In The Blink Of An Eye

by Andrew Parker

  I picked up the largest piece of thin, flat shale on the table. It had the dimensions of a large roof slate, and its smooth surface bore a detail of the most fearsome member of the Burgess community - Anomalocaris. The body was big, nearly half a metre long and broad with it. Emerging from the head, the grasping forelimbs, once thought to be shrimp-like animals in their own right, were obvious. And I had already identified the front end of the body thanks to another give-away clue - the large pair of eyes that were equally obvious.

  The eyes of Anomalocaris appeared as two buttons jutting out from the sides of the head. Their smooth, rounded outlines were obvious, although that was all to be seen with the naked eye. But their position on the sides of the head suggested these were eyes and nothing else. In Chapter 1 we learnt that no new animal phyla have evolved on Earth since the Cambrian explosion - the phyla we see today are those that existed in the Cambrian (with few possible exceptions). There is a law also that animals today live and function as did their ancestors in the Cambrian. There have been no magical periods in history since the Cambrian explosion where things happened differently. Today it is clear that the button-like structures protruding slightly from the head of Anomalocaris could be only one thing - eyes.

  Figure 7.6 Anomalocaris and Waptia from the Burgess Shale. At around 7.5cm, Waptia is several times smaller than Anomalocaris.

  Back in the laboratory at the Smithsonian Institution, I examined the well-preserved analogues of another member of the Burgess community - Waptia. Waptia was a shrimp-like animal, a member of the arthropod phylum and possibly a crustacean. It was also about the size of an average shrimp of today, and seemed to share the shrimp’s eye characteristics. Like shrimps and crabs, Waptia had eyes on stalks. This means that its eyes could have moved independently of its head. They would have been specialists at looking within a narrow range of the Cambrian environment in detail. They would have seen Anomalocaris as it swam in front of them. But as Anomalocaris moved, the eyes of Waptia would have moved too, and followed their giant neighbour. Unlike the compound eyes of insects, which are known as sessile because they are fused with the head and so cannot move independently, stalked eyes can change their field of view without head movement.

  I mentioned ‘compound’ eyes during this discussion of Waptia. Although the eyes of the Anomalocaris I examined revealed little additional detail under the microscope, a microscopic view of a well-preserved Waptia specimen told a different story. The internal architecture of the Waptia eye became evident - and it matched that of a crustacean today. The stalked apposition compound eyes of a crustacean known as a ‘mysid’ are producing images of animals swimming past them in the sea today. And Waptia would have seen similar pictures in Cambrian seas. Waptia had apposition compound eyes.

  Figure 7.7 Micrographs of the heads of a living ‘mysid’ crustacean and Waptia from the Burgess Shale. Eyes show comparable internal architectures. Scale bars represent 2mm (top picture) and 0.5mm (bottom picture).

  Looking through the collection of arthropods in the Smithsonian’s Burgess Shale collection, it became obvious that Anomalocaris and Waptia are not alone. They were not the sole beneficiaries of vision: far from it.

  Within the Smithsonian fossil deposit, the Burgess specimens are enclosed by a large metal cage, which provides additional security in the style of a bank vault. Doug Erwin is custodian of Charles Doolittle Walcott’s collection today, which embraces quite a variety of multicelled animal forms. Doug kindly allowed me use of his microscope, a key to the Burgess vault, and a large wooden tray.

  Examining the invaluable fossils was time-consuming. They were stored in dozens of cabinets, with hundreds of drawers full of specimens. I looked into each drawer and tried to select the best-preserved representatives to fill my tray. This is difficult to do with the naked eye, and I probably missed some informative examples.

  When I had made each selection, the individual fossil was placed in my tray and an official museum form was put in the empty space in the drawer. On the back of each fossil was painted a catalogue number, and this, along with my name and the name of the specimen and its original location was recorded on the form. The level of security and guardian-ship echoed that at the Burgess quarries themselves. The small quarries are approached by only one path - there are no back doors on the exposed mountainside. In the vicinity of the quarry, the path is policed by Des Collins’s field team, whose camp is positioned just the other side of the path to the Burgess quarries. The two exits of the path, each at least three hours hike from the quarries, are patrolled by wardens from Parks Canada. And the security pays off. The world fossil trade is a considerable one. There are many private fossil collections and shops around the world. Some include complete skeletons of dinosaurs, such as T. rex, but none contains a single specimen from the Burgess Shale.

  I examined specimens of the Burgess arthropods Canadaspis, Odaraia, Perspicaris, Sanctacaris, Sarotrocercus, Sidneyia and Yohoia. All possessed eyes, varying in size with respect to body length. Again, the smaller specimens appeared to have relatively larger eyes. And all these ‘eyes’ really were eyes; based on comparisons with the visual organs of living species, they would have formed images in the Cambrian. In many other Burgess arthropods, the presence or absence of eyes could not be resolved with accuracy due to imperfect preservation or unfavourable orientations within the rock. Maybe I had chosen the wrong specimens to examine. For instance, I failed to detect the eyes of perhaps the commonest Burgess arthropod, Marrella. Recently Des Collins and his Spanish colleague Diego Garcia-Bellido identified eyes on Marrella resembling those of woodlice today. But I was certain of one thing - eyes were common in the Burgess arthropods.

  There are a few Burgess animals from other phyla with eyes, but not many. Actually there may be only Nectocaris and the weird, five-eyed Opabinia. But then Opabinia is probably an arthropod, although Nectocaris appears closer to the chordates than the arthropods. More specimens of these rare species are needed in order to classify them with certainty. But eyes are either rare or absent in the non-arthropod Burgess animals.

  Figure 7.8 Yohoia, Perspicaris, Nectocaris and Sarotrocercus - examples of Burgess animals with eyes.

  The Burgess Shale community lived in the Cambrian, but more precisely they lived 515 million years ago. The question we would most like to answer in the chapter is ‘When did the first eye appear on Earth?’. Now we know that eyes were well in place on Earth some 515 million years ago, but the Cambrian explosion took place sometime between 543 and 538 million years ago. So at this point I will leave the Burgess Shale fauna and continue my search for eyes in other, older fossils (I hope) from the Cambrian period.

  Other Cambrian eyes

  On the subject of weird-looking Cambrian fossils, Cambropachycope and its relatives are bizarre arthropods that were the ancestors of the crustaceans of today. They are known from Cambrian fossils preserved in the ‘Orsten’ limestone of Sweden. Their preservation is actually quite exceptional, and in full 3D. The German palaeontologist Dieter Walossek is responsible for the excellent interpretations of these fossils, and as their guardian he obligingly sent a specimen of Cambropachycope to me for examination in electron microscopes. I was interested in this animal for one reason in particular - its eye. I use the singular here because Cambropachycope had a huge visual organ compared with its body size . . . but only one of them.

  Cambropachycope was a small arthropod, just a few millimetres long. Its body is distinct for having a big, paddle-shaped limb on either side, so swimming may have been possible. The head of Cambropachycope is just as unusual. It is fused with the rest of the body, and has an obvious mouth near the fusion. But then it constricts to form both a false ‘neck’ and a huge bulbous projection in front of the body and mouth. The projection is basically a compound eye. Maybe it evolved following the fusion of two stalked eyes, but it certainly would have seen whatever was ahead of it with some accuracy. I drew this conclusion after studying its cornea - unfortunately that
’s all that remains of this eye.

  Although from the Cambrian, Cambropachycope and the other Orsten arthropods with eyes are no older than the Burgess Shale community. But, as we learnt in Chapter 1, there is a site in China where an exceptionally well-preserved suite of Cambrian fossils has been recovered. And these ‘Chengjiang’ fossils are ten million years older than those of the Burgess Shale.

  Figure 7.9 The tiny Cambrian arthropod Cambropachycope, with a single compound eye.

  Figure 7.10 The Cambrian arthropods Canadaspis laevigata and Fortiforceps foliosa from Chengjiang, China.

  The Chengjiang fossils also include many species with eyes. Here there are both stalked eyes that are moveable, and sessile eyes that are fused with the body in any of several possible positions. They can arise from the underside of the animal, extending forwards under the front margin of the head shield, such as in Fuxianhuia, Leanchoilia and Isoxys. In Retifacies, however, the eyes also sprout from the underside of the body but do not protrude forward. Then again the eyes of Chengjiang animals can also be positioned on top of the body, such as in Xandarella.

  Like the Burgess fossils, most if not all eyes in the Chengjiang community belong to the arthropods. And these two fossil assemblages have been used to trace the position of the eye on the body through time. It is believed that the compound eyes of Cambrian arthropods shifted position from the under side to the top side of the body, and became successively incorporated into the shield or shell that covers the head. I am not sure how much we can read into this, but the same event may have taken place independently in another group of arthropods to those considered up till now - the trilobites. I will return to trilobites shortly.

  It is interesting that nearly all of the Cambrian animals I have mentioned up to this point are arthropods - they belong to the phylum with hard, external skeletons that include crabs and insects. But during my description of eyes in animals today in the first half of this chapter, other phyla were very much involved. There were the swimming alciopid bristle worms in the annelid phylum (1), box jellyfishes in the cnidarian phylum (2), velvet worms in the onycophoran phylum (3), cuttlefishes and snails in the molluscan phylum (4), and of course ourselves in the chordate phylum (5). These animals all have image-forming ‘simple’ eyes. Then there were the ark clams within the molluscan phylum (4), and the fan worms within the annelid phylum (1) that, along with the arthropods (6), possess image-forming ‘compound’ eyes. But do any of these non-arthropod animals have Cambrian ancestors with eyes?

  Figure 7.11 The evolutionary tree of animals at the level of phyla (all those with representatives alive today are included; note that Choanoflagellata is not a true multicelled group). Asterisks mark the phyla with eyes (which are also numbered 1 to 6 as they appear in the text). Modified from a paper by Rouse and Fauchald.

  The answer to this question can obviously be ‘no’ when the eyed group did not evolve within its phylum until after the Cambrian, as determined from computer-generated predictions of the evolutionary tree. This applies to the cuttlefish group, a branch within the mollusc phylum. In fact the most primitive molluscs, which date back to the Cambrian, are eyeless. For similar reasons, the groups of bristle worms with eyes today can also be ruled out of the Cambrian eye club. So who is left in this ancient visual circle after the first round of elimination? The contenders now are the arthropods (1) and chordates (2), who together boast the majority of eyes today, and velvet worms (3) and box jellyfish (4).

  The box jellyfish and velvet worms can be discarded as hosts of Cambrian eyes, because they probably can’t see as such today. Both groups probably cannot see images that flow through the brain like the frames of a movie. The box jellyfish has no brain with which to interpret the information coding for a series of images, and its single eye remains very much a mystery. The eyes of velvet worms do not produce proper images, but are probably rather adapted to movement - they notice the approach of fast-moving individuals, but cannot make identifications. These organs may virtually bypass the brain. In true eyes, an image is assembled in the brain. The brain then makes a decision on how to react, and has the whole body at its disposal. In the case of the box jellyfish and velvet worms, as well as the bristle worms with compound eyes, their ‘visual organs’ may simply be binary detectors. A visual signal is interpreted by the organ as either react or do nothing. A camouflaged velvet worm may freeze when a fast-moving animal approaches. The brain is not needed during this process - the detector is wired directly to the muscles that perform the single response. This form of detection has nothing to do with vision. And to substantiate this further, the fossils of box jellyfish and velvet worms provide no evidence of eyes in the Cambrian. So now our list is reduced to just the arthropods and chordates.

  Sometimes relatives of today’s eyed species did exist in the Cambrian. To decide whether these ancestors, or indeed any extinct group, possessed eyes in the Cambrian, we must turn to Cambrian fossils and the law of minimum eye size.

  There are few chordates known from the Cambrian. The best known are Pikaia from the Burgess Shale, and the earliest of all Haikouella from Chengjiang. Fossils of Pikaia reveal a clear body outline along with fine details of internal parts, including muscles and a notochord, a kind of backbone. But features of the front end of the animal are too small to be seen without a microscope. They are, consequently, too small to be eyes. The same can be said of all Cambrian chordates - they could not see.

  Figure 7.12 Haikouella lanceolata from Chengjiang - the earliest known chordate.

  Today most blind chordates live in environments with extremely little or no light. Think of the mole. And then there is the Mexican cave fish that has eyes where light is present, and no eyes where light is absent. But there are at least two species of chordate known from the Cambrian, and they lived in sunlit environments. Indeed, many of their neighbours had eyes. So where most of this group have eyes today, why did they not in the Cambrian? This is not what we would expect. The idea that life happened in the Cambrian as it continues today fits for arthropods - they can see now and they could see then. And most modern chordates can see.

  So far I have considered that the eye evolved at only one point in time, and that all eyes in existence today stem from that ancestral organ. This implies that the eye must have evolved before the divergence on the evolutionary tree of all animals with eyes. The animal with the ancestral eye must have been the ancestor to the arthropods, chordates, bristle worms and molluscs - animals with eyes today. In which case the eye must have evolved hundreds of millions of years before the Cambrian explosion, when these phyla diverged from each other (albeit remaining within similar, soft bodies). Things, however, did not happen this way.

  There are chordates living in sunlit environments today that have no eyes. They are the most primitive forms of chordate - the type that existed in the Cambrian. I refer to the hagfish, and animals even more primitive. If the most ‘primitive’ chordates did not possess eyes but the more derived chordates did, this means that the first chordate eye evolved at some point within the chordate branch of the evolutionary tree. And now we can justify the lack of chordate eyes in the Cambrian - the eye has a multiple origin. It evolved on more than one occasion - the arthropod eye evolved and the chordate eye evolved, but independently and, it seems, at different points in evolutionary history. When the chordates first branched out from the evolutionary tree they did not have eyes. And the same goes for all other phyla. Now it seems more than possible that an eye appeared on Earth in one phylum before any others - it seems veritable. And that phylum with the first eye was the Arthropoda.

  There is one group of arthropods I have yet to examine, a group well represented in the Burgess Shale. These are the trilobites.

  Earlier in this chapter I casually added trilobites to the list of arthropods with compound eyes. But I did not suggest the exceptional nature of the trilobite. Compound eyes were common in trilobites, which in turn were common in the Cambrian, so it is appropriate to devot
e part of this chapter to trilobite eyes.

  We know that trilobites reigned in abundance throughout the seas. This reign ended 280 million years ago, but began 543 million years ago, at the beginning of the Cambrian explosion. Four thousand species of trilobites have been identified, and they were particularly successful during the first term of their dominion, when they flourished.

  We need not rely on the Burgess Shale and Chengjiang fossils for information about trilobites in the Cambrian. Trilobites are found all over the world and from all periods within the Cambrian - their preservation was not dependent on particularly favourable conditions. And the diversity of Cambrian trilobites suggests they were by far the most important and ubiquitous arthropods around in the Cambrian. In fact trilobites are believed to be the stem group of all arthropods - they probably wore the prototype shells, or ‘exoskeletons’. From some groups of trilobites the crustaceans, and later the insects, evolved. From another group the sea spiders, and later the spiders, evolved.

  The exceptional preservation of trilobites can be attributed to the constituents of their shells - fossilisation-friendly chemicals. And the conservation of their optics allows us a glimpse into their vision - most trilobites had compound eyes.