Lobefins today have dwindled to the lungfishes and the coelacanths (‘dwindled’ as ‘fish’, that is, but mightily expanded on land: we land vertebrates are aberrant lungfish). They are ‘lobefins’ because their fins are like legs rather than the ray fins of familiar fishes. Indeed, Old Fourlegs was the title of a popular book on coelacanths written by J. L. B. Smith, the South African biologist most responsible for bringing them to the world’s attention after the first live one was dramatically discovered in 1938 in the catch of a South African trawler: ‘I would not have been more surprised if I had seen a dinosaur walking down the street.’ Coelacanths had been known before, as fossils, but they had been thought extinct since the time of the dinosaurs. Smith movingly wrote of the moment when he first cast eyes on this astonishing find, to which he had been summoned by its discoverer, Margaret Latimer (he later named it Latimeria), to give his expert opinion:
We went straight to the Museum. Miss Latimer was out for the moment, the caretaker ushered us into the inner room and there was the – Coelacanth, yes, God! Although I had come prepared, that first sight hit me like a white-hot blast and made me feel shaky and queer, my body tingled. I stood as if stricken to stone. Yes, there was not a shadow of doubt, scale by scale, bone by bone, fin by fin, it was a true Coelacanth. It could have been one of those creatures of 200 million years ago come alive again. I forgot everything else and just looked and looked, and then almost fearfully went close up and touched and stroked, while my wife watched in silence. Miss Latimer came in and greeted us warmly. It was only then that speech came back, the exact words I have forgotten, but it was to tell them that it was true, it was really true, it was unquestionably a Coelacanth. Not even I could doubt any more.
Coelacanths are closer cousins to us than they are to most fish. They have changed somewhat since the time of our shared ancestor, but not enough to be moved out of the category of animals that, colloquially and to a fisherman, would be classified as fish. But they, and lungfish, are definitely closer cousins to us than to trout, tuna and the majority of fish. Coelacanths and lungfish are examples of ‘living fossils’.
Nevertheless, we are not descended from lungfish, or from coelacanths. We share an ancestor with lungfish, which looked more like a lungfish than it looked like us. But it didn’t look much like either. Lungfish may be living fossils, but they are still not very like our ancestors. In the quest for those, we must instead seek real fossils in the rocks. And in particular we are interested in fossils from the Devonian era that capture the transition between water-dwelling fish and the first vertebrates to live on land. Even among real fossils, we would be too optimistic if we hoped literally to find our ancestors. We can, however, hope to find cousins of our ancestors that are sufficiently close to tell us approximately what they were like.
One of the most famous gaps in the fossil record – conspicuous enough to have been given a name, ‘Romer’s Gap’ (A. S. Romer was a famous American palaeontologist), stretches from about 360 million years ago, at the end of the Devonian period, to about 340 million years ago, in the early part of the Carboniferous, the ‘Coal Measures’. After Romer’s Gap, we find unequivocal amphibians crawling through the swamps, a rich radiation of salamander-like animals, some of them as large as crocodiles, which they superficially resembled. It seems to have been an age of giants, for there were dragonflies with a wing span as long as my arm, the largest insects that ever lived.* Starting about 340 million years ago, we might almost call the Carboniferous the amphibian equivalent of the age of dinosaurs. Before that, however, was Romer’s Gap. And before his gap, Romer could see only fish, lobe-finned fish, living in water. Where were the intermediates, and what led them to venture out on to the land?
My undergraduate imagination at Oxford was fired by the lectures of the prodigiously knowledgeable Harold Pusey who, despite his dry and prolonged delivery, had a gift for seeing beyond dry bones to the flesh-and-blood animals that had to make a living in some departed world.* His evocation of what drove some lobe-finned fish to develop lungs and legs, which was derived from Romer himself, made memorable sense to my student ears, and it still makes sense to me even though it is less fashionable among modern palaeontologists than it was in Romer’s time. Romer, and Pusey, envisaged annual droughts during which lakes and ponds and streams dried up, only to flood again the following year. Fishes that made their living in water could benefit from a temporary ability to survive on land, while they dragged themselves from a shallow lake or pond that was threatened with imminent desiccation to a deeper one in which they could survive until the next wet season. On this view, our ancestors didn’t so much emerge on to the dry land as use the dry land as a temporary bridge to escape back into the water. Many modern animals do the same.
Rather unfortunately, Romer introduced his theory with a preamble whose purpose was to show that the Devonian era was a time of drought. Consequently, when more recent evidence undermined this assumption, it seemed to undermine the whole Romer theory. He’d have done better to omit the preamble, which was, in any case, overkill. As I argued in The Ancestor’s Tale, the theory still works, even if the Devonian was less drought-ridden than Romer originally thought.
Let us, in any case, return to the fossils themselves. They trickle sparsely through the late Devonian, the period immediately preceding the Carboniferous: tantalizing traces of ‘missing links’, animals that went some way towards bridging the gap between the lobe-finned fishes that were so abundant in Devonian seas, and the amphibians that later slithered through the Carboniferous swamps. On the fish side of the gap, Eusthenopteron was discovered in 1881 in a collection of fossils from Canada. It seems to have been a surface-hunting fish and probably didn’t ever come on land, notwithstanding some early imaginative reconstructions. Nevertheless, it did have several anatomical similarities to the amphibians of 50 million years later, including its skull bones, its teeth and, above all, its fins. Although they were probably used for swimming and not walking, the bones followed the typical pattern of a tetrapod (the name given to all land vertebrates). In the forelimb, a single humerus was joined to two bones, the radius and ulna, joined to lots of little bones, which we tetrapods would call carpals, metacarpals and fingers. And the hind limb shows a similar tetrapod-like pattern.
Then, near the amphibian side of the gap, some 20 million years later, at the border between the Devonian and Carboniferous, great excitement was caused by the 1932 discovery in Greenland of Ichthyostega. Don’t be misled by thoughts of cold and ice, by the way. Greenland in the days of Ichthyostega was on the equator. Ichthyostega was first reconstructed by the Swedish palaeontologist Erik Jarvik in 1955, and again he portrayed it as closer to a land-dweller than modern experts do. The most recent reconstruction, by Per Ahlberg at Jarvik’s old university of Uppsala, places Ichthyostega mostly in the water, although it probably made occasional forays on to the land. Nevertheless, it looked more like a giant salamander than a fish, and it had the flat head that is so characteristic of amphibians. Unlike all modern tetrapods, which have five fingers and toes (at least in the embryo, although they may lose some in the adult), Ichthyostega had seven toes. It seems that the early tetrapods enjoyed more freedom to ‘experiment’ with varying numbers of digits than we have today. Presumably at some point the embryological processes fixed upon five, and a step was taken that was hard to reverse. Although, admittedly, not as hard as all that. There are individual cats, and indeed humans, who have six toes. These extra toes probably arise through a duplication error in embryology.
Eusthenopteron
Ichthyostega
Another exciting discovery, also from tropical Greenland and also dating from the boundary between the Devonian and the Carboniferous, was Acanthostega. Acanthostega, too, had a flat, amphibian skull and tetrapod-like limbs; but it too departed, and even further than Ichthyostega, from what we now think of as the fivefinger standard. It had eight digits. The scientists most responsible for our knowledge of it, Jenny Clack and Mich
ael Coates of Cambridge University, believe that, like Ichthyostega, Acanthostega was largely a water-dweller, but it had lungs and its limbs strongly suggest that it could cope with land as well as water if it had to. Again, it looked pretty much like a giant salamander. Moving back now to the fish side of the divide, Panderichthys, also from the late Devonian, is also slightly more amphibian-like, and slightly less fish-like, than Eusthenopteron. But if you saw it you would surely want to call it a fish rather than a salamander.
Acanthostega
Panderichthys
So, we are left with a gap between Panderichthys, the amphibian-like fish, and Acanthostega, the fish-like amphibian. Where is the ‘missing link’ between them? A team of scientists from the University of Pennsylvania, including Neil Shubin and Edward Daeschler, set out to find it. Shubin made their quest the basis for a delightful series of reflections on human evolution in his book Your Inner Fish. They deliberately thought about where might be the best place to look, and carefully chose a rocky area of exactly the right late Devonian age in the Canadian Arctic. There they went – and struck zoological gold. Tiktaalik! A name never to be forgotten. It comes from an Inuit word for a large freshwater fish. As for the specific name, roseae, let me tell a cautionary tale against myself. When I first heard the name, and saw photographs like the one reproduced on colour page 10, my mind immediately leapt to the Devonian, the ‘Old Red Sandstone’, the colour of the eponymous county of Devon, the colour of Petra (‘A rose-red city, half as old as time’). Alas, I was quite wrong. The photograph exaggerates the rosy glow. The name was chosen in honour of a benefactor who helped finance the expedition to the Arctic Devonian. I was privileged to be shown Tiktaalik roseae by Dr Daeschler when I had lunch with him in Philadelphia, shortly after its discovery, and the lifelong zoologist in me – or perhaps my inner fish – was moved to speechlessness. Through rose-tinted spectacles I imagined I was gazing upon the face of my direct ancestor. Unrealistic as that was, this not-so-rose-red fossil was probably as close as I was going to get to meeting a real dead ancestor half as old as time.
If you were to meet a real live Tiktaalik, snout to snout, you might start back as if threatened by a crocodile, for that is what its face resembled. A crocodile’s head on a salamander’s trunk, attached to a fish’s rear end and tail. Unlike any fish, Tiktaalik had a neck. It could turn its head. In almost every particular, Tiktaalik is the perfect missing link – perfect, because it almost exactly splits the difference between fish and amphibian, and perfect because it is missing no longer. We have the fossil. You can see it, touch it, try to appreciate the age of it – and fail.
I MUST GO DOWN TO THE SEA AGAIN *
The move from water to land launched a major redesign of every aspect of life, from breathing to reproduction: it was a great trek through biological space. Nevertheless, with what seems almost wanton perversity, a good number of thoroughgoing land animals later turned around, abandoned their hard-earned terrestrial retooling, and trooped back into the water again. Seals and sea lions have only gone part-way back. They show us what the intermediates might have been like, on the way to extreme cases such as whales and dugongs. Whales (including the small whales we call dolphins), and dugongs with their close cousins the manatees, ceased to be land creatures altogether and reverted to the full marine habits of their remote ancestors. They don’t even come ashore to breed. They do, however, still breathe air, having never developed anything equivalent to the gills of their earlier marine progenitors. Other animals that have returned from land to water, at least some of the time, are pond snails, water spiders, water beetles, crocodiles, otters, sea snakes, water shrews, Galapagos flightless cormorants, Galapagos marine iguanas, yapoks (aquatic marsupials from South America), platypuses, penguins and turtles.
Whales were long an enigma, but recently our knowledge of whale evolution has become rather rich. Molecular genetic evidence (see Chapter 10 for the nature of this kind of evidence) shows that the closest living cousins of whales are hippos, then pigs, then ruminants. Even more surprisingly, the molecular evidence shows that hippos are more closely related to whales than they are to the cloven-hoofed animals (such as pigs and ruminants) which look much more like them. This is another example of the mismatch that can sometimes arise between closeness of cousinship and degree of physical resemblance. We noted it above in connection with fish that are closer cousins to us than they are to other fish. In that case, the anomaly arose because our lineage left the water for the land, and consequently surged away in evolution, leaving our close fish cousins, the lungfish and coelacanths, resembling our more distant fish cousins because they all stayed in the water. Now we meet the same phenomenon again, but in reverse. Hippos stayed, at least partly, on land, and so still resemble their more distant land-dwelling cousins, the ruminants, while their closer cousins, the whales, took off into the sea and changed so drastically that their affinities with hippos escaped all biologists except molecular geneticists. As when their remote fishy ancestors originally went in the other direction, it was a bit like taking off into space, or at least like launching a balloon, as the ancestors of whales floated free of the constraining burden of gravity and severed their moorings to dry land.
At the same time, the once rather scanty fossil record of whale evolution has been convincingly filled out, mostly by a new trove from Pakistan. However, the story of fossil whales has been so well treated in other recent books, for example Donald Prothero’s Evolution: What the Fossils Say and Why it Matters, and, more recently, Jerry Coyne’s Why Evolution is True, that I have decided not to cover the same details here. Instead, I have confined myself to one diagram (below), taken from Prothero’s book, showing a sequence of fossils ordered in time. Note the careful way the picture is drawn. It is tempting – and older books used to do this – to draw sequences of fossils with arrows from older to younger ones. But nobody can say, for example, that Ambulocetus was descended from Pakicetus. Or that Basilosaurus was descended from Rodhocetus. Instead, the diagram follows the more cautious policy of suggesting that, for example, whales are descended from a contemporary cousin of Ambulocetus which was probably rather like Ambulocetus (and might even have been Ambulocetus). The fossils shown are representative of various stages of whale evolution. The gradual disappearance of the hind limbs, the transformation of the front limbs from walking legs to swimming fins, and the flattening of the tail into flukes, are among the changes that emerged in elegant cascade.
Fossil whales
Figure 14.16. Evolution of whales from land creatures, showing the numerous transitional fossils now documented from the Eocene beds of Africa and Pakistan. (Drawing by Carl Buell)
That’s all I’m going to say about the fossil history of whales, because it has been so well treated in the books I mentioned. The other, less numerous and diverse but just as thoroughly aquatic group of marine mammals, the sirenians – dugongs and manatees – are not so well documented in the fossil record, but one outstandingly beautiful ‘missing link’ has recently been discovered. Roughly contemporary with Ambulocetus, the Eocene ‘walking whale’, is Pezosiren, the ‘walking manatee’ fossil from Jamaica. It looks pretty much like a manatee or dugong, except that it has proper walking legs both front and rear, where they have flippers in the front and no limbs at all in the rear. The picture opposite shows a modern dugong skeleton above, Pezosiren below.
Just as whales are related to hippos, so sirenians are related to elephants, as a great deal of evidence, including the all-important molecular evidence, attests. Pezosiren, however, probably lived like a hippo, spending much of its time in water and using its legs to walk on the bottom as well as swim. The skull is unmistakably sirenian. Pezosiren may or may not be the actual ancestor of modern manatees and dugongs, but it is certainly excellent casting for the role.
This book was about to go to the printer when exciting news came in, from the journal Nature, of a new fossil from the Canadian Arctic, plugging a gap in the ancestry of modern seals,
sea lions and walruses (collectively ‘pinnipeds’). A single skeleton, about 65 per cent complete, Puijila darwini dates from the early Miocene epoch (about 20 million years ago). That’s recent enough that the map of the world was almost the same as today. So this early seal/sea lion (they had not diverged yet) was an Arctic animal, a denizen of cold water. Evidence suggests that it lived and fished in fresh water (like most otters except the famous sea otters of California), rather than in the sea (like most modern seals except the famous Lake Baikal seal). Puijila did not have flippers, but webbed feet. It probably ran like a dog on land (very unlike a modern pinniped) but spent much of its time in water, where it swam like a dog, unlike either of the two styles adopted respectively by modern seals and sea lions. Puijila neatly straddles the gap between land and water in the ancestry of pinnipeds. It is yet another delightful addition to our growing list of ‘links’ that are no longer missing.
Modern dugong
Pezosiren – ancient dugong
I now want to turn to another group of animals that returned from the land to the water: a particularly intriguing example because some of them later reversed the process and returned to the land a second time! Sea turtles are, in one important respect, less fully given back to the water than whales or dugongs, for they still lay their eggs on beaches. Like all vertebrate returners to the water, turtles haven’t given up breathing air, but in this department some of them go one better than whales. These turtles extract additional oxygen from the water through a pair of chambers at their rear end that are richly supplied with blood vessels. One Australian river turtle, indeed, gets the majority of its oxygen by breathing (as an Australian would not hesitate to say) through its arse.