Who's a Bonehead? Novel Insights into Evolutionary History from Reptilian Skull Roof Structure

Through investigating the reptile skull roof by means of high-resolution computed tomography (µCT), we unveiled a hitherto unknown case of convergent evolution and provide novel insights into the lifestyle of extinct species.
Published in Ecology & Evolution
Who's a Bonehead? Novel Insights into Evolutionary History from Reptilian Skull Roof Structure

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BioMed Central
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First evidence of convergent lifestyle signal in reptile skull roof microanatomy - BMC Biology

Background The study of convergently acquired adaptations allows fundamental insight into life’s evolutionary history. Within lepidosaur reptiles—i.e. lizards, tuatara, and snakes—a fully fossorial (‘burrowing’) lifestyle has independently evolved in most major clades. However, despite their consistent use of the skull as a digging tool, cranial modifications common to all these lineages are yet to be found. In particular, bone microanatomy, although highly diagnostic for lifestyle, remains unexplored in the lepidosaur cranium. This constitutes a key gap in our understanding of their complexly interwoven ecology, morphology, and evolution. In order to bridge this gap, we reconstructed the acquisition of a fossorial lifestyle in 2813 lepidosaurs and assessed the skull roof compactness from microCT cross-sections in a representative subset (n = 99). We tested this and five macroscopic morphological traits for their convergent evolution. Results We found that fossoriality evolved independently in 54 lepidosaur lineages. Furthermore, a highly compact skull roof, small skull diameter, elongate cranium, and low length ratio of frontal and parietal were repeatedly acquired in concert with a fossorial lifestyle. Conclusions We report a novel case of convergence that concerns lepidosaur diversity as a whole. Our findings further indicate an early evolution of fossorial modifications in the amphisbaenian ‘worm-lizards’ and support a fossorial origin for snakes. Nonetheless, our results suggest distinct evolutionary pathways between fossorial lizards and snakes through different contingencies. We thus provide novel insights into the evolutionary mechanisms and constraints underlying amniote diversity and a powerful tool for the reconstruction of extinct reptile ecology.

Why are terrestrial vertebrates so highly diverse? In times of anthropogenic change and mass extinctions, this key question to evolutionary research is more relevant than ever. We often attribute this phenomenon to modifications in accordance with different environments and lifestyles. However, it is not always easy to reconstruct from the fossil record how historic key events determined the destinies of entire lineages millions of years ago. Therefore, 160 years after Darwin's theory of evolution, our understanding of certain evolutionary mechanisms remains incomplete.

In order to better understand the complex interrelations between vertebrate lifestyle, form, and evolution, we looked into the skull roof structure of squamate reptiles i.e., lizards and snakes. We wanted to understand to what extent their bone structure reflects certain lifestyles. Although many of these reptiles use their skulls as a digging tool, this question has never been systematically investigated. In our paper First Evidence of Convergent Lifestyle Signal in Reptiles Skull Roof Microanatomy, we therefore employed computer simulations to reconstruct the evolution of a specialised burrowing lifestyle over a period of 240 million years. Remarkably, we found that burrowing evolved independently in 54 squamate lineages. These reptiles are therefore particularly well suited as a model system for the study of convergent evolution.

Scincoid lizards, such as this representative from the Australian east coast, are among the most diverse squamates – both ecologically and taxonomically. Nonetheless, we were surprised to identify 20 independent acquisitions of a specialized burrowing lifestyle in this clade alone. Photo by Roy Ebel.

In the second phase of our study, we compared the skull roof structure of lizards and snakes in accordance with their lifestyles. To this end, we made use of high-resolution computed tomography (micro-CT) for the 3D visualisation of bone tissue and employed a new, effective protocol for data analysis. Doing this, we achieved a large sample size, allowing us to draw conclusions about the entire squamate reptilian clade with over 11,000 species. We found that burrowing lizards and snakes have repeatedly evolved a particularly dense and compact skull roof in independent evolutionary processes. We further identified typical proportions of both the skull and between the skull roof bones as convergently evolved modifications associated with this lifestyle.

This desk at the CT-Vis-Lab of the Museum für Naturkunde Berlin says quite a bit about our working routine. From right to left: VG Studio MAX for processing 3D-volumes acquired with µCT, ImageJ for processing extracted slices, and R-Studio for the analysis of convergence and lifestyle signal. As a coincidence, the stages of data reduction correlate with decreasing screen size. ...and who would have thought that this is how a biologist's workspace may look like? Photo by Roy Ebel.

In our study, we present a novel case of convergent evolution: in different lineages, very similar structures have independently evolved in response to a common lifestyle. Such similarities reflect a certain function, in this case burrowing, and may therefore provide little information on the phylogenetics relations between the considered taxa. Nonetheless or precisely therefore, the knowledge of these processes is of outstanding importance: by means of skull roof structure, we can now reconstruct the lifestyle of reptiles that became extinct millions of years ago. Our findings thus cast completely new light on the evolutionary history of certain lineages. This may particularly apply to snakes, for which both an aquatic and burrowing origin have been controversially discussed for decades. Our work now adds to a growing body of evidence for the latter. Having said this, our findings may also have important implications beyond squamate reptiles. A burrowing lifestyle has likely played a key role in the evolutionary history of turtles and certain amphibians. Recent studies even suggest that the mammalian stem lineage may not have survived the largest mass extinction in earth's history at the end of the Permian about 250 million years ago without adopting a burrowing lifestyle. It is therefore invaluable to understand such historical lifestyle transitions.

This little critter is a rare burrowing gymnophthalmid lizard from Brazil, which quickly became a lab favourite for its happy smile. We were able to include the specimen in our dataset due to a loan from the American Museum of Natural History (AMNH R64876). In total, our dataset comprises specimens from 13 herpetological collections worldwide. Photo by Roy Ebel.

Should our work have sparked your interest in the fascinating field of squamate skull morphology and its implications for their ecology and evolution, you may be pleased to hear that we uploaded the µCT-scans employed in our study into the Data Repository of the Museum für Naturkunde Berlin. They will thus be available for future research projects worldwide.

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