Scientists from the United Kingdom and Spain have discovered that tetrapods had more complex connections between their skull bones than fish and, rather than promoting the diversification of life on land, these changes to skull anatomy actually restricted the evolution of tetrapod skulls.
The developmental underpinnings and functional consequences of modifications to the limbs during the origin of the tetrapod body plan are increasingly well characterized, but less is understood about the evolution of the tetrapod skull; decrease in skull bone number has been hypothesized to promote morphological and functional diversification in vertebrate clades, but its impact during the initial rise of tetrapods is unknown; Rawson et al. tested this by quantifying topological changes to cranial anatomy in fossil and living species bracketing the fin-to-limb transition using anatomical network analysis. Image credit: Zina Deretsky, National Science Foundation.
Tetrapods evolved from fish and were the earliest land animals with limbs and digits; the ancestors of everything from amphibians to humans.
Their origin was a transformative event in vertebrate evolution and involved marked changes to the body plan of vertebrates.
“Tetrapod skulls generally have fewer skull bones than their fish ancestors, but simply counting the number of bones misses some important data,” said Dr. James Rawson, a researcher at the University of Bristol.
“We used a technique called network analysis, where the arrangement of skull bones — which bones connect to which — is recorded in addition to bone number.”
In their research, Dr. Rawson and his colleagues quantified the organization of skull bones in over 100 living and fossil animals.
“Traditionally, anatomy research has been mostly descriptive or qualitative,” said Dr. Borja Esteve-Altava, a researcher at the Universitat Pompeu Fabra.
“Network analysis provides a sound mathematical framework to quantify anatomical relations among bones: a kind of data often overlooked in most studies on morphological evolution.”
The researchers found that tetrapods having fewer skull bones than fish made the organization of their skulls more complex.
“It might seem strange, but having fewer bones means each of those bones must connect with more of its neighbors, resulting in a more complex arrangement,” Dr. Rawson said.
“Modern frogs and salamanders had the most complex skulls of all the animals we studied.”
The skulls of the earliest tetrapods also became more consolidated into a single unit, whereas their fish ancestors had skulls made of several distinct sections.
By looking at the variety of skull bone arrangements over time, the authors also discovered that the origin of tetrapods coincides with a drop in the variety of skull bone arrangements.
“We were surprised to find these changes to the skull seemed to limit tetrapod evolution, rather than promoting radiation to new habitats on land,” said Professor Emily Rayfield, a researcher at the University of Bristol.
“We think that the evolution of a neck, extinction events or a bottleneck in skull development may be responsible.”
“We also see a similar drop in structural variability for the limb bones in early tetrapods, but the drop in the limbs happens 10 million years earlier,” Dr. Rawson said.
“It seems that different factors were affecting skull and limb evolution in early tetrapods, and we have so much more to learn about this crucial time in our own evolutionary history.”
The research is described in a paper published today in the journal Science Advances.
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James R.G. Rawson et al. 2022. Early tetrapod cranial evolution is characterized by increased complexity, constraint, and an offset from fin-limb evolution. Science Advances 8 (36); doi: 10.1126/sciadv.adc8875
