised upper or 'dorsal' side and a specialised 'ventral' or lower side, rather than simply not caring which side faces the sea bottom and which side faces the sky.

Put our front-rear asymmetry together with our dorsal-ventral asymmetry, and we have automatically defined a left side and a right side. But unlike the other two axes, we find no general reason to distinguish the left side from the right side: no reason why they should be anything other than mirror images. Danger is not more likely to threaten from the left than the right, or vice versa. Food is not more likely to be found on the left or the right side, though it may well be more likely above or below. Whatever is the best way for a left side to be, there is no general reason to expect any difference for the right. Limbs or muscles that were not mirrored left-right would have the unfortunate effect of driving the animal round in circles, instead of in direct pursuit of some goal.

Perhaps revealingly, the best exception I can think of is fictional. According to a Scottish legend (probably invented for the amus.e.m.e.nt of tourists, and said to be believed by many of them), the haggis is a wild animal living in the Highlands. It has short legs on one side and long legs on the other, in accordance with its habit of running only one way round the sides of steep Highand hillsides. The prettiest real-life example I can think of is the wonky-eyed jewel squid of Australian waters, whose left eye is much larger than its right. It swims at a 45-degree angle, with the larger, telescopic left eye looking upwards for food, while the smaller right eye looks below for predators. The wrybill is a New Zealand sandpiper whose bill curves markedly to the right. The bird uses it to flick pebbles to the side and expose prey. Striking 'handedness' is to be seen in fiddler crabs, who have one hugely enlarged claw for fighting or, more to the point, displaying their ability to fight. But perhaps the most intriguing story of asymmetry in the animal kingdom was told me by Sam Turvey. Trilobite fossils often display bite marks, indicating narrow escapes from predators. The fascinating thing is that about 70 per cent of these bite marks are on the right-hand side. Either trilobites had an asymmetrical awareness of predators, like the wonky-eyed jewel squid, or their predators had handedness in their attack strategy.

But those are all exceptions, mentioned for their curiosity value and to make a revealing contrast with the symmetrical world of our primitive worm and its descendants. Our crawling archetype has a left and a right side which are mirror images of each other. Organs tend to arise in pairs, and where there are exceptions, such as the wonky-eyed jewel squid, we notice it and comment.

How about eyes? Would the first bilaterian have had eyes? It isn't enough to say that all modern descendants of Concestor 26 have eyes. It isn't enough, because the various kinds of eyes are very diverse: so much so that it has been estimated that 'the eye' has evolved independently more than 40 times in various parts of the animal kingdom.5 How do we reconcile this with the statement that Concestor 26 had eyes? How do we reconcile this with the statement that Concestor 26 had eyes?

To give intuition a steer, let me say first that what is claimed to have evolved 40 times independently is not light-sensitivity per se, but image-forming optics. The vertebrate camera eye and the crustacean compound eye evolved their optics (working on radically different principles) independently of one another. But both these eyes are descended from one organ in the common ancestor (Concestor 26), which was probably an eye of some kind.

The evidence is genetic, and it is persuasive. In the fruit fly Drosophila Drosophila there is a gene called there is a gene called eyeless eyeless. Geneticists have the perverse habit of naming genes by what goes wrong when they mutate. The eyeless eyeless gene normally negates its name by making eyes. When it mutates and fails to have its normal effect on development, the fly has no eyes, hence the name. It is a ludicrously confusing convention. To avoid it, I shall not refer to the gene normally negates its name by making eyes. When it mutates and fails to have its normal effect on development, the fly has no eyes, hence the name. It is a ludicrously confusing convention. To avoid it, I shall not refer to the eyeless eyeless gene, but will use the comprehensible abbreviation gene, but will use the comprehensible abbreviation ey ey. The ey ey gene normally makes eyes, and we know this because when it goes wrong the flies are eyeless. Now the story starts to get interesting. There is a very similar gene in mammals, called gene normally makes eyes, and we know this because when it goes wrong the flies are eyeless. Now the story starts to get interesting. There is a very similar gene in mammals, called Pax6 Pax6, also known as small eye small eye in mice and in mice and aniridia aniridia (no iris) in humans (again named for the negative effect of its mutant form). (no iris) in humans (again named for the negative effect of its mutant form).

The DNA sequence of the human aniridia aniridia gene is more similar to the fruit fly's gene is more similar to the fruit fly's ey ey gene than it is to other human genes. They must be inherited from the shared ancestor which was, of course, Concestor 26. Again, I shall call it gene than it is to other human genes. They must be inherited from the shared ancestor which was, of course, Concestor 26. Again, I shall call it ey ey. Walter Gehring and his colleagues in Switzerland did an utterly fascinating experiment. They introduced the mouse equivalent of the ey ey gene into fruit fly embryos, with astounding results. When introduced into the part of a fruit fly embryo that was destined to make a leg, it caused the eventual adult fly to grow an extra 'ectopic' eye on its leg. It was a fly eye, by the way: a compound eye, not a mouse eye. I don't think there is any evidence that the fly could see through it, but it had the unmistakable properties of a respectable compound eye. The instruction given by the gene into fruit fly embryos, with astounding results. When introduced into the part of a fruit fly embryo that was destined to make a leg, it caused the eventual adult fly to grow an extra 'ectopic' eye on its leg. It was a fly eye, by the way: a compound eye, not a mouse eye. I don't think there is any evidence that the fly could see through it, but it had the unmistakable properties of a respectable compound eye. The instruction given by the ey ey gene seems to be 'grow an eye here, of the kind that you would normally grow'. The fact that the gene is not only similar in mice and flies, but induces the development of eyes in both, is very strong evidence that it was present in Concestor 26; and moderately strong evidence that Concestor 26 could see, even if only the presence versus the absence of light. Perhaps, when more genes have been investigated, the same argument can be generalised from eyes to other bits. In fact, in one sense, this has already been done we'll deal with it in the Fruit Fly's Tale. gene seems to be 'grow an eye here, of the kind that you would normally grow'. The fact that the gene is not only similar in mice and flies, but induces the development of eyes in both, is very strong evidence that it was present in Concestor 26; and moderately strong evidence that Concestor 26 could see, even if only the presence versus the absence of light. Perhaps, when more genes have been investigated, the same argument can be generalised from eyes to other bits. In fact, in one sense, this has already been done we'll deal with it in the Fruit Fly's Tale.

The brain, sitting at the front end for the reasons we have argued, needs to make nervous contact with the rest of the body. In a wormshaped animal, it is sensible that it should do so via a main cable, a princ.i.p.al nerve trunk, running along the length of the body, probably with side branches at intervals along the body to exercise local control and take in local information. In a bilaterally symmetrical animal like a ragworm or a fish, the trunk nerve must run either dorsal or ventral of the digestive tract, and here we strike one of the main differences between us deuterostomes on the one hand and the protostomes, who have joined us in such strength, on the other. In us, the spinal nerve cord runs along the back. In a typical protostome like a ragworm or a centipede, it is on the ventral side of the gut.

If Concestor 26 was indeed some kind of worm, it presumably followed either the dorsal nerve pattern or the ventral nerve pattern. I can't call them deuterostome and protostome patterns because the two separations don't quite coincide. The acorn worms (those rather obscure deuterostomes who arrived with the echinoderms at Rendezvous 25 Rendezvous 25) are hard to interpret, but at least on some views they have a ventral nerve cord like a protostome, although for other reasons they are cla.s.sified as deuterostomes. Let me instead divide the animal kingdom into the dorsocords and the ventricords. The dorsocords are all deuterostomes. The ventricords are mostly protostomes, plus some early deuterostomes perhaps including the acorn worms. The echinoderms, with their remarkable reversion to radial symmetry, don't fit into this cla.s.sification at all. Probably the deuterostomes, as I say, were still ventricords until some time later than Concestor 26.

The difference between dorsocords and ventricords extends to other things than just the position of the main nerve running along the body. Dorsocords have a ventral heart, whereas ventricords have a dorsal heart, pumping blood forward along a main dorsal artery. These and other details suggested in 1820 to the great French zoologist Geoffroy St Hilaire that a vertebrate could be thought of as an arthropod, or an earthworm, turned upside down. After Darwin and the acceptance of evolution, zoologists from time to time suggested that the vertebrate body plan had actually evolved through a worm-like ancestor literally turning upside down.

That is the theory that I want to support here, on balance and with some caution. The alternative, which is that a worm-like ancestor gradually rearranged its internal anatomy while staying the same way up, seems to me less plausible because it would have involved a greater amount of internal upheaval. I believe a change in behaviour came first suddenly by evolutionary standards and it was followed by a whole lot of consequential evolutionary changes. As so often, there are modern equivalents to make the idea vivid for us today. The brine shrimp is one example, and we hear its tale next.

THE BRINE SHRIMP'S TALE.

Brine shrimps, Artemia Artemia, and the closely related fairy shrimps are crustaceans that swim on their backs, and therefore have their nerve cord (the 'true' zoological ventral side) on the side that now faces the sky. The upside-down catfish, Synodontis nigriventris Synodontis nigriventris, is a deuterostome that does the same thing the other way round. It is a fish that swims on its back, and therefore has its main trunk nerve on the side facing the river bottom, which is the 'true' zoological dorsal side. I don't know why brine shrimps do it, but the catfish swim upside down because they take food from the water surface, or from the undersides of floating leaves. Presumably, individual fish discovered that this was a good source of food and learned to turn over. My conjecture6 is that, as the generations went by, natural selection favoured those individuals who learned to perform the trick best, their genes 'caught up' with the learning, and now they never swim any other way. is that, as the generations went by, natural selection favoured those individuals who learned to perform the trick best, their genes 'caught up' with the learning, and now they never swim any other way.

The brine shrimp's inversion is a recent re-enactment of something that happened, in my view, more than half a billion years ago. An ancient, long-lost animal, some kind of worm with a ventral nerve cord and a dorsal heart like any protostome, turned over and swam, or crawled, upside down like a brine shrimp. A zoologist who happened to be present at the time would have died rather than relabel the main nerve trunk dorsal just because it now ran along the side of the body facing the sky. 'Obviously', all his zoological training would have told him, it was still a ventral nerve cord, corresponding to all the other organs and features that we expect to see on the ventral surface of a protostome. Equally 'obvious' to this Precambrian zoologist, the heart of our inverted worm was, in the deepest sense, a 'dorsal' heart, even though it now beat under the skin nearest the sea bottom.

Given enough time, however given enough millions of years of swimming or crawling 'upside down' natural selection would come to reshape all the organs and structures of the body to fit in with the upside-down habit. Eventually, unlike our modern brine shrimp, which has only recently turned over, the traces of the original dorsal/ventral h.o.m.ologies would become obliterated. Later generations of palaeo-zoologists who encountered the descendants of this early maverick, after some tens of millions of years of upside-down habit, would start to redefine their concepts of dorsal and ventral. This is because so many anatomical details would have changed over evolutionary time.

Other animals that swim on their backs are sea otters (especially when engaging in their remarkable habit of smas.h.i.+ng sh.e.l.lfish with stones on the belly), and the aptly named backswimmers (all the time). Backswimmers are a kind of bug,7 sometimes known as greater water boatmen, which row themselves underwater with their legs. The related lesser water boatmen do the same kind of thing, but they swim the right way up. sometimes known as greater water boatmen, which row themselves underwater with their legs. The related lesser water boatmen do the same kind of thing, but they swim the right way up.

Imagine that the descendants of our modern water boatmen or brine shrimps on the one hand, and the descendants of our modern upside-down catfish on the other, were to maintain their habits of swimming upside down for 100 million years into the future. Isn't it entirely likely that they might each give rise to a whole new subkingdom, each body plan so radically reshaped by the upside-down habit that zoologists who didn't know the history would define the brine shrimps' descendants as having a 'dorsal' nerve cord, and the descendants of the catfish as having a 'ventral' nerve cord.

As we saw in the Ragworm's Tale, the world presents important practical differences between up and down, and these would start to imprint themselves, by natural selection, on the sky-pointing side and the floor-pointing side respectively. What had once been the zoologically ventral side would start to look more and more like a zoologically dorsal side, and vice versa. I believe this is exactly what happened somewhere along the line leading to vertebrates, and that is why we now have a dorsal nerve cord and a ventral heart. Modern molecular embryology offers some supporting evidence from the ways in which genes that define the dorso-ventral axis are expressed genes a bit like the Hox genes that we shall meet in the Fruit Fly's Tale but the details are beyond our scope here.

The upside-down catfish, recent though its inverted habit undoubtedly is, has already taken one revealing little step in this evolutionary direction.8 Its Latin name is Its Latin name is Synodontis nigriventris. Nigriventris Synodontis nigriventris. Nigriventris means 'dark belly', and it introduces a fascinating vignette at the end of the Brine Shrimp's Tale. One of the main differences between up and down in the world is the predominant direction of light. While not necessarily directly overhead, the sun's rays generally come from above rather than below. Hold your fist up and you'll find, even under an overcast sky, that its upper surface is better lit than its lower surface. This fact opens a key way in which we and many other animals can recognise solid, three-dimensional objects. A uniformly coloured curved object, such as a worm or a fish, looks lighter on top, darker below. I am not talking about the hard shadow cast by the body it is a more subtle effect than that. A gradient of shading, from lighter above to darker below, smoothly betrays the curvature of the body. means 'dark belly', and it introduces a fascinating vignette at the end of the Brine Shrimp's Tale. One of the main differences between up and down in the world is the predominant direction of light. While not necessarily directly overhead, the sun's rays generally come from above rather than below. Hold your fist up and you'll find, even under an overcast sky, that its upper surface is better lit than its lower surface. This fact opens a key way in which we and many other animals can recognise solid, three-dimensional objects. A uniformly coloured curved object, such as a worm or a fish, looks lighter on top, darker below. I am not talking about the hard shadow cast by the body it is a more subtle effect than that. A gradient of shading, from lighter above to darker below, smoothly betrays the curvature of the body.

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Turn the fish upside down. Upside-down catfish ( Upside-down catfish (Synodontis nigriventris) in characteristic pose.

It works in reverse. The photograph of moon craters is printed upside down. If your eye (well, to be more precise, your brain) works in the same way as mine, you will see the craters as hills. Turn the book upside down, so that the light appears to come from another direction, and the hills will turn into the craters that they truly are.

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Turn the book upside down. Craters on the far side of the moon. Craters on the far side of the moon.

One of my very first experiments as a graduate student demonstrated that newly hatched baby chicks seem to see the same illusion, straight out of the egg. They peck at photographs of simulated grains, and strongly prefer them if lit as if from above. Turn the photograph over and they shun it. This seems to show that baby chicks 'know' that light in their world normally comes from above. But since they have only just hatched out of the egg, how do they know? Have they learned it during their three days of life? It is perfectly possible, but I tested it experimentally and found it not to be so. I raised chicks and tested them in a special cage in which the only light they ever saw came from below. Experience of pecking grain in this upside-down world would, if anything, teach them to prefer upside-down photographs of solid grains. Instead, they behaved exactly like normal chicks raised in the real world with light coming from above. Apparently because of genetic programming, all the chicks prefer to peck at photographs of solid objects lit from above. The solidity illusion (and hence, if I am right, the 'knowledge' of the predominant direction of light in the real world) seems to be genetically programmed in chicks what we used to call 'innate' rather than learned as (I'm guessing) it probably is in us.

Whether learned or unlearned, there is no doubt that the surface shading illusion of solidity is a powerful one. It has provoked a subtle form of camouflage called countershading. Look at any typical fish, out of water on a slab, and you'll notice that the belly is much lighter in colour than the back. The back may be dark brown or grey, while the belly is light grey, verging on white i