Eusthenopteron belongs to a family called the tristichopterids, though it is not the most primitive member of this family. Thus, it is necessary to check whether any feature cited as representing the transition was really present in more primitive members, or whether Eusthenopteron has developed it in parallel with tetrapods. This is a general principle when trying to work out evolutionary transitions.
Eusthenopteron grew up to a meter long. Its fin skeleton, with a substantial humerus, radius, and ulna as well as other robust skeletal elements, has provided the baseline from which to evolve a limb. It has been known since the early twentieth century, when it provided the basis for many transformation scenarios.
A feature shared by most fishes is the bone called the hyomandibula that supports the palate and controls movements of the gill apparatus. It is a long bone that pivots on the walls of the bone housing the brain and ear capsules, the braincase, and it has attachment points to the gill bars and the opercular series, the plate-like bones that cover and protect the gills. They are all part of the pumping mechanism used in breathing and feeding. Eusthenopteron was entirely typical of early fish in this respect.
In 1938, parts of the skull of a fossil fish were found in the same deposits as Eusthenopteron. Although only known from a partial skull roof, its proportions seemed more like those of a tetrapod than a fish (Westoll 1938). It was named Elpistostege, and it remained a tantalizing and intriguing puzzle for many decades, even though additional material in the 1980s added more information and corroborated Westoll’s view (Schultze and Arsenault 1985). Elpistostege is now recognized as closely related to the next two players in the story.
More recently, two such fish have been increasingly under the spotlight as being more closely related to tetrapods and having more transitional characters. The first is called Panderichthys, and though it has been known from reasonably complete specimens since the 1970s, many of its key features are only just being described. It comes from the Late Devonian of the Baltic states and Russia, and it is approximately contemporary with Eusthenopteron, even possibly a little earlier. It grew to well over a meter in length (Figs. 1 and 6). Its tetrapod-like features include loss of all its midline fins—dorsal and anal—a flatter skull, a much longer snout, and larger and more dorsally place eye sockets than Eusthenopteron (Vorobyeva and Schultze 1991). Its humerus and shoulder girdle are relatively larger and show more tetrapod-like morphology than those of Eusthenopteron, for example in having larger areas for muscle attachment (Vorobyeva 1995, 2000). Recently, it has been shown that its spiracular cleft is larger than that in Eusthenopteron and approaches that of an early tetrapod in size and shape. The spiracle may have been open to the outside, a feature that has been associated with air breathing. The ossified portion of the hyomandibula is much shorter than in Eusthenopteron, although it still contacted the opercular bones (Brazeau and Ahlberg 2006). Based on the interpretation of computed tomography scans of a relatively uncrushed specimen, it has been further shown that its fin skeleton possesses the most tetrapod-like features of any fish (Boisvert et al. 2008; Figs. 1 and 6).
In the last couple of years, a second, in some ways even more tetrapod-like fish, has been discovered. This is Tiktaalik, from the Late Devonian of Canada. A joint team from the Universities of Chicago and Harvard and the Academy of Natural Sciences in Pennsylvania targeted a locality on Ellesmere Island in northern Canada because a geological survey showed rocks of the right age and environmental setting to yield fossils representing the fish–tetrapod transition. For several years, they found nothing much, but eventually their predictions paid off and their efforts were rewarded with magnificent specimens of a new tetrapod-like fish (Daeschler et al. 2006; Figs. 1 and 7).
Tiktaalik is known from several almost complete specimens, preserved in three dimensions. It shows many typical fish-like features such as scales, in its case bony and rhomboidal in shape. Its head, which grew to over 300 millimeters long, shows some similar features to Panderichthys, but is even more tetrapod-like: It has an even longer snout and even larger eyes. Furthermore, the shoulder girdle appears not to contact the back of the head as it does in fish including Panderichthys. In some ways, it is even more similar to Elpistostege. Crucially, however, because of its excellent preservation, some key features were shown. In other fish, including Eusthenopteron and Panderichthys, as well as the opercular bones that cover the gill region, another series joins the head to the shoulder girdle. In Tiktaalik, the operculars and some of the shoulder series were no longer present. The hyomandibula is shorter again than in Panderichthys, suggesting the onset of changes to the gill region and to the fish’s breathing mechanism compared with conventional fish. Detachment of the head from the shoulder girdle implied that the head was more mobile and could have been raised and lowered further and more easily than in other fish. On top of the head, the opening to the spiracular chamber is broad and rounded (Daeschler et al. 2006).
One important aspect of Tiktaalik’s fin structure is that because of the excellent preservation, the bones of the fin skeleton could be removed from the surrounding rock and actually manipulated against one another to investigate their range of movement. The team describing this movement suggested that it showed a joint construction that foreshadowed that of a tetrapod wrist and that it could be used in support of the front end of the body. Whether this was done with the body in or out of water is not certain, but it would certainly be reckoned as a forerunner of a supportive limb (Shubin et al. 2006). Supporting the notion that Tiktaalik was raising the front end of the body, it has broad overlapping ribs running down the length of the trunk to form a strengthening “corset.” At the same time, the paired fins of Tiktaalik still retain fin rays: Loss of fin rays is part of the way in which limbs are distinguished from fins. By that criterion, Tiktaalik is still a fish: It has fins as well as scales, but its overall construction helps to blur the conventional boundary between “fish” and “tetrapod.”
Tiktaalik, Panderichthys, and Eusthenopteron show very similar construction in the lower jaw and in the arrangement of teeth in those jaws, suggesting that they fed in similar ways (Daeschler et al. 2006). It turns out that early tetrapods can be recognized because they show new features of the dentition and jaw construction, so that tetrapods can be identified just from their lower jaws (Ahlberg and Clack 1998). The implication is that tetrapods had begun to diverge away from a fish-like feeding technique. Since they also differ between taxa, they had begun to diversify into different niches.
One of the first tetrapod fossils to be recognized in this way was Elginerpeton, first identified from some fragments of skull and lower jaw in the University Museum in Oxford. The elements come from Scat Craig, near Elgin in Scotland and date from the early part of the Late Devonian (Ahlberg 1991). As well as jaw fragments, the fossils include tetrapod-like girdle elements. Thus, Elginerpeton is the earliest animal known to have had limbs. They also indicate the existence of a rather large animal (Fig. 1), as the skull is considered to be about 400 millimeters long (Ahlberg 1995, 1998).
Another Devonian tetrapod first recognized from a lower jaw is Ventastega. Initially interpreted as belonging to a panderichthyid, it was eventually recognized as a tetrapod on the basis of lower jaw and girdle material collected by Russian and Lativan paleontologists. Further expeditions to the site have yielded spectacular material. This site, from the late part of the Late Devonian, is on a river bank, and the fossils occur in almost unconsolidated sand. They require little excavation, though the bones need to be consolidated with resins before they can be studied (Ahlberg et al. 1994).
Remains from this site now include, in addition to many lower jaws, an almost complete skull, along with some shoulder and hip girdle elements that closely resemble those of another Devonian tetrapod, Acanthostega (see below; Figs. 1 and 8). From this, it is inferred that Ventastega had limbs with digits. The skull of Ventastega falls in appearance almost exactly intermediate between Tiktaalik and Acanthostega: The differences are largely those of proportion. It has relatively larger eyes and a longer snout, and the portion of the skull behind the eye sockets is relatively shorter than in Tiktaalik. In the region of the snout in which fish such as Eusthenopteron and Panderichthys have a mosaic of small bones, Ventastega actually has a gap running along the midline of the skull, suggesting that this might be a stage in losing that mosaic. However, the opening of the spiracular cleft and some details of the back of the skull are virtually identical between Ventastega and Tiktaalik. Ventastega also shows a mixture of fish-like and tetrapod-like characters in the braincase. Some of the most profound changes that took place during the fish–tetrapod transition affected this region of skull anatomy (Ahlberg et al. 2008).
The differences between fish such as Eusthenopteron and Panderichthys and tetrapods such as Acanthostega in the bones of the braincase and ear region have been considered as representing a sudden and complex change as compared with those to the skull, which have been seen as gradual. Although the braincase changes may be have been relatively rapid, information from Ventastega tends to suggest that they nevertheless took place by a series of small changes, rather than one extreme change (Ahlberg et al. 2008).
It was the discovery and description of Acanthostega in the 1990s that really initiated the revival of studies and thinking about the fish–tetrapod transition. It came from the same localities as Ichthyostega in Greenland, and the two were contemporary. However, renewed collecting in Greenland in 1987 found almost complete skeletons of Acanthostega that changed perceptions of what a Devonian tetrapod was like (Figs. 1 and 9). Acanthostega was preserved in hard rock, and the fossil bones had to be dug out very slowly and carefully in a process that took several years to complete. This done, whereas Ichthyostega had proved somewhat of an anomaly, Acanthostega proved to be more or less exactly what an early tetrapod “ought” to be like. It retained a number of fish-like features, but was nevertheless a tetrapod by the definition of having limbs with digits.
The fish-like features of Acanthostega include a tail fin supported by long bony rays, to make an oar shape. Fin rays had been found in the tail of Ichthyostega, but they were much shorter and less numerous. The ribs of Acanthostega are short and slender and much the same all down the length of its body (Coates 1996; Fig. 1). Ichthyostega was known to have had broad overlapping ribs at least in its trunk region. In the skull, Acanthostega has a slot running down the midline of the snout, similar to the gap found there in Ventastega (Clack 2003). Acanthostega also retains a set of well-ossified grooved gill bars, suggesting that these were still actively involved in gill breathing, though it probably breathed air by gulping as well (Coates and Clack 1991).
In other respects, Acanthostega showed some typical tetrapod features. It has a robust pelvic girdle and a large femur. It is the pelvic region and the hind limb that most conspicuously distinguish a fish from a tetrapod, and that distinction is still valid among modern animals. In fish, the pelvic girdle is usually small and not attached to the vertebral column and the pelvic fin is diminutive, whereas in tetrapods, the pelvic girdle is large, attached to the vertebral column and bears the substantial hind limbs that provide most of the propulsive power in walking. In Acanthostega, although the pelvic girdle is enlarged, it is still relatively small compared with later tetrapods and was only attached to the column by soft tissue rather than a bony junction (Coates 1996).
The humerus bears close comparison with those of Panderichthys and Tiktaalik, and most of the muscle attachment points and other features can be recognized as similar between them. In that of Acanthostega, however, they are much further elaborated, suggesting larger and more differentiated musculature. The radius and ulna as well as the tibia and fibula attach at the extreme ends of their respective humerus and femur. Combined with the more or less horizontal orientation of the forearm, this suggests that the elbow and knee joints were relatively weak and did not form an effective supporting limb, at least not for walking on land. That arrangement fits with other information about the limbs that constitutes the most unexpected aspect of Acanthostega (Coates 1996).
Some excellent specimens showed that it had eight digits on the forearm (Figs. 5 and 9) and almost certainly eight (or maybe more) on the hind limb. That they are so neatly laid out in the fossil may be because they were enveloped in a web of skin. The wrist bones were not ossified, but it is clear that the digits were arranged in a broad arc around where those bones would have been, but the result would not have made a flexible or supportive wrist. The limb was in effect a paddle (Coates and Clack 1990). Similarly, although the ankle bones are well ossified, they do not show an obvious joint surface along which the limb could bend. Again, the limb seems to have been a paddle. From that evidence, it was suggested that limbs with digits first evolved not for walking on land but for swimming or wading through water (Coates and Clack 1995).
In the braincase and ear region, Acanthostega showed features in which it was distinctively more tetrapod-like than fish-like. In tetrapods, rather than a hyomandibula pivoting on the braincase wall, essentially the same bone but now termed the stapes, fits into a hole in the braincase wall called the fenestra vestibuli or fenestra ovalis. Acanthostega shows this pattern in a very early form (Clack 1989, 1994). The arrangement later became modified into the combination of a stapes and a fenestra ovalis that is characteristic of all tetrapods and is still part of the hearing mechanism in humans.
If Acanthostega is a mixture of fish-like and tetrapod-like characters, Ichthyostega is a mixture of apparently aquatic specializations with others that appear more modified for land excursions. Recent study has revealed a rather different animal from the old image of an overlarge salamander-like body form.
One of the parts of the anatomy that had puzzled earlier workers was the ear region. Using newly collected and prepared fossil material, together with microcomputed tomography scanning of key fossils, the unique arrangement found in Ichthyostega has been interpreted as a highly specialized underwater auditory organ (Clack et al. 2003). By contrast, work on its postcranial skeleton has suggested that it may have had a unique form of locomotion on land. The vertebral column is differentiated into separate regions, including a lumbar portion that seems to have accommodated dorsoventral flexion (Ahlberg et al. 2005). The shoulder girdle and forearm are large and robust, suggesting extensive musculature, perhaps for pulling the animal along on land. Its hind limb is quite similar in construction to that of Acanthostega, that is to say a paddle with no obvious ankle joint, and it has seven toes arranged in a unique pattern (Coates and Clack 1990). A group of three small toes form a strengthening bar along the leading edge, with four stouter ones behind (Figs. 1 and 3). It is likely that, as in Acanthostega, these were contained in a web of skin. The hind limb may have given stability and purchase on the substrate and been used as a flipper in water, but it was not a conventional walking leg. It is no surprise that this peculiar morphology caused problems for early workers trying to understand Devonian tetrapods. It shows that even by that time, tetrapods had diversified into a wider range of morphologies than was previously appreciated.
Analysis of all the skull specimens of Ichthyostega has shown changes to proportions and skull bone ornamentation that varies throughout its history and that document microevolution at the specific level in these very early tetrapods. Skulls from lower formations are narrower, with finer ornament, than those from higher up in the geological sequence (Blom 2005).
Two other localities have yielded Devonian tetrapod remains that consist of more than lower jaw fragments and give evidence of further diversity and geographical distribution. The third Devonian tetrapod to be identified, in the mid-1980s, came from Russia. It consists of a partially articulated skeleton and is called Tulerpeton (Lebedev 1984). The limbs are well preserved and show long bones that are more slender and more like those of later tetrapods than either Acanthostega or Ichthyostega, suggesting at first sight a more terrestrial animal. However, Tulerpeton has six toes on the forelimb (Fig. 5) and almost certainly six on the hind; its wrist and ankle bones are not easily comparable with those of later tetrapods; and it was found in the environmental setting of a shallow marine sea (Lebedev and Clack 1993; Lebedev and Coates 1995). This was the first hint that the earliest tetrapods were not necessarily purely freshwater animals and that they did not have the conventional number of five toes. Both conclusions, surprising at the time, have been confirmed since by other finds.
A road cut near Hyner in Pennsylvania, called Red Hill, has given us a number of Late Devonian tetrapod elements. The environment it shows was a river flood plain with a monsoonal climate, and the site has yielded a great variety of plants, invertebrates, and fish, as well as tetrapods (Cressler 2006). The best-known tetrapods are two different lower jaws and two similar partial shoulder girdles (Daeschler 2000; Daeschler et al. 1994). The shoulder girdles show some similar features to those of Acanthostega but suggest that the animal had a greater muscle mass. There is also an unusual isolated humerus that almost certainly does not belong to the shoulder girdles (Shubin et al. 2004). The jaws show that there were at least two kinds of tetrapod there, but further isolated bones have since been identified that imply the existence of three or four. One of these is a single bone from the snout of a tetrapod, the lacrimal bone. Intriguingly, it resembles that of a later tetrapod, Pederpes, from the Early Carboniferous of Scotland (Daeschler et al. 2008).
The transition to fully terrestrial tetrapods did not end in the Devonian. It was a gradual process that continued into the Early Carboniferous, though the fossil record of post-Devonian tetrapods is notoriously sparse for about 30 million years after the Devonian/Carboniferous boundary. Pederpes is one of the few fossil animals known from that period (Clack 2002b; Clack and Finney 2005) (Figs. 1 and 10). This animal, belonging to a group known as the whatcheeriids, not only shows some primitive features in which it resembles the Devonian forms but also has more advanced features that suggest the beginnings of terrestriality. Its hind limb was fairly typical of a conventional tetrapod from the Late Carboniferous and appears to have had five digits. The foot appears to have pointed forward as in a terrestrially walking animal, rather than to the side as in Acanthostega. However, the forelimb may have had more than five digits, because the only two that are known are both extremely small and resemble the supernumeraries of Acanthostega and Ichthyostega. Pederpes has broad flanges on its ribs that resemble those of Ichthyostega in some ways. Its stapes is like that of Acanthostega.
The first indisputably fully terrestrial tetrapod known in the fossil record is Casineria from the Early Carboniferous of Scotland. It has a fully pentadactyl forelimb with a hand capable of flexing and with claw-like terminal elements and gracile limb bones (Paton et al. 1999; Fig. 11). This makes the point that the origin of tetrapods is not the same thing as the origin of terrestriality and walking.