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Convergence and functional evolution of longirostry in crocodylomorphs
Untangling the evolution of feeding strategies in ancient crocodiles

by University of Bristol

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Crocodylomorphs were a highly morphologically and ecologically diverse clade. These extinct crocodile relatives had a much richer variety of skull shapes than living crocodilians, suggesting a wide range of feeding strategies. Credit: Darren Naish, Tetrapod Zoology

Ancient aquatic crocodiles fed on softer and smaller prey than their modern counterparts and the evolution of skull shape and function allowed them to spread into new habitats, reveal paleobiology researchers from the University of Bristol and UCL.

For the study, published today in Paleontology, the team digitally reconstructed the skull of an extinct species of marine crocodile and compared it to similar living species to gain new insights into the diet of ancient crocodiles and their role in ecosystems around 230 million years ago.
Modern crocodiles are known for their characteristic anatomy and apex predator role in semiaquatic ecosystems but their ancient ancestors, which lived side-by-side with the first dinosaurs in the Late Triassic period, were tiny land-dwellers that soon gave rise to a great diversity of forms.
One group, the thalattosuchians, went into the sea and became marine specialists. They had long, thin snouts, resembling that of the living gharial, which feeds on fish in rivers in India. An early member of this group, Pelagosaurus typus, inhabited shallow marine environments in what is now Europe during the Early Jurassic.
By looking at the different shapes of their skulls, scientists were able to work out what crocodiles were eating. As reported in the journal Palaeontology today, the biomechanical and macro-evolutionary approaches applied during this latest study show how ancient crocodiles came to occupy diverse and specialized ecological niches.
Ph.D. student Antonio Ballell, from the University of Bristol's School of Earth Sciences and lead author of the study, said: "We used up-to-date techniques to explore how the skull of these extinct crocodilians functioned and evolved. Our first aim was to compare how the skull stressed and strained under simulated feeding loads in Pelagosaurus compared to the living gharial and gain new understanding of how the extinct species fed."
Using modern computational methods, coupled with 3-D digital skull models obtained from CT scans of Pelagosaurus and the gharial, the research team was able to look for muscle scars in the fossils that mark where the muscles once attached to reconstruct the jaw-closing musculature.
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Skull of the 180 million-year-old marine crocodilian Pelagosaurus typus from Strawberry Bank, England. Credit: Antonio Ballell

This approach was coupled with finite element analysis, an engineering technique that predicts how biological structures behave under specific loading scenarios such as feeding loads.
Co-author, Dr. Laura Porro from UCL Cell and Development Biology, said "Modern computational techniques allow palaeobiologists to 'bring extinct species back to life' and infer how they fed and lived from the anatomical information provided by fossils. Using CT scans, we are able to visualise internal areas of the skull and scars on the bones, indicating where muscles attached, that scientists had never observed before. Engineering methods allowed us to test how the skull responds to biting, 230 million years after this animal's last meal."
Their results show that the weaker jaw of Pelagosaurus might indicate that it specialized on softer and smaller prey than the modern gharial.
The team also analysed how fast feeding-related characters of the jaws evolved in a wide range of extinct crocodilian species. This showed that traits related to the long snouts of thalattosuchians evolved rapidly, suggesting that they occupied a very specific marine ecological niche soon after the origin of the lineage.
Co-author Dr. Benjamin Moon from the University of Bristol added: "Pelagosaurus and closely related species differ from other crocs in their slender lower jaws, and this helped their evolutionary success in the Early Jurassic, when marine ecosystems were still recovering from the devastating End-Triassic mass extinction."
The study contributes to the increasing understanding of functional evolution of crocodylomorphs and the ecological dynamics of Mesozoic marine reptiles.
Antonio Ballell concluded: "Our findings highlight the spectacular diversity of feeding strategies present in extinct crocodile relatives and how this was important in the evolution and diversification of the group. We found that different lineages explored and conquered ecological niches in different ways.
"The evolutionary history of crocodiles was very complex and looking at it from a functional perspective is fundamental to understand it".

Journal Reference:
Antonio Ballell et al. Convergence and functional evolution of longirostry in crocodylomorphs, Palaeontology (2019). DOI: 10.1111/pala.12432

During the Mesozoic, Crocodylomorpha had a much higher taxonomic and morphological diversity than today. Members of one particularly successful clade, Thalattosuchia, are well‐known for being longirostrine: having long, slender snouts. It has generally been assumed that Thalattosuchia owed their success in part to the evolution of longirostry, leading to a feeding ecology similar to that of the living Indian gharial, Gavialis. Here, we compare form and function of the skulls of the thalattosuchian Pelagosaurus and Gavialis using digital reconstructions of the skull musculoskeletal anatomy and finite element models to show that they had different jaw muscle arrangements and biomechanical behaviour. Additionally, the relevance of feeding‐related mandibular traits linked to longirostry in the radiation of crocodylomorph clades was investigated by conducting an evolutionary rates analysis under the variable rates model. We find that, even though Pelagosaurus and Gavialis share similar patterns of stress distribution in their skulls, the former had lower mechanical resistance. This suggests that compared to Gavialis, Pelagosaurus was unable to process large, mechanically less tractable prey, instead operating as a specialized piscivore that fed on softer and smaller prey. Secondly, innovation of feeding strategies was achieved by rate acceleration of functional characters of the mandible, a key mechanism for the diversification of certain clades like thalattosuchians and eusuchians. Different rates of functional evolution suggest divergent diversification dynamics between teleosaurids and metriorhynchids in the Jurassic.

In this study we tested the proposed functional convergence between Pelagosaurus and Gavialis. Digital muscle reconstruction and FE modelling confirm that Pelagosaurus shares a similar biomechanical behaviour with Gavialis as a consequence of longirostry. However, the higher stresses recorded in the skull of Pelagosaurus suggest that the two taxa occupied slightly different ecological niches. Instead, our results suggest that the thalattosuchian was a particularly specialized piscivore that fed on softer and smaller prey than the gharial. Palaeoenvironmental conditions and ecological interactions with other marine reptiles may have played a role in the acquisition of this particular feeding strategy. Consequently, this study notes the limitations of relying only on morphological similarity when testing functional hypotheses in fossils and supports previous work that highlights the relevance of testing functional convergence with extant models to infer feeding habits in extinct taxa.
Patterns of evolutionary rates indicate that functional innovation in the mandible was an important factor in the radiation of some crocodylomorph clades by allowing development of novel feeding strategies. Constant evolutionary changes in AMA were a driving force for feeding specialization within Thalattosuchia, while MJD evolutionary rates support an ‘early burst’ of evolution at the origin of teleosaurids, associated with the acquisition of a new feeding strategy. Dissimilar rates of evolution between the two thalattosuchian clades suggest that in the Early Jurassic, teleosaurids rapidly radiated into an empty ecological niche, while metriorhynchids diversified more slowly in the more competitive Late Jurassic marine environment. Finally, decrease in jaw depth was a mechanism that facilitated the ecological transition of eusuchians to become semiaquatic ambush predators.
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