Written in Stone: Evolution, the Fossil Record, and Our Place in Nature

by Brian Switek

  When Kulling’s colleague Erik Stensiö examined the fossils he determined that they had come from some hitherto unknown vertebrate, but more fossils would be needed to figure out what it was. As explorations of Greenland continued the Swedish geologists continued to pick up fossils, and in 1931 the leader of that year’s expedition, Gunnar Säve-Söderbergh, found skull fragments from a creature unlike any of the fish common in the Devonian deposits. It appeared to be the earliest tetrapod ever discovered, and Säve-Söderbergh named it Ichthyostega.

  Subsequent forays into the field brought back even more parts of Ichthyostega. Little by little, the body of the tetrapod was pieced together, but before a full description could be carried out Säve-Söderbergh succumbed to tuberculosis in 1948. The analysis of the fossils ground to a halt. Even though the bones of this odd creature had been recovered, its significance to the origins of the first tetrapods was still largely unknown.

  Ichthyostega was too important to be left collecting dust, however, and the responsibility of describing it was passed on to Erik Jarvik, one of Säve-Söderbergh’s assistants who had accompanied him into the field starting in 1932. Jarvik seemed to work at a glacial pace, issuing reports on partial aspects of the skeleton every now and then, leaving the anatomy of Ichthyostega mostly a mystery. There was little that could be done about this. To scoop Jarvik by finding more fossils of the same animal and describing them first would breach the unspoken code of conduct among fossil hunters. The scientific community would have to wait. (A full report on the creature would not be published until 1996.)

  Yet even at an early date it did not appear that Ichthyostega was all that paleontologists had been hoping for. In 1956 Jarvik published skeletal and fleshed-out restorations of what Ichthyostega would have looked like, and in some ways it seemed to be too specialized to be the ancestor of all later tetrapods. It was not so much an intermediate form between fish and amphibians, Romer (among others) thought, as a creature close to the common ancestry of reptiles and amphibians. It represented the oldest skeletal evidence of a tetrapod, finally supplanting the relatively uninformative track that Lull cited, but it already had a neck, shoulders, arms, legs, hands, feet, fingers, and toes. The fossil gap between fish and tetrapod seemed as wide as ever.

  By the 1980s the situation was becoming intolerable. Paleontologists interested in the origin of tetrapods either had to specialize in the array of fleshy-finned fish that came before them or the various amphibious vertebrates that succeeded Ichthyostega. There was nothing in between to study, or at least nothing not already spoken for by other scientists. This presented a substantial problem for the English paleontologist Jenny Clack.

  After struggling to find a niche for herself in academia as an expert on early tetrapods, Clack sought out a new direction in which to take her work. At this point Jarvik was still sitting on Ichthyostega, and a new early tetrapod that would be named Tulerpeton in 1984 was out of reach, as it was being described by Soviet scientists. It seemed like the only hope of finding something new was to go back to Greenland.

  Without a good lead on a new fossil locality, launching an expedition to Greenland was too much of a gamble. Even if the harsh physical conditions could be surmounted Clack was doubtful that the Swedish paleontologists who had worked under Säve-Söderbergh and Jarvik had left anything worth picking up. The old dig sites had likely been cleaned out.

  Clack’s hunt for another fossil locality of the right age and type led her to Cambridge geologist Peter Friend, who had done fieldwork in Greenland during the 1960s and 70s. His team had not been looking for tetrapods, but Clack was hoping that somewhere in the mass of technical papers and field notebooks there would be signs of another tetrapod graveyard. She was in luck. Not only were fossils of tetrapods fairly common in some areas, the field notes said, but one member of the team had brought some fossils back to England. They were sitting in the basement of the Sedgwick Museum, where Friend worked.

  When Clack tracked down the hunk of rock Friend’s team had brought back, she found that it contained three skulls. They were not Ichthyostega. A peculiar pair of horn-shaped projections at the back of the skulls identified them as Acanthostega, a 360-million-year-old early tetrapod that was known only from a few skull fragments Jarvik briefly described in 1952. This was a fantastic find, but Clack needed more complete skeletons, and fortuitously another team of scientists from Denmark were planning on further exploring the area from which the skulls had been exhumed. With the promising prospect of significant fossils still in the field Clack landed a spot on the expedition, and in 1987 she found even more remains of both Acanthostega and Ichthyostega.

  To help her prepare these fossils Clack contacted vertebrate paleontologist Michael Coates, and they began to winnow the fossils out of the rock in 1989. Clack had already seen the complete skulls of Acanthostega , but as she and Coates peeled back the rock over the rest of the skeleton they began to find some very unusual features. The radius and ulna—the two long bones between the wrist and upper arm bone—were of different lengths, with the bone on the “thumb side” of the arm, the radius, being much longer than its neighbor.

  What the scientists found at the end of the arms was even more bizarre. It had long been assumed that the standard number of digits for tetrapods was five, and scientists expected that early tetrapods would either have five digits or would show signs that they had successively added digits until five fingers were formed. As Coates picked away at the hand of Acanthostega he did find five digits, but then he found more. When his work was done, eight fingers could clearly be seen on the hand of Acanthostega.

  Acanthostega was not an aberration. The early tetrapod from Russia, Tulerpeton, had six fingers, and a hindlimb of Ichthyostega Clack had brought back from Greenland had seven toes. Viewed together, the archaic hands and feet of these creatures seemed better suited for propelling them through the water than crawling on land, and five fingers was clearly not the norm among the earliest tetrapods. Now paleontologists not only had to account for how fins were transformed into limbs, but how the polydactyl paddles of Acanthostega and Ichthyostega were transformed into a limb suitable for walking on land.

  The pectoral (“shoulder”) and pelvic (“hip”) fins of the fleshy-finned fish Eusthenopteron formed the foundation of the change. Both pairs of fins were connected to the body by a single bone, the equivalent of the humerus in our arms and femur in our legs, and both sets were linked to each other through embryological development. Some of the earliest fish only had pectoral fins, but during their evolution a duplication event occurred in which genes that regulated the development of the fish created a second pair of fins further down the body. This ancient duplication event meant that these fins had a similar construction and were undergirded by the same genetic instructions.

  FIGURE 21 - The skeletons of Ichthyostega (top) and Acanthostega (bottom). The brackets above the Ichthyostega skeleton denote the different kinds of vertebrae: 1) cervical, 2) thoracic, 3) lumbar, 4) caudal.

  The lower limbs of Eusthenopteron were more complicated. Bones that are homolgous to the radius and ulna in our limbs were present, but they were part of a branching out of bony elements that were surrounded by little rods of bone called lepidotrichia, which supported the margins of the fin. These bones were arranged along what embryologists called the metapterygial axis, a line of growth that runs from the parts of the bones nearest the body and branches out in the portions that are further away. This growth pattern is seen in living lungfish, and it was what gave the fins of fish like Eusthenopteron their distinctive shape.

  The question was where this axis of growth could be drawn in the limbs of early tetrapods. While Eusthenopteron was not directly ancestral to early tetrapods, it was certainly a close relative and therefore useful as a model for the fish ancestors of tetrapods. As such, early tetrapod limbs would have grown along a metapterygial axis, too, but although the axis passed through the humerus (the only bone in the upper arm) its path afterward wa
s unclear. This was an old question, one that anatomists had been debating since the nineteenth century, but the fossil record alone was insufficient to provide the answer.

  The solution was to be found among living descendents of the earliest tetrapods. Despite some relatively minor tweaks, the overall form of the tetrapod limb has been widely conserved among living members of the group. Scientists hoped that by studying the limb development of living organisms they might also find clues as to how the limbs of early tetrapods evolved. This is precisely what paleontologist Neil Shubin and embryologist Pere Alberch did in 1986. What they found was very different from any growth scenario that had been proposed before.

  At the time that Shubin and Alberch published their study it was well known that the limb bones of tetrapods started out as cartilage that condensed from the cells of the embryo. (Only later are the structures transformed into bone through a process called ossification.) This is how the parts of the limb closest to the body, the upper arm and leg bones, form. From there the nascent limb continues to grow and gives rise to the precursors of the lower limb bones (the radius and ulna of the arm, and tibia and fibula of the leg), which are separated from the upper limb bones by a joint.

  Then the pattern of development shifts. The pairs of lower limb bones continue to grow while the radius and tibia split off a few bones of the hand and foot; the ulna and fibula begin to spout off bones arranged in an arc that sweeps across the bones of the wrist or ankle. The bones that are produced in this arc are the fingers and toes. Rather than running straight down the limb through a finger, this pattern revealed that the metapterygial axis became twisted, producing digits starting from the “pinky” side to the thumb/big toe side.21 The ancient genetic and developmental link between the fore- and hindlimbs—the duplication that produced the pelvic fins in fish—meant that both hands and feet grew along these same pathways.

  This pattern was supported by the observed action of Hox genes during limb development. Hox genes are like switches in an organism’s DNA that regulate development and turn cascades of other genes on and off. Their most prominent function is organizing the head-to-tail organization of animal bodies, but there are also Hox genes that regulate the development of fins and limbs. Embryologists have traced the activity of some of these regulatory genes, such as Hoxd-11 and Hoxd-13, during fin and limb development in fish and tetrapods, and they show some surprising differences. In zebrafish, bony fish not very closely related to tetrapods or fleshy-finned fish like Lepidosiren the Hox genes are active along an axis that goes straight down the fin. In tetrapods, however, the same genes are active in the same straight-line pattern until they abruptly whip across the limb bud from the “pinky” side to the “thumb” side, the same metapterygial axis that Subin and Alberch identified as giving rise to digits.

  This twist made sense of why early tetrapods seemed to have extra fingers. During embryonic development there is part of the tetrapod limb bud on what will become the “pinky” side called the Zone of Polarizing Activity, or ZPA for short. This area produces a protein given the whimsical name Sonic Hedgehog, which travels to the edge of the limb bud, where it triggers the release of a hormone that stimulates growth. This hormone, in turn, tells the ZPA to make more Sonic Hedgehog and activates particular Hox genes that guide the development of digits. This developmental cycle produces the digits, from the “pinky” side of the hand or foot first, and the longer it goes on the more digits are produced. If it gets shut off early, fewer digits are formed, meaning that this developmental conveyor belt probably remained active longer in early tetrapods. A little tweak in development produced hands and feet instead of fins.22

  The presence of hands and feet in Acanthostega did not mean that it was a terrestrial animal, however. Contrary to expectations, the overall constellation of features Clack and Coates found in the skeleton of Acanthostega were hallmarks of an aquatic animal. Its flattened skull was attached to its shoulders by way of a very short neck, so there was little space between the lower jaw and the front of the pectoral girdle. In fish, the bones that made up the shoulders were attached to the back of the skull, and while separated in Acanthostega, they were still closely associated. Its limbs were also short and its feet were broad, good for sculling through the water but not as well suited to walking. This was matched by the presence of bones in the tail that would have supported a broad paddle that would have helped propel Acanthostega through the water. As if that were not enough, Acanthostega still retained bony gill arches: it could have drawn oxygen directly from its watery habitat.

  That Acanthostega probably had both gills and lungs is not altogether surprising. The most archaic forms of living bony fish, including lungfish, have both. Though such a dual system might seem unusual to us obligate air-breathers, it is essential to the survival of fish that inhabit waterways in which oxygen can often become depleted. Rather than representing a peculiar advancement toward tetrapods as nineteenth-century naturalists supposed, Lepidosiren and its allies may have more in common with more ancient kinds of fish.

  Even though most bony fish do not have lungs they can breathe with, they do have modified lungs in the form of a swim bladder. Lungs did not evolve from swim bladders but rather the other way round: swim bladders in many familiar fish are a derived specialization that evolved long after the first tetrapods appeared. This suggests that many early fish, including the ancestors of tetrapods, probably had both gills and lungs. Some lineages retained lungs while others modified or lost theirs, but contrary to what we might expect, lungs are actually a very old vertebrate trait. Early tetrapods did not need to evolve lungs anew. They already had them thanks to their ancestry.

  Like Acanthostega, Ichthyostega also had gill arches, lungs, a paddle-shaped tail, and an array of pressure sensors along its body called a “lateral line,” but its skeleton also contained signs that it at least occasionally walked on land. Ichthyostega had a longer neck than Acanthostega , and its shoulders, situated farther back, bore huge shoulderblades that would have provided ample space for the muscles needed to deal with the stresses of terrestrial locomotion. Ichthyostega also had slightly differentiated types of vertebrae along the spine. In fish and earlier tetrapods the vertebrae are almost all identical since the sinuous side-to-side swimming patterns of these aquatic animals did not require much variation, but walking on land put new stresses on these bones. This resulted in modifications of the vertebral column; neck, upper back, lower back, hip, and tail vertebrae all differ in Ichthyostega, just as in our own skeletons.23 Just how it might have moved on land is still unknown, especially since its overlapping ribs would have greatly constrained its movement from side to side, but the details of its anatomy suggest that Ichthyostega was a much more terrestrial animal than its cousin.

  Together both Acanthostega and Ichthyostega showed that many traits thought to mark life on land had evolved in the water first. Tetrapods had not evolved as a result of fish wriggling over baking soil as Lull and Romer had suggested, and geologists realized that the rust-colored rocks in which the first were found did not represent the arid world that Barrell had envisioned. Acanthostega and Ichthyostega lived in shallow, swampy environments that were not under threat of evaporating completely. Fins had evolved into limbs and fingers in these aquatic habitats; rather than being a consequence of moving on land they were a preexisting condition for it.

  The tetrapod story had suddenly been altered, and the discovery of the complete skeletons of these tetrapods prompted paleontologists to scour museum collections to see if there were any more hiding in forgotten cabinets. These searches turned up the fragmentary remains of early creatures like Elginerpeton, Ventastega, and other members of an early radiation of tetrapods. But old problems still remained. There was still nothing between Eusthenopteron and the earliest known tetrapods to document how fins were transformed into limbs. Anatomy and embryology confirmed that it must have happened, but there was still a gap in the fossil record.

  As before, long-negl
ected fossil specimens would play an important role in fleshing out early tetrapod history. Despite being named in 1942, the fleshy-finned fish Panderichthys had for decades only been known from fragments. It did not seem to hold much relevance to the questions surrounding early tetrapods, and even when a partial skeleton of the fish was dug out of a quarry in Latvia in 1972 it languished in storage, undescribed, for years. As paleontologists with an eye for early tetrapods dove back into old collections in search of new material, however, Pandericthys stood out.

  FIGURE 22 - A comparison of the forelimbs of Eusthenopteron, Panderichthys, Tiktaalik, and Acanthostega. Abbreviations: H, humerus; Int, intermedium; R, radius; U, ulna; Ure, ulnare. Scale bar, 1 cm.

  Though classified as a fish, Panderichthys very closely resembled early tetrapods. From nose to tail it had a flattened body well suited to life in the shallows, and its fins were reminiscent of those in the earliest known tetrapods. It was not a terrestrial animal, but its limbs would have allowed it to push its upper body off the bottom to gulp air from the surface.

  But Panderichthys was soon overshadowed by another creature. During the 1990s Neil Shubin, the paleontologist who had teamed up with Pere Alberch to explain the development of the tetrapod limb, was studying the Devonian-age rocks of Pennsylvania with his student Ted Daeschler. Together they helped to describe the fragmentary remains of a new tetrapod found in those rocks they called Hynerpeton, but it was nowhere near as complete as the Acanthostega fossils Clack had dug out of Greenland. Looking for early tetrapods in Pennsylvania was difficult business. Most of the deposits of the right age and type were covered by soil or sat under suburban developments, rendering them inaccessible. The few available deposits had been exposed as a result of department of transportation crews blasting through hills to clear the way for roads, often destroying fossils in the process. Even though the Pennsylvania sites had potential, getting anything out of them was a massive headache. Shubin and Daeschler resolved to look elsewhere.