The evolutionary step from water to land, when fishes evolved into the first four-legged animals or “tetrapods”, was a pivotal event in the history of life. All amphibians, reptiles, birds and mammals, including the human race, can trace their ancestry back to the first tetrapods. We can obtain some clues about how the earliest tetrapods lived from their body form and the environments in which their fossils are preserved, but life history data - information about individual age, growth history, sexual maturity and so forth - have been completely absent until now.

We have used the unique capabilities of beamline ID19 to cast light for the first time on the life history of one of the earliest tetrapods, Acanthostega gunnari, which lived about 360 million years ago. The results caught everyone by surprise.

Almost all fossils of Acanthostega come from a single locality: a sandstone layer, high up on a Greenland mountainside, which represents a dried-up river channel in a tropical inland delta similar to today’s Okavango in Botswana. Dozens of Acanthostega skeletons lie packed together in the sandstone, suggesting that they were caught in the drying channel and perished when the water disappeared. Acanthostega resembles a small crocodile, about 70 cm long, but has a fish-like tail fin and feeble-looking limbs carrying eight toes each (Figure 61).

FIG-061-HL-2016.jpg

Fig. 61: Top: Acanthostega gunnari, from [1]. Scale bar, 100 mm. Middle, humerus UMZC T.1295 showing mineralisation front (mf) with remnants of calcified cartilage (agl). Bottom, humeri MGUH 29019 (left) and MGUH 29020 (right) showing cortical growth rings.

We used propagation phase contrast synchroton microtomography (PPC-SRµCT) with voxel sizes ranging from 20.24 to 0.638 μm to image the four known humeri (upper arm bones) of Acanthostega, focusing especially on the dense outer layer or cortex of the bone (c, Figure 61). This cortex can contain annual growth rings, which record the age of the animal. Traditionally, these have been studied by cutting physical thin sections and viewing them under the microscope. By imaging them using PPC-SRµCT, we were able to avoid damaging the unique fossils and have also revealed three-dimensional features that would not have been visible in thin section.

The humeri of Acanthostega have between two and six evenly spaced growth rings in the cortical bone (black arrows in Figure 61). They also have thin patches of calcified cartilage (agl, Figure 61) on the inside of the cortex, just where it joins the spongy interior bone of the humerus. To understand the importance of these features, we need to consider how a humerus grows. It starts out as cartilage, but then two things happen: cortical bone starts to be deposited on the outside of the cartilage, and the cartilage itself first calcifies and is then broken down and replaced by spongy bone (t, Figure 61). The removal of the calcified cartilage is not quite complete, so little patches of it remain on the inner face of the cortex (agl, Figure 61).

In Acanthostega, the cortex is very thin and the presence of calcified cartilage on the inside shows that it has not been remodelled internally. The cartilaginous humerus must thus have reached almost full size before being covered with bone. The onset of bone deposition was followed by up to six years of slow growth that only added a millimetre or so to the overall size of the humerus. Acanthostega must thus have had a long “childhood”, perhaps spanning a decade or more, during which its limbs were entirely cartilaginous - and thus unsuited to walking on land. The even spacing of the growth rings is an even bigger surprise. In both modern and fossil vertebrates, the onset of sexual maturity is associated with a slowing of growth; this is reflected in the limb bones, where the growth rings become more tightly spaced. This is not yet happening in the Acanthostega humeri, so it looks like all four individuals are juveniles.

The implications are startling. It seems that Acanthostega had a very long aquatic juvenile phase, and that the mass-death deposit captured a shoal of such juveniles. Nobody has ever seen an adult Acanthostega. We don’t know how big they became or where they lived. Our results provide a first precious glimpse into the lives of the earliest tetrapods, but also highlight how little we really know about their world.

 

Principal publication and authors

Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography, S. Sanchez (a,b), P. Tafforeau (b), J.A. Clack (c) and P.E. Ahlberg (a), Nature 537, 408-411 (2016); doi: 10.1038/nature19354.
(a) Science for Life Laboratory and Uppsala University, Evolutionary Biology Centre, Uppsala (Sweden)
(b) ESRF
(c) University Museum of Zoology, Department of Zoology, University of Cambridge (UK)
 

References

[1] P.E. Ahlberg et al., Nature 437, 137-140 (2005).