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Evolution

Teenage tetrapods

Bone analysis of aquatic tetrapods from around the time when these four-limbed vertebrates began to move onto land reveals that the large specimens were only juveniles, raising questions about how these animals developed. See Letter p.408

One of the most fascinating topics in vertebrate evolution is the transition of finned fish to four-limbed tetrapods. This transition involved changes to many aspects of the biology of our fish ancestors, including their respiration, waste removal and skeletal system1. The evolution of the limb, which eventually led to our own arms and legs, was a prerequisite for tetrapods' conquest of the land and ability to evolve the amazing variety of body forms and means of locomotion observed in both extinct and modern vertebrates. Given the pivotal role of this move onto land, the anatomical transformations involved have been a major focus of research, not only in palaeontological studies, but also in studies of evolutionary developmental biology and the relationship between anatomical structures and their function2,3. A paper on page 408 by Sanchez et al.4 reveals insights into growth patterns of the early tetrapod Acanthostega. Their results will provide a deeper understanding of the development and evolution of our four-legged forerunners.

Although many advances have been made in understanding the evolutionary transition from fish to tetrapod, a key piece of the puzzle has remained elusive — how did the earliest tetrapods grow? The process by which an organism develops from the fertilized egg to the adult form (known as ontogeny) reveals details about the evolution and biology of a species that cannot be made by studying adult individuals alone. Series of fossils that chart the development of later tetrapods from larvae to adults5 have provided a wealth of developmental data. However, the ontogenetic development of the earliest tetrapods has been poorly understood because such information is rare in the fossil record, and juvenile and adolescent stages had not been identified.

Sanchez and colleagues' study animal, Acanthostega, is one of the earliest known tetrapods, and lived about 365 million years ago during the Devonian period. The authors used synchrotron microtomography, a non-destructive way to generate 3D structural representations of the microstructure of fossil bone, and studied the long upper bone of Acanthostega's forelimb, the humerus. Bone is a dynamic tissue, and studying its microstructure can reveal unique information about the physiology, growth and life history of vertebrates, because the internal structures provide indications of how fast an animal grew, how old an individual was and when growth ceased. Sanchez et al. investigated Acanthostega samples from a fossil assemblage site in which the individuals had all died together, probably in a drought following a catastrophic flood event. Although only a few humeri were available, they provide a glimpse into the growth patterns of this transitional species.

In tetrapods, the humerus initially forms as a cartilage precursor, with bone material being subsequently deposited in a process known as ossification. Surprisingly, Sanchez and colleagues' imaging data indicate that all of the specimens they investigated were still in the juvenile growth phase and had not reached sexual maturity. Even more surprisingly, Acanthostega seemingly reached almost its final size while retaining a cartilaginous humerus during an early-juvenile period that lasted several years (near final size was inferred when the bone microstructure showed that growth had slowed substantially). By contrast, ossification of the limb bones in modern tetrapods starts much earlier than in either Acanthostega or our fish predecessors. The finding that Acanthostega grew to almost final size and still had a cartilaginous humerus supports the hypothesis that the earliest tetrapods had a predominantly, if not an exclusively, aquatic lifestyle, because a cartilaginous humerus would probably have been unable to bear much weight. This indicates that limbs initially served a purpose on land other than locomotion.

However, the most compelling of Sanchez and colleagues' results lies in a clear disjunction between size and degree of ossification — some individuals reached the same degree of ossification in the long bones at a much smaller body size than others. Developmental plasticity, an organism's capacity to respond flexibly to different external cues throughout life, is thought to have an important role in evolution6,7. Studies of fossils and modern amphibians have elucidated the complex and fascinating connections between developmental plasticity and the responses of individuals to cues of population dynamics and environmental factors, including competition between juveniles, length of growth period, climatic factors and predation8,9,10,11. Sanchez et al. identified two size classes in their study (Fig. 1), although the small sample size limits interpretations with respect to possible drivers of plasticity. It is possible that there were more size classes, which may be revealed when further samples are available.

Figure 1: Possible developmental pathways in the tetrapod Acanthostega.
figure1

Sanchez et al.4 analysed the internal microstructure of fossil forelimb bones of juvenile Acanthostega. The authors found that ossification began at a late stage, after the animals had grown to nearly full size, and that there were at least two size classes (solid arrows). The two classes could represent differences in body size for male and female forms, or developmental plasticity in response to intrinsic or environmental factors. Further size classes might have existed (dotted arrows), which could potentially be revealed by larger sample sizes.

In Acanthostega, the decoupling of size and degree of ossification in a long juvenile stage could indicate that developmental plasticity, and possibly alternative life-history strategies, were already present in the earliest tetrapods. A high degree of developmental plasticity might have provided the means for our early ancestors to respond to changing intrinsic and environmental conditions, and could thereby have had a central role in the initial evolutionary success and subsequent diversification of tetrapods. Footnote 1

Notes

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Correspondence to Nadia B. Fröbisch.

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Fröbisch, N. Teenage tetrapods. Nature 537, 311–312 (2016). https://doi.org/10.1038/nature19432

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