In The Blink Of An Eye

by Andrew Parker

  To uncover the real cause of the Cambrian explosion all the pieces of the puzzle are needed. After introducing the problem in Chapter 1, the following seven chapters of this book will be dedicated to the more significant pieces. In the course of these chapters a multidimensional picture will be painted showing how life works today, what happened during the course of evolution on Earth and, consequently, how life worked at different times in the geological past. Having been warned that the more technical terms I adopt the smaller my audience will be, I have responded by keeping scientific names and terminology to a minimum. I have tried to use, or even invent, common names of animals wherever possible, and must apologise if this method appears too simplistic or distracting. Nonetheless, the most important, recurring scientific terms have necessarily survived the editorial process.

  By the beginning of the penultimate chapter, all the clues needed to solve the why of the Cambrian explosion will have been presented. Scientific evidence will be extracted not just from biology, but also geology, physics, chemistry, history and art. Subjects such as eyes, colour, fossils, predators, Egyptian statues, the deep sea and coral reefs will be entertained. What was the significance of Maxwell’s breakfast or of Newton’s peacock to our understanding of evolution? Might they be on a par with Charles Doolittle Walcott’s monumental discovery of the Cambrian ‘Burgess Shale’ fossils themselves? I feel that the Cambrian explosion is something worthy of anyone’s time, and that the explanation of this event is worthwhile publicising. I hope readers will agree.

  My road to the Cambrian was possible only because of some wonderful opportunities presented to me, for which I am extremely grateful. In the first place there were Penny Berents and Pat Hutchings, who offered me my first position at the Australian Museum in Sydney. Here I was lucky enough to spend several years examining living and preserved specimens from every major animal group on Earth - an experience which contrasted greatly with my days studying animal diversity from a textbook as an undergraduate. Then there were Jim Lowry and Noel Tait, at the Australian Museum and Macquarie University (Sydney) respectively, who registered my research for a Ph.D. degree, and taught me so much about animal diversity, ecology and evolution. But I also received considerable help and encouragement from many more members of the Australian Museum than I have space to list here. I am grateful to them all.

  By now I had chosen to study seed-shrimps as my specialist subject, and received expert tuition from Lou Kornicker at the Smithsonian Institution (Washington, DC) and Anne Cohen (Los Angeles County Museum of Natural History). Their kindness and patience were important to my early career. But, as will be revealed in this book, seed-shrimps led me into a very unexpected and different subject - classical optics.

  Michael Land (Sussex University), Sir Eric Denton (Marine Biological Association of the UK, Plymouth) and Peter Herring (Southampton Oceanography Centre) in England had produced some inspiring work on optics and colour in animals. It was great to join in their subject, and I thank them for all the help they gave me, and for tolerating my strange enquiries. After training in the subject of animal structural colours I was ready to bother the optical physicists, particularly Ross McPhedran and David McKenzie (following a significant introduction by their colleague, Maryanne Large) at Sydney University (although many others gave considerable time to my cause). Thanks to these physicists I quickly became familiar with an otherwise unfamiliar subject from its beginnings. And I have found the application of optics to nature quite fascinating.

  Looking forwards, sideways, or who knows which direction, I caught a glimpse of the Cambrian. I was steered around the subject of Cambrian biology by numerous palaeontologists. In particular I am grateful to Greg Edgecombe (Australian Museum), Simon Conway Morris (Cambridge University) and the late Stephen Jay Gould (Harvard University) for thought-provoking discussions and comments on my work, and Des Collins (Royal Ontario Museum, Toronto, Canada) for the trip of a lifetime to the famed ‘Burgess Shale’ quarry in the Canadian Rockies.

  Many of the above people supported my move to Oxford University, and I thank Marian Dawkins and Paul Harvey for making that possible. And then there is the small matter of funding, without which my research would never have begun. This commenced with research grants from the Australian Museum, Macquarie University and the Smithsonian Institution. Then came more substantial funding (for three-year projects) from the Australian Biological Research Study to examine seed-shrimp diversity, and from the Australian Research Council to investigate structural colours in animals. Today I am fortunate to hold a Royal Society University Research Fellowship, which frees maximum time for research. That has been a huge help, but has been gratefully topped up with grants from the Engineering and Physical Sciences Research Council and the Natural Environment Research Council in the UK. Also I am thankful to Somerville College, Oxford, for making me a Research Fellow as supported by the Ernest Cook Research Fund.

  Outside my research career, I have people to thank for their necessary help with this book specifically. Cathy Kennedy, of the Oxford University Press, taught me the trade of writing for an audience beyond that of my academic peers, and must have been horrified by my first attempts - after strict scientific conditioning, the popularisation of science is not easy! Peter Robinson of the Curtis Brown literary agency in London helped to refine my technique. But it was the editors I worked with, particularly Andrew Gordon in the UK (and Amanda Cook in the US), who after struggling through early drafts of half-science-half-popular-science, finally transformed my ideas into something readable. And I thank Jeremy Day of Day & Co., London, and the American scientist Ronald Watts for sparking Chapter 10, which may not have happened without their stimulating discussions and interest in my Cambrian ideas.

  Finally I thank my parents, other members of my family and a close friend for their continual encouragement and support of my research career.

  1

  Evolution’s Big Bang

  The explosive evolution during the Cambrian . . . one of the most enigmatic episodes in the history of life

  DEREK BRIGGS, DOUGLAS ERWIN AND

  FREDERICK COLLIER (1994)

  The ‘Cambrian explosion’ . . . a pivotal moment in the history of life

  STEPHEN JAY GOULD, Wonderful Life (1989)

  Why was there a radiation in the Cambrian? Our most sincere answer is that we do not know

  JAN BERGSTRÖM (1993)

  Life as we know it

  I have a clear memory of animal diversity classes as an undergraduate. Each week I would open my vintage textbook at a different chapter to find a meaningless black and white line drawing of a representative from a new animal group, blending naturally into its background of page creases, ink blots and previous students’ scribbles. All in all, the illustrations were hardly more exciting than the thick, blotted stamps of the antediluvian typewriter. They bore no relation to living creatures, nor could one separate the extinct from the living.

  A few years later I lowered my head under water in anticipatory awe of one of the world’s natural wonders. All I saw was a dark brown cloud. I had come too close to a cuttlefish for its liking. But as the ink disappeared I adapted to the blaze of colours that strike the eye from every direction. The vast diversity of life forms quickly became apparent in the shallow waters of Australia’s Great Barrier Reef. Following my student experiences, I was wholly unprepared for my second introduction to animal diversity. The antlers, domes, fans, brains and pipes of corals were the first to manifest themselves. Polyps, each only a few millimetres across, are the living parts of corals which stretch out their tentacles to feed at night, appearing like small anemones or even upside-down jellyfish. Their hard, supporting limestone structures stretch for over a thousand miles, forming the foundations of this famous reef that is visible even from the moon.

  Regardless of their external appearance and lifestyles, corals, anemones and jellyfish actually belong to the same higher classification of animals, known as a phylum (plural phyla) becau
se they share the same internal body plan. That is, the organisation of their internal parts - the nutrient processing factories and oxygen transport systems - is similar. Back in the Great Barrier Reef, the complete spectrum of colours present among the corals was paralleled by an almost complete anthology of animal phyla. So began a journey into the unknown. The coral skeleton of the reef was decked out with gardens of sponges, which matched the corals in their diversity of shapes and colours. The sponges provided shelter within their water-filled passageways for animals belonging to other phyla. These lodgers include the bristle worms - a common group of animals that make up a phylum with earthworms and leeches. Some display shimmering opalescent or iridescent colours, like the bizarre-looking sea mouse, a worm whose appearance is best described as a hedgehog with the iridescence of a compact disc.

  Sea gooseberries look like transparent variants of their fruit name-sakes, flashing with eight iridescent bands. These alien-like blobs of jelly have an internal body plan like no other group of animals and so belong to a phylum of their own - the comb jellies. Starfish are not only obvious during the day but some glow at night with their bioluminescence, emerging from darkness like an extraterrestrial visitor. Starfish are related to common sea urchins and belong to the same phylum of animals. Giant clams display fluorescent blues, greens and purples.

  Figure 1.1 The division of life into categories of different levels, using the woodlouse Porcellio scaber as an example. There are thirty-eight phyla of multicelled animals.

  They belong to the mollusc phylum along with another animal rather more infamous for its colour - the blue-ringed octopus. During aggressive spells, the blue rings of this small octopus light up to warn of its deadly venom. The less familiar ‘moss animals’ live in colonies often with unusual shapes and colours, sometimes appearing like the mosses or lichens found on terrestrial rocks. Worms are ubiquitous but hide a plethora of phyla, such as the ‘ribbons’, ‘peanuts’, ‘arrows’, ‘acorns’ and flatworms. Ribbon worms, as their name suggests, are ribbon-like in appearance and seem quite placid until they make their presence known with their powerful jaws. Peanut worms are less dangerous and have a swollen rear end. Its similarity to a peanut is questionable, but a brownish colour is the norm. The acorn analogy is even less convincing, although arrow worms are more appropriately named. Similarly, the flatworms are flat, and some of those capable of swimming by undulating their bodies possess colours that can shock.

  Although very few insects are found in the sea, the crustacean representatives from the arthropod phylum are often at their most spectacular on the Great Barrier Reef, and include the crabs, lobsters and shrimps. Another phylum that is best known for its terrestrial members is the Chordata. This name may sound familiar because it is the group containing amphibians, reptiles, birds and mammals, including humans. But the fishes of the reef, along with some lesser known animals such as sea squirts and lancelets, also belong to this phylum and were once its only members.

  Before leaving the water I found, in precisely the same place, the ink culprit, with about thirty of its comrades. The cuttlefish from the mollusc phylum formed an exact arc around me, tentacles to face, eye to eye. Their brown bodies instantaneously bleached as I moved towards them and they all retreated by precisely the same distance. Then their bodies displayed a wave of colour changes. Brown and white synchronised undulations rapidly flowed along the length of their bodies, then suddenly a ‘loud’ red cut into the sequence, followed by a calming green as I retreated. Meanwhile, the regions housing their eyes remained silver, like mirrors.

  Understanding the variety of life

  The cuttlefish eye shows strong similarities to the human eye. This is an example of the evolutionary biologists’ red herring - convergence. From similar basic building materials a comparable organ has evolved independently to achieve the same function, in two different phyla. But we have learnt it is the internal organisation of an animal that defines its phylum, not its external appearance. As we saw with the worms, the worm-like shape is shared by a number of phyla, but these are unrelated because their internal constructions are very different. If a worm has a mouth but no anus it belongs to the flatworm phylum. Acorn worms are blessed not only with an anus but also a brain and, of importance, a pharynx (the front end of the gut). We also possess an anus, brain and pharynx, but not the body shape of a worm. Now we can divide the body of any animal into two parts - the innards and the outer layers (the ‘skin’ and ‘shells’).

  The job of an evolutionary biologist is to make sense of the conflicting diversity of form - there is not always a relationship between internal and external parts. Early in the history of the subject, it became obvious that internal organisations were generally more important to the higher classification of animals than are external shapes. The internal organisation puts general restrictions on how an animal can exchange gases, obtain nutrients and reproduce. So we are more closely related to acorn worms than to flatworms. Also, acorn worms are more closely related to us than to flatworms. The complexity of an individual’s development from embryo to adult mirrors the sophistication of internal organisation of the adult. To construct an animal with a complex but specific internal organisation from a collection of just a few cells, a specific method of development is required. As one can envisage, from a few cells more steps are required to form a human baby with all its internal complexity than a simple jellyfish - an infolded ball of three tissue layers. Now we can examine the reason why internal organisations carry so much weight in animal classification. It is worth taking the time to understand this subject since it forms the backbone of evolution.

  The internal organisations, methods of development from embryo to adult and external shapes of animals are governed by their genes, the set of instructions carried by the chromosomes within the cells. Copious genes govern internal organisation and development. In contrast, the external shape of an animal is generally under the control of considerably fewer genes. But what governs the genes themselves? First we need to take another look at convergence - similarities in external shapes between animals with different internal organisations.

  By external parts of animals I refer to the materials, colours and shapes of the outer layers. These have a closer association with the environment than do internal organisations. The environment includes physical factors, such as temperature and light conditions, and biological factors, such as the animal neighbours. The external parts of an animal, in particular, must be adapted to its specific environment, and they may do so within broad limits set by the internal body plan. If two animals live in the same type of environment, they may share comparable external parts, regardless of their internal organisations. This is possible because the external parts are controlled by a relatively small number of genes, and the chances of those genes mutating to code for the same structures in different species are not remote. If we roll two dice, the chances of both landing on a six are 36 to 1. Even though many more than two genetic mutations will be involved in the evolution of external body parts, single mutations can be retained and accumulated. Consequently if a lamp shell and a razor shell, which belong to different phyla, live on the same type of sand into which they burrow, but also require protection from the same predators, it is not surprising that they share a similar external shape - possibly an optimal design. But their internal organisations remain very different. Internal organisations are under the control of many more genes, which all have to mutate at the same time to initiate a new internal body plan. Unlike external architectures, internal body plans cannot be built up gradually because usually they can’t function in intermediate stages. This is a monumental difference between the mechanisms that control internal body plans and external parts. A spine on the outside of an animal can begin as a small bump, then pass through intermediate stages from a large bump to a long, pointed spine. Importantly, all intermediate stages can exist in their own right because they provide some advantage for their host. But for a change in body plan tha
t involves the abrupt appearance of blood space, or a sudden flipping upside-down of everything internal, for example, there can be no intermediate stages. Internal body plans cannot be constructed stepwise, and so are less influenced by the environment. Hence convergence of internal body plans does not occur. If we roll a thousand dice, the chances of them all landing on a six are 1,000,000,000,000,000,000 to 1 - extremely improbable.

  Charles Darwin and Alfred Russel Wallace were first to realise that evolution, an ever-branching process, is the mechanism responsible for animal diversity. Because modifications in the physical and biological environments are taking place continuously, species must also change continuously to maintain an optimal design (or as near as possible to it). This is adaptation. So a modification in the environment can be thought of as a pressure on the local animals to change. Hence the term ‘selection pressure’ was introduced.

  A minor selection pressure may result in a slight modification in a local animal. An animal walking on the sea floor may develop slightly broader feet to prevent it from sinking if the sand or mud becomes softer. A weighty selection pressure may result in a considerable modification in a local animal. The introduction of a new food source may lead to the evolution of new mouthparts and limbs for movement. A collection of modifications in a population can lead to a new species, all within a single phylum. The fewer the modifications between species, the closer their evolutionary relationship or branching point on the evolutionary tree. Here I have been talking about external characters only. Animal phyla today have unique internal organisations, and a mixture of unique and shared (convergent) external characters. But did their internal organisations evolve in tandem with their characteristic shapes? And when did these both evolve? These questions lead us to the major evolutionary problem that this book will attempt to solve. They will be asked again a little later in this chapter when, after an exploration of the history of life on Earth, they will be easier to digest.