The Runes of Evolution - Templeton Press · The Runes of Evolution &7 How the Universe Became Self-Aware Simon Conway Morris TEMPLETON PRESS Runes_Book_Final.indb 3 5/12/15 1:38 PM

The Runes of Evolution

Runes_Book_Final.indb 1 5/12/15 1:38 PM


The Runes of Evolution&7

How the Universe Became Self-Aware

Simon Conway Morris

TEMPLETON PRESS


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© 2015 by Simon Conway Morris

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To the memory of my parents



Bernard of Chartres used to compare us to [puny] dwarfs perched on the shoulders of giants. He pointed out that we can see more and farther than our predecessors, not because we have keener vision or greater height, but because we are

lifted up and borne aloft on their gigantic stature.

The Metalogicon of John of Salisbury, Book III [Translated by D.D. McGarry

(University of California Press; 1962) p. 167]



Contents

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . xiii

Introduction. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

1. Dinner on the Lagoon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

2. Consider the Octopus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

3. Convergence: How Clear Is the Signal? . . . . . . . . . . . . . . . . . . . . . . . . . . 21

4. The Inevitability of Form . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 31

5. Swallowing Convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44

6. Biting Convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53

7. Walking (and Swimming) to Convergence . . . . . . . . . . . . . . . . . . . . . . . 67

8. Sticking to Convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82

9. When Evolution Begins to See . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93

10. The Color of Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 108

11. The Smell and Taste of Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 120

12. (In)tangible Evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128

13. The Road to Mushrooms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 150

14. The Road to Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155

15. The Arthropods Show the Way. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165

16. Converging on the Farm. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 177

17. The Road to the Sky . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 189

18. The Birds Converge . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 200

19. Sexual Convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 209

20. The Road to Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 221


x contents

21. The Roots of Sentience . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 234

22. Convergent Brains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241

23. The Road to “King Cortex” . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 252

24. Convergent Minds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263

25. Playing with Convergence . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273

26. The Final Steps . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 286

27. Back to the Lagoon . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 301

Notes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 305

General Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463

Index of Genera . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 489


Illustrations Following page 178

1. Octopus

2. Octopus

3. Sea-hare

4. Bat

5. Dendrobatid frog

6. Puffer fish

7. Bombardier beetle

8. Mantis shrimp

9. Nurse shark

10. Mosasaur

11. Cownose rays

12. Moray eel

13. Myrmecophage

14. Praying mantis

15. Saber-tooth cat

16. Duck-billed platypus

17. Komodo dragon

18. Sea-snake

19. Leaf-cutter

20. Gecko

21. Chameleon

22. Weta

23. Cockroach

24. Tuna

25. Hummingbird

26. Pitcher plant

27. Spider silk

28. Mosquito

29. Brittle star

30. Firefly

31. Hawkmoth

32. Rattlesnake

33. Robber crab

34. Termites

35. Kiwi

36. Dolphin

37. Lichen

38. Rust fungus

39. Cactus

40. Rafflesia

41. Titan arum

42. Dung beetle

43. Ants and aphids

44. Flying fish

45. Flying lemur

46. Hoatzin

47. Vulture

48. Kea

49. Archer

50. Capuchin monkey



Acknowledgments

Like many other things in my life this book needs to start with an apology. Its gen-esis lay in the generous invitation to deliver the 2007 Gifford Lectures at the University of Edinburgh. As this work grew, however, it became clear that it had diverged from my original theme by too great an extent. It is still my firm intention to publish the Gifford lectures and it is incumbent on me to thank the many people in Edinburgh—most espe-cially Wilson Poon, Isabel Roberts and Susan Manning—for this memorable time marked by their many kindnesses. I am in debt to many other people. First is Vivien Brown who has handled manuscript preparation with panache, verve—and patience. Next are the Map of Life team, Chloë Cyrus-Kent and Verena Dietrich-Bischoff as well as the web-designer Francis Rowland who collec-tively not only delivered what I believe is a very effective website (www.mapoflife.com) but drew innumerable facts to my attention. The project was supported generously by the John Templeton Foundation and I warmly thank them for their support. More recently my wits have been sharpened by discussions with Sylvain Gerber, Jen Hoyal-Cuthill, Vic-toria Ling and Mags Pullen. Then there are those who gave their time to read various

sections, especially Rob Asher, Nick Davies, William Foster, Peter Grubb, Chris Howe, David Norman and Nick Strausfield. All offered acute criticisms and by no means agreed with all I said; the faults remain firmly with me. Many others also alerted me to recently published papers, and I especially thank Pablo de Felipe and Ken McNamara. Practically every word written draws on the painstaking work of the “invisible college” and I hope that the research and conclusions drawn by them are dealt with honestly. In places I use short quotations and these fall under the rubric of fair usage. Librarians across Cambridge assisted the chasing of ref-erences and I especially thank Sarah Humbert. Mr R. Garry has also sent me a remarkable range of books and other material. My agent Barbara Levy zealously guarded my interests and offered constant encouragement and sup-port. In addition my brother Roderick kindly provided the translations in the last chapter. Finally I warmly thank my Department and St. John’s College for providing a secure basis where long-term projects can reach some sort of fruition. Finally, as ever, I thank Zoë for her love and forbearance even if the conversation seemed to revolve around the number of bot-tles consumed, ink that is.



The Runes of Evolution



Introduction

Long books demand short introductions. Yes, another book on evolution, but one with a difference. Not to dispute the realities of evolution, or for that matter the primacy of the Darwinian explanation. Neither would it dream of contesting the self- evident obser-vation that we humans are just one endpoint of, to paraphrase the science fiction writer Brian Aldiss, a 3- billion-year evolutionary spree. But here is a book that is prepared to be heterodox, and not before time. So what is it all about?

Even among the mammals, let alone the entire Tree of Life, humans represent one minute twig of a vast (and largely fossilized) arborescence. So, it would be very poor form were we to demand center stage. Nor is that my intention. Every living species is a linear descendant of an immense string of now- vanished ancestors, but evolution itself is the very reverse of linear. Rather it is end-lessly exploratory, probing the vast spaces of biological hyperspace. Indeed this book is a celebration of how our world is (and was) populated by a riot of forms, a coruscating tapestry of life.

But only humans understand this, and so while there is no narrative of human origins, no “Monad to Man,” threaded through this book are some of the staging posts that led from a eukaryotic cell to animals, including fish that clambered onto land, furry reptiles that transformed into mammals, and in one branch evolved into primates, great apes, and

ultimately ourselves. If from unicell to human every generation is taken as a stepping- stone then they would total billions. Even a tally of really key steps as to how the first eukary-ote evolved into the biological form writing these lines would run into the hundreds, if not the thousands. We need to be selective, and while far from imagining this list to be exhaustive, among the most significant might be: multicellularity,1 tissues (including a nervous system), sensory systems (not least vision), limbs (including those that grasp), toolmaking, and intelligence. Others, such as an immune system (notably an adaptive one2), placentas (and even a penis), agricul-ture, and sleep might be less obvious but in one way or another each was biologically seis-mic. All are part of a much longer list that collectively entails becoming human. They have, however, a wider significance. Each of the features just listed is an essential compo-nent in a much broader argument that forms the core of this book. Each and every one of them is either demonstrably convergent or inherent in terms of prior history, that is, drawing on building blocks that have already evolved (and as often as not for a quite sepa-rate purpose).

Of these two concepts, evolutionary con-vergence is the more familiar. It is the other-wise uncontroversial observation that from very different starting points in the Tree of Life very much the same solution has evolved multiple times. Did you know, for example,


4 simon conway morris

that something very like a tapeworm has evolved in a group of protistans known as the dinoflagellates?3 Should we rise to the challenge of Tristam Stayton’s4 question, “Is convergence surprising?”5 Yet his inquiry is rhetorical; simulations employing four sep-arate metrics lead Stayton to conclude that evolution is far from random. The real world tells the same story, as outlined earlier by myself 6 and George McGhee.7

In this book, however, the net been thrown much wider than before, and as a conse-quence a whole series of neglected evolu-tionary questions arise. Some are remarkably general. Why, for example, are convergences such as parasitism, carnivory, and nitrogen fixation in plants8 concentrated in particular taxonomic hot spots? Why do certain groups have a particular propensity to evolve toward particular states? Another chestnut involves what is referred to as “deep homology.” If the underlying genetic mechanisms (such as the famous example of the paired- box gene Pax6 in eyes) are the same in quite different groups, then how can it be legitimate to speak of con-vergence? The reality is rather different and points to some much more interesting prin-ciples. Other questions are more specific but lead to unexpected evolutionary insights. If bees sleep (as they do), do they dream? Why is that insect copulating with an orchid? Why have sponges evolved a system of fiber optics? What do mantis- shrimps and submarines have in common? If mosasaurs had not gone extinct, what would have happened next? Will a saber- toothed cat ever reevolve?

With this blizzard of questions we must trust to Ariadne’s thread as we pace the lab-yrinths of this book. Yet not only is the jour-ney punctuated by regular shafts of light but as importantly the local, even the anecdotal, melds into the general. Like a tapestry one has to stand back to see how the figures and build-ings are set in a wider landscape where the recurrent themes of the narrative reveal the

deeper patterns of evolution. If we are going to start this journey, then where better than in a restaurant and out in the Venetian lagoon? Episodes in the lagoon open and close this book, but at the beginning it is my shadowy colleague Mortimer who, turning from his wine, exclaims “Consider the octopus!” What better starting point? Of course, with its cam-era eyes the octopus is a totem of convergent evolution, but most intriguing are the cogni-tive convergences that, toward the end of this book, open dramatic new territory.

Whatever other significance convergence might have, it is central in the study of evo-lution because it confirms the power of adaptation. Most familiar are the forms of mimicry. Apart from the classic instances of Batesian and Mullerian mimicry, a more mysterious world shadows these famous examples in the form of chemical mimicry, not least those putrid “carrion” flowers with their loathsome scents that some insects find irresistible. And what about the remarkable bolas spider and their whirling balls of sticky silk that intercept moths lured by fake sex-ual signals? Equally striking in the context of convergence are so- called ecomorphs—that is, recurrent body forms that are spawned by similar environmental pressures. Justly cele-brated are the anolid lizards of the Caribbean islands, but perhaps even more startling are ecomorphological convergences between the poison dart frogs of the Neotropics and the mantellid frogs of Madagascar. Is there not, however, a hitch in this argument? Are not some ecomorphs unique? With its percussive skull, sticky tongue, and distinctive stance, the woodpecker is confirmed by both orni-thologists and molecular biologists to have a single—that is, monophyletic—origin. This book insists, however, that we need to take the wider view. Woodpeckers are unique, but “woodpeckeroids,” both among other birds and further afield, most certainly are not. And just as one can invoke woodpeckeroids,


introduction 5

so it is equally legitimate to conjure up “hum-mingbirdoids” with evolutionary analogues like the sphinx moth flickering into conver-gent existence.

Ecomorphs remind us that many conver-gences are most easily explored in terms of functional morphology. Nevertheless, a com-plaint recurs that sometimes the concept of convergence is pushed too far with similari-ties that are really quite superficial. Would we bother, for example, to discuss topics such as nesting or gliding? Yet, even here, there can be subtleties, such as foam nests, and surprises: Who would have predicted a gliding snake? More important, however, are where the apparently superficial similarities conceal a more interesting story. Such skin- deep differ-ences are exemplified in the tuna and lamnid sharks, both fish but, respectively, as a teleost and chondrichthyean not at all closely related. It is hardly rocket science to notice that both are superbly hydrodynamic. But look a little closer: quite independently each has evolved a complex musculotendinous system to pro-vide powerful thrusts to the large tail, but each has also developed a warm- bloodedness that represents a quantum leap in preda-tory effectiveness and range of operation.

We would hope that any ichthyologist would have sufficient command of the area to appreciate not only these skin- deep differ-ences but inquire also whether extinct thun-niform counterparts (think of the Mesozoic pachycormid fish and ichthyosaurs) might provide further insights. Yet, as a whole, taxonomists necessarily specialize: she on cycads, he on ascomycetes, myself on priapu-lids. Inevitably with such focus on a particu-lar group (and as often a lifetime’s dedication of study), the recognition of deeper patterns and commonalities in biology may be frus-trated. Yet the prospect of a more general theory of biology will depend in teasing out what unites form rather than divides it. Who, for example, would have expected that the

manner in which a cockroach (with inciden-tally its convergent milk production) strides across the floor is strikingly similar in terms of the biomechanics to a mammal? So, too, the neural circuits that fire the walking pro-grams are intriguingly convergent. But this example is overshadowed by the extraordi-nary way in which the octopus can transform its arm into a simulacrum of a vertebrate arm. These general rules of operation extend far beyond biology because they are now having a major influence on the design of robots and other biomimetic systems.

Convergence brings into focus a profound tension between the basic rules of organiza-tion, if you like the geometry of life, and the innumerable historical pathways that pale-ontologists in particular revel in discovering. How in other words does history mesh with the immutable realities of the Universe? One hotly debated area is to what extent evolution is any more than a vast exploration of dead ends, biological cul- de- sacs where organisms “run out of things to do.” This question has profound implications for the possible lim-its of biological exploration, but we should never underestimate the versatilities of evo-lution. Consider the bats. Superb fliers (and independently they have evolved echoloca-tion), but notoriously poor walkers and once landed they usually roost. Vampire bats face a problem. They fly to their luckless host, but once perched then how do they get around and choose the best place to slice open the skin and start lapping the blood? Simply by reinventing the capacity to walk and run. Perhaps, however, the most startling exam-ple of reinvention is linked to the capacity of insects to taste and smell. In the same way as vision, these sensory systems employ a canonical protein (opsins and the like) with a diagnostic series of helices (seven in total) that span the cell membrane. Just the same arrangement is found in the insects, except that here it is completely independent. Why



they discarded a perfectly good system and by recruiting a convergent protein reinvented the wheel is less clear. It is, however, powerful evidence that biology travels through history but ends up at much the same destination.

The aim of this book is far wider than simply to show the ubiquity of evolutionary convergence. Such does indeed suggest a metaphorical landscape where the adaptive peaks are very few relative to the immensity of territory that remains permanently inac-cessible, except of course to our imaginations. And here is the nub of the problem. How is it that we have imaginations that can conjure up counterfactual possibilities? More generally, how is it that the Universe became self- aware? Convergence, especially of cognitive systems, shows us that it certainly happens, but in what context?

In this discussion, one stumbling block needs to be dynamited straightaway: the notion that while convergence per se is unre-markable, there still remain key transitions. If, so the argument goes, any of these were frustrated, then this would forever preclude one or another evolutionary adventure. This is not to contest the fact that our under-standing of many of these major transitions is woefully incomplete. Nevertheless, straws in the wind suggest likelihoods of outcome. Consider the eukaryotes. Without them, then no fungi, nor animals, nor plants. Yet we need to take the wider view. First it is increasingly clear that not only are there interesting con-vergences between eukaryotes and bacteria, but significant components of the eukaryotic condition have evolved in bacteria and are available for co- option.9 So, too, key steps—such as the acquisition of chloroplasts from once free- living bacteria—are replicated today, suggesting that, as revolutionary as this step was, it was, by no means inherently improbable.10

The neglected concept of inherency—that is, how waiting in the wings of the evolu-

tionary theater are the players for the next act—reinforces the sense of evolutionary inevitability. Evolutionary co- option and horizontal gene transfer are well enough known. On the other hand, the extent to which the molecular equipment required for a key innovation actually evolved long before it was recruited to its new role is far more pervasive than sometimes is appreci-ated. The proteins that confer transparency to the lens and cornea of animal eyes, the so- called crystallins, represent a classic example of co- option. Be it via the familiar modalities of vision, smell, or tactility to the seemingly alien worlds of infrared perception, echolo-cation, and electrosensation, each and every sensory system is fascinating in many other regards. This is true both in terms of individ-ual convergences and also unexpected com-monalities, such as not only optical foveae but striking tactile, auditory, and electrical analogues. What also emerges is the aston-ishing sensitivity of these (and many other) evolutionary systems. Repeatedly we find a breathtaking precision of operation, be it the operation of the Johnston’s organ (a sort of ear) of the mosquito or the infrared detector of the buprestid fire- beetle. One can make a general argument that in their different ways these sensory systems have effectively reached the limits of the physical universe, at least as far as biology is concerned. Science, of course, opens inaccessible windows of obser-vation to which the universe would otherwise be blind.

Animals not only need to see and smell but among other things also support themselves and transmit instructions. With respect to the former, the protein collagen plays a key structural role. Yet not only is this mole-cule convergent, evolving independently in both fungi and bacteria, but more impor-tantly collagen itself evolved in the group of protistans known as the choanoflagellates.11 Their appearance far predated that of ani-


introduction 7

mals. Choanoflagellates are too small for collagen to have a structural function, and in animals evidently it has been co- opted for its new role. Nestling in these tiny protistans is one component essential to the elephant. More striking still is the case of the nervous system. Unique to animals (although a dual origin is possible) and, more importantly, a significant part of both its genetic basis and molecular machinery (especially with respect to synaptic functions) evolved long before any nervous system materialized. Deep in the history of eukaryotes lies the potentiality for a brain.

Evolutionary inherency is no more sur-prising than convergence, but it does pose unsolved problems as to the versatility of molecular systems. How are they recruited, and, as importantly, how do the various com-ponents build on each other to give systems of increasing complexity? In the history of life, things not only change but they get decidedly more interesting. One might observe, “Once there were bacteria, now there is New York.”12 We need to be careful, however, not to equate “simple” with “primitive.” In fact, however far you go down the Tree of Life, really simple things are pretty elusive. Molecular phyloge-nies allow us to infer with some accuracy what the common ancestor possessed, and in the case, for example, of the earliest eukaryotes they turn out to be “surprisingly” complex. And this is the general rule. So, too, organ-isms of apparent simplicity turn out not only to have been derived from much more com-plex predecessors, but they remain highly sophisticated. Among the most astonishing are minute animals known as dicyemids. They consist of less than a hundred cells, have no real organs, and spend their lives drenched in urine, living as they do on the surface of cephalopod kidneys. Despite their simplic-ity, dicyemids clearly derive from advanced animals. But there is more. First, they are strikingly convergent on a group of pro-

tistans known as the ciliates, specifically the chromodinids, that also infest cephalopod kidneys. Second, long thought to be parasites (another treasure trove for convergence), it is more likely that they contribute to renal func-tion13 and so are a vital ingredient in allowing the cephalopods to transcend their mollus-kan origins and become “honorary fish.”

This honorific status is matched by the cephalopods having remarkably large brains, indicative that independently in these mol-lusks a mind is stirring. For Darwin the mys-tery of mysteries was the origin of species, but for us it is the nature of mind. Conver-gence helps us to stake out the territory. Giant brains and cognitive sophistication have evolved multiple times. Obvious manifesta-tions are learned vocalizations, toolmaking, and social play. Less tangibly, sleep, mirror self- recognition, and even an awareness of death are as much tantalizing as informative. All are patently a product of evolution, and the differences that separate us from apes, crows, dolphins, and maybe even octopus are paper thin. This is what Darwin taught, but now we stand alone. For nearly all biologists this is simply a matter of seamless extrapo-lation. By Darwinian descent this is patently correct, but is it true of mind? Yes, we share the same nervous system, the same types of brain (even if convergent) and a cognitive architecture that confers memory, learning, manipulative skill, and so on. But do our ani-mal counterparts actually understand what they are doing? Their ingenuity, not least in the New Caledonian crow’s toolmaking, is indeed remarkable. Cleverly devised exper-iments, however, are beginning to suggest severe limits to animal intelligence, and when it comes to rationality perhaps they remain in the dark. If this is the case, then maybe ratio-nality is not so much a question of emergence but one of discovery?

The book is a long journey, but at the end we return to a lagoon and a short chapter



of pure speculation. As the Universe has become self- aware, we as one of its products can appreciate its deep beauty. But suppose—and this is by no means a novel idea—mind is not so much self- realized as brains increase in size and complexity but rather the brain

serves as conduit. In this way it encounters the abstract realms of mathematics, music, and language, all of infinite potentiality. Such realms are familiar, but they also hint at the existence of orthogonal worlds. Perhaps our journey has only just begun?


Fig. 1. The octopus is the cynosure of convergent evolution. (pp. 12, 72, 100, 288) [photograph: iStock]

Fig. 2. An octopus? Yes, but pretending to be a sea-snake. Such mimicry is rampantly convergent. (p. 15) [photograph: iStock]

Fig. 3. The sea-hare is apparently vulnerable; however, its protective ink clouds provide an object lesson in convergence. (p. 15) [photograph: iStock]


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The Runes of Evolution - Templeton Press · The Runes of Evolution &7 How the Universe Became Self-Aware Simon Conway Morris TEMPLETON PRESS Runes_Book_Final.indb 3 5/12/15 1:38 PM