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.
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.
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.
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.
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.
Notes
References
- 1.Clack, J. A. Gaining Ground: The Origin and Evolution of Tetrapods 2nd edn (Indiana Univ. Press, 2012).
Schneider, I. & Shubin, N. H. Trends Genet. 29, 419–426 (2013).
Standen, E. M., Du, T. Y. & Larsson, H. C. E. Nature 513, 54–58 (2014).
Sanchez, S., Tafforeau, P., Clack, J. A. & Ahlberg, P. E. Nature 537, 408–411 (2016).
Fröbisch, N. B., Olori, J. C., Schoch, R. R. & Witzmann, F. Semin. Cell Dev. Biol. 21, 424–431 (2010).
Moczek, A. P. et al. Proc. R. Soc. B 278, 2705–2713 (2011).
West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003).
Schoch, R. R. Annu. Rev. Earth Planet. Sci. 37, 135–162 (2009).
Schoch, R. R. Evolution 63, 2738–2749 (2009).
Urban, M. C., Richardson, J. L. & Freidenfelds, N. A. Evol. Appl. 7, 88–103 (2014).
Whiteman, H. H. et al. Oecologia 168, 109–118 (2012).
Author information
Affiliations
Nadia B. Fröbisch is at the Museum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany.
- Nadia B. Fröbisch
Corresponding author
Correspondence to Nadia B. Fröbisch.Rights and permissions
To obtain permission to re-use content from this article visit RightsLink.
About this article
Publication history
Published
DOI
Share this article
Anyone you share the following link with will be able to read this content:
Subjects
Comments
By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.
Nenhum comentário:
Postar um comentário
Observação: somente um membro deste blog pode postar um comentário.