The Runes of Evolution
How the Universe Became Self-Aware
By Simon Conway Morris
Templeton Press Copyright © 2015 Simon Conway Morris
All rights reserved.
Dinner on the Lagoon
Mortimer had taken me to the best restaurant he knew, and we were not disappointed. The food was a sensation, a visual triumph, appetizing aromas and exquisitely balanced flavors: eyes, noses, and taste buds all jostled for attention. Beyond the quay the lagoon shimmered, with vast thunder-heads illuminated by the setting sun. We had much to discuss and would only just catch the last vaporetto. "Do you recall that lecture by Gould? How insistent he was that evolution had no directionality, how the history of life veered erratically and unpredictably, clobbered by catastrophe after catastrophe, supereruption followed by cometary impact. To think evolution was like either physics or chemistry, that it is with a deep structure, real predictabilities, was absurd. Rerun the tape of life, as ironically he repeated so often, and the outcome will be entirely different. Humans? Yet another accident of evolution, as interesting in their own way as a tapeworm, or, if you prefer, a tulip. Of course, it was perfectly clear that, like any scientist, Gould had based his stance on deep, if hardly articulated, metaphysical roots. His worldview made no sense unless humans were utter flukes of circumstance. Only then could we construct the world as we wished it to be, rather than as it actually is." Mortimer emptied his wineglass, and then grinned. "Now we know that he was gloriously wrong, and indeed the evidence stares us in the face."
Mortimer gestured at the rim of his wineglass. Just visible were a couple of fruit flies, a stock-in-trade for molecular biologists (where they are just "fly" or Drosophila). Finding them hovering around the wine was scarcely surprising. In the wild they seek out fruit, which of course soon rots and, by fermenting, so dinner for the fruit fly is laced with alcohol. As he explained, Mortimer filled both glasses, emptied the bottle, and signaled to the waiter. "Tricky stuff, alcohol," and taking an appreciative sip continued, "and highly poisonous. Pity the fruit fly; yes it, too, becomes inebriated, and not surprisingly the device biologists use is the inebractometer. No, no, I am not joking. Well, you see the fascinating thing is, if you study how the flies get drunk — sorry? Oh yes, you see how fast their little legs are moving, well, would you believe it but their behavior is remarkably similar to the way we get drunk? Wonderful example of evolutionary convergence, and you can hardly be surprised if the genes for alcoholism in a fruit fly have names like barfly, not to mention cheapdate and amnesiac.
"Sounds trivial, but it isn't. Think about it. How different biology appears to be from either physics or chemistry. Where are the grand principles, the major laws, the equivalent of the periodic table or the theory of general relativity? Of course, there is evolution, but that doesn't predict anything! Just as Gould claimed was the case: everything a fluke. But that story of the fruit flies getting intoxicated is just one example of convergence. It looks like Douglas Adams was right. Remember that episode in The Hitchhiker's Guide to the Galaxy where jynna-tonnyx turns out to be the galactic-wide refreshment? And what's true for alcoholism, and for all we know gin and tonic, applies across biology: from enzymes to penis, from insecticide resistance to toolmaking and technology, from love darts to music, everywhere you look evolution is hedged in by convergence. By no means everything is possible; in fact nearly everything is impossible.
"At last I do believe we might be on the threshold of a general theory for biology. The implications are" — and here Mortimer paused and looked at the first stars that had begun to shine above the lagoon — "well, I think they might be rather considerable. After all, what is it about life? I'm no vitalist, but you can't help being amazed by the intricacies of that tiny chemical factory we call the cell. Why, it far outstrips even our most advanced nanotechnology. And then think of the way the embryo develops — not only the wonderful way in which it unfolds, but how robust it is against insult and injury. Polanyi was quite right: Life is much more than just a sort of souped-up chemistry and physics. And there is so much to play for: I have a hunch that convergence could even give us some new clues on that mystery of mysteries: what consciousness is, but if anybody thinks mind is entirely material they are barking up the wrong tree. And aren't these conclusions positively cosmic? When I look at the night sky then like Pascal those infinities terrify me. Where on earth are they? You know — the extraterrestrials! Fermi was on to something, and now we know about convergence we really can predict what these extraterrestrials will look like, and as importantly how they'll think. Physicists know that the elements they see in the farthest reaches of the Universe are exactly the same as on Earth. So if life is universal, which incidentally might not be quite as secure an assumption as is usually thought, and the roads of evolution are indeed narrow and inevitable, then the differences between us and an alien will be trivial. But as I said: Where on earth are they? Is life just a fluke? Could there be something very peculiar about the Earth? Whichever way you look at it, something doesn't add up. ..."
In the silence the next dish was served. "Splendid," remarked Mortimer. "What better example of convergence? Consider the octopus."
Consider the Octopus
The octopus has a remarkable hold on our imaginations. It is certainly no accident that in The War of the Worlds H.G. Wells peopled (if that is the word) the sinister tripods that stalked across a terrified and panic-struck England with octopoidlike occupants. Although best-known as a consummate writer, Wells was more than biologically literate, having not only studied under the great Thomas Henry Huxley but literally aped him. Moreover, as Peter Kemp reminds us, Wells had long been fascinated in the octopus, with their apparently inhuman and groping tentacles (but see below), not to mention a weakness for human flesh. Nor is this fascination simply the purlieu of gifted novelists, however competent they might be in biology. Ian Gleadall and Nadav Shashar echoed this in their nice review on octopus vision when they wrote, "Cephalopods are among the most exotic and alien life forms imaginable."
Yet for all its alien attributes, in reality the octopus shows many remarkable similarities with the vertebrates, even though in terms of the animal kingdom the evolutionary gap could scarcely be wider. But as Andrew Packard remarks, "ours is a functional and democratic age: no longer is genealogy of primary importance. And cephalopods functionally are fish. "Vertebrates, which include fish and such descendants as the mammals (and thereby us), are closely related to the starfish (and the other echinoderms). The octopus (and other cephalopods such as the squid and cuttlefish), however, are close cousins of the oyster (and other mollusks). This evolutionary gulf means that the many similarities we see between the octopus and vertebrate have clearly been arrived at independently. There are two reasons for thinking this must be correct. First, the common ancestor lived about 550 million years ago and may have approximated a sluglike beast. In any event, what this remote form could not possibly have possessed are the many complex features that the two groups now share. Second, while the convergences are indeed very striking, in each case there is a clear "footprint" that clearly points to a completely separate evolutionary trail.
In many ways cephalopods like the squid can be justly labeled "honorary fish." The similarities are certainly not exact (convergence never claims they are), and in such features as locomotion, respiration, and digestion the squid clearly takes second place. Nevertheless, they remain immensely successful and in the deep oceans arguably outclass the fish. Ingeniously in this environment they store the waste product ammonia, which, having a low density, imparts buoyancy. A nice trick, and one that in this group has evolved independently several times. Nor is this the only way cephalopods can achieve neutral buoyancy. In fish the standard method is to employ the swim-bladder, but just such a structure has evolved independently in the octopus, specifically the deepsea Alloposus and the females of Ocythoe. In the latter case, why not their companions? Presumably because they occur as dwarf males. Not surprisingly, therefore, investigators have been repeatedly struck by not only the versatility of the cephalopod body plan, but the way they have pushed it to some quite extraordinary limits. This is true, for example, of their circulatory system and even more so in terms of nervous development. So far as the latter is concerned, cephalopods now stand on the threshold of new worlds: stirring in their nervous system is a mind.
The Gaze of the Mollusk
Look at the octopus, and it looks back. In both cases the eye is built somewhat like a camera. Indeed this independent evolution of the camera eye is rightly celebrated as one striking example of convergence. In fact, as we will see (p. 106), the camera eye has evolved independently at least six more times. Evidently it is an excellent arrangement — one might say design (but with no implication of so-called intelligent design). By definition the lens must be transparent, which this is achieved by using proteins that, in the context, are appropriately known as crystallins. They are a compelling example of molecular convergence, so it is quite unsurprising to learn that both octopus and vertebrate have equally transparent lenses and have crystallins that function in exactly the same way, but in reality the crystallins in either group have completely different evolutionary origins (p. 93).
Typically the lens in cephalopods and vertebrates is spherical, but this presents a special problem when it comes to how the light travels through it. As is well known, when light moves from one medium to another, usually the path it must take is slightly bent. Lower a perfectly straight stick into water, and it will appear bent (the degree of bending being determined by what is called the refractive index). In the case of a lens this is potentially very serious because if the bending of the light is not properly corrected, the image will not be precisely focused on the retina. The result: A blurred image and potential disaster for the octopus. The solution to this problem is for the octopus to progressively change the refractive index from the center to the edge of the lens so as to correct precisely the spherical aberration. This degree of correction is very close to the ideal a physicist would employ. So, too, it is almost identical to what we see in the equivalent vertebrate, in this case the example chosen being a fish (trout) as it is also aquatic. Not only are the camera eyes convergent, but so is the correction for spherical aberration. This refractive correction is, of course, molecular, but not only is it based on remarkably high concentrations of the crystallin proteins but specific amino acid substitutions that find intriguing parallels between vertebrate and cephalopod. Now in one way all this is entirely predictable: after all, if the lens cannot focus properly it is pretty useless. Nevertheless, it is a reminder that, as often as not, convergences are far from superficial; not only are they subtle, but they suggest the constraints are far from being accidental. Rather they point to universal principles.
So far as the camera eyes of octopus and vertebrate are concerned, the convergences extend far beyond the overall anatomy, employment of crystallins, and correction for spherical aberration. Rather, the roster of similarities extends to the cornea, pupil, the so-called extraocular muscles (responsible for rotating the eyeball), as well as details of the retina. Striking as this checklist of convergences might be, evolutionary convergence neither means the structure is identical nor that all the solutions discovered are optimally equivalent. Thus, the many correspondences between the octopus and vertebrate eye should not allow us to overlook that in various respects the retina of the latter is more sophisticated and is involved with signal processing in a way not found in any cephalopod. But is the cephalopod really so disadvantaged? Recall first that it has the more "sensible" arrangement of the retina being uppermost, unlike the vertebrates, where in principle (p. 97) the light has to travel through a layer of cells before it impinges on the retina. Nobody doubts their acuity of vision, and in some squid it can rival that of humans. Less surprising, therefore, is to see that the outer cortex (or deep retina) of the cephalopod optic lobe, which is juxtaposed to the eye and connected of course by the optic nerves, is convergent with the vertebrate retina. In extending his study to the optic lobe of a squid, J. Z. Young remarked how his analysis brought "out further remarkable similarities between the pattern of organization of the visual system in cephalopods and vertebrates. The general resemblance between the retina profunda and the vertebrate retina is obvious enough, but similarity extends even into details." As Binyamin Hochner notes, this "similarity [is] all the more striking as the octopus's typically invertebrate mechanisms of transduction and physiological responses to light are quite different from those of vertebrates." Recalling also that the vertebrate retina is an outgrowth of the brain — and so in terms of evolutionary ancestry is crucially different from the mode of origination of the cephalopod retina, which is formed by the infolding of the skin — in the final analysis the proclaimed differences in the modes of visual processing in fact are achieving the same result by different routes.
Getting a Grip
If squid are "honorary fish," then we would expect them to be highly effective swimmers. And so they are, but unlike the fish, which wave a tube of muscle from side to side, cephalopods employ a form of jet propulsion. Although this system is inherently less efficient (not least in the employment of a cumbersome respiratory protein known as haemocyanin) and makes extraordinary respiratory demands, there is a striking analogy in fish and squid between those muscles used for sudden bursts of speed as against normal cruising. Not only is it likely that in the squid this arrangement has evolved independently several times, but the similarity extends to the cellular level. The reason is that the corresponding two types of muscle fiber found in fish that exhibit markedly different oxidative metabolisms find a direct counterpart in the squid. Effectively, therefore, we find an equivalent to the white and red muscles in fish, which in turn reveals an extraordinary story of convergence when we come to look at the tuna (pp. 78–80). Of course, muscle needs to be enclosed in an integument, a skin. Mollusks they may be, but once again we find that the cephalopods have departed from such close relatives as the bivalves and snails, because now they have evolved an integument much more similar to that of the vertebrates.
So, "honorary fish" they remain, but if their apparent alienness appears to have somewhat receded, what about those famous tentaclelike arms? I put down my fountain pen, my friend lifts her book. In either case at its simplest a set of rods articulate via a series of joints. With its flexible tentacles with effectively unlimited freedom of movement it is difficult to imagine anything much more dissimilar — until, that is, we look at the octopus more closely, using a high-speed camera. Then, rather extraordinarily, the tentacles turn out to be far more like our arms than might have been expected. The tentacle is transformed into an arm! To be sure there are no fingers as the food is grasped by the highly tactile suckers. What happens, however, is that waves of muscular contraction roll along the arm, and when they collide form a pseudo-joint. The net result is a quasi-arm, defined by three segments, with most of the rotation taking place at the "elbow." The position of the articulatory "joints" are not precisely fixed, but interestingly the proportion between the lengths of the two main segments usually remains remarkably constant. Germán Sumbre and his colleagues take pains to note that this striking functional convergence may at first sight be surprising but it actually suggests that when evolution needs an arm, then there really is an "optimal design." That's the way the world works. Moreover, although each of the eight arms is effectively identical (apart from those octopus with an add-on penis [p. 425n59]), the octopus evidently knows the difference because particular arms appear to be chosen to undertake specific tasks. But if the arms of the octopus are less alien than imagined, surely the suckers of the arms — traditionally clamped to the face of the doomed diver — have no useful counterpart elsewhere? In one sense this is correct, but in many ways they are a sort of analogue of the elephant's trunk and its versatility (p. 131). In fact, the octopus suckers have multiple functions, ranging from display to locomotion. But of these, perhaps the most extraordinary is the way an individual sucker can fold into two halves and, acting like a mittened hand, is quite capable of grasping a strand of fishing line. Not only that, but as Jennifer Mather also notes, the manipulative ability of arms extends to being able to "untie knots in the finest surgical silk." (Continues...)
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