Evolutionary biologists are tasked with understanding the great diversity of organisms around us. For all we have discovered about the natural world, there is still so much yet to be understood.

Researchers at the University of Adelaide‘s Environment Institute are using comparative approaches to understand how phenotypic diversity evolves by the process of natural selection, using a surprising group of animals: sea snakes. 

Sea snakes, related to Australian venomous snakes such as tiger snakes, are an excellent system to study trait evolution. The vide above shows us how some sea snakes have evolved a unique body shape – a tiny head atop a narrow forebody with a wide hindbody – to exploit the niche of feeding on eels hidden in burrows on the seafloor. 

Image: A microcephalic species demonstrating the tiny head and forebody relative to the hindbody (Hydrophis atriceps; credit: Arne Rasmussen).

The research behind this video was led by Dr Emma Sherratt and Associate Professor Kate Sanders. They examined the system from different angles, looking at evolutionary history, morphological change during development, and dietary specialisation, to create a big picture of how these so-called ‘microcephalic’ forms evolved multiple times among other species of sea snake. 

Dr Sherratt, A/Prof Sanders and their colleagues published their findings in a series of four papers. The first of these quantified the evolutionary link between a diet of burrowing eels and the microcephalic phenotype. This was done by reconstructing an evolutionary tree for all sea snake species, and observing that multiple species that specialise on eel prey and have the microcephalic phenotype despite not being closest relatives. This shows that extreme body shape changes have occurred repeatedly during sea snake evolution; burrowing eels must present an important resource for hungry sea snakes.

The researchers were curious about the developmental changes that might allow sea snakes to shift their body shapes so readily in response to feeding opportunities.This led them to question whether microcephalic sea snakes, which give birth to live young, are born already microcephalic or obtain their distinctive head and body shapes as they grow into adults. By measuring lots of museum specimens of different ages they found that regular sea snakes have fore and hind bodies that grow in proportion, whereas the hind bodies of microcephalic species grow faster than their forebodies, causing their shape to become more extreme as they grow to adulthood.

Image: Digital rendering of a microcephalic sea snake skeleton (Microcephalophis gracilis; credit: Dr Emma Sherratt).

Looking inside the museum specimens using X-rays revealed yet more developmental changes. The researchers found that skulls of adult microcephalic species closely resembled those of juveniles of other species. They also found microcephalic sea snakes have more vertebrae than regular sea snakes, particularly in forebody. In fact, the vertebrae are not just numerous, they are very small compared to those along the rest of the body in both adults and newborn microcephalic sea snakes. These findings together suggest that the microcephalic phenotype originates at the embryo stage, as a result of changes to the timing of development, a process known as heterochrony. 

By linking a novel diet of burrowing eel prey to the repeated evolution of extreme head and body shape changes in sea snakes, Dr Sherratt, A/Prof Sanders and colleagues uncovered a dynamic story of powerful selection pressures and rapid evolution. Going a step further, they revealed that this innovative solution to the challenge of finding food is achieved by complex changes in timing during sea snake development. But every answer prompts a fresh question. Ongoing research seeks to discover the identity and history of genetic variants responsible for shape shifts, and quantify the role of these changes in speciation.   

Articles:

Sherratt, E., Rasmussen, A. R., & Sanders, K. L. (2018). Trophic specialization drives morphological evolution in sea snakes. Royal Society Open Science, 5(3). https://doi.org/10.1098/rsos.172141

Sherratt, E., Coutts, F. J., Rasmussen, A. R., & Sanders, K. L. (2019). Vertebral evolution and ontogenetic allometry: The developmental basis of extreme body shape divergence in microcephalic sea snakes. Evolution and Development, 21(3), 135–144. https://doi.org/10.1111/ede.12284

Sherratt, E., Sanders, K. L., Watson, A., Hutchinson, M. N., Lee, M. S. Y., & Palci, A. (2019). Heterochronic Shifts Mediate Ecomorphological Convergence in Skull Shape of Microcephalic Sea Snakes. Integrative and Comparative Biology, 59(3), 616–624. https://doi.org/10.1093/icb/icz033

Sherratt, E., & Sanders, K. L. (2020). Patterns of intracolumnar size variation inform the heterochronic mechanisms underlying extreme body shape divergence in microcephalic sea snakes. Evolution and Development, 22(3), 283–290. https://doi.org/10.1111/ede.12328

Acknowledgements:

• Video by Animate Your Science
• A/Prof Kate Sanders was funded by ARC FT130101965
• Dr Emma Sherratt funded by The University of Adelaide Research Fellowship
• Video supported by the Environment Institute and The University of Adelaide Research Fellowship
• Article by Dr Emma Sherratt and A/Prof Kate Sanders