Ever since Darwin, we know that as a consequence of evolutional adaptation, species may change their appearances and body functions as the environment changes. A common question of evolutionary biologists is if the body shape can be directly linked to a specific ecological trait, like diet. In a new study published in the journal Evolution, Guilherme Hermanson and his team of the University of Fribourg studied the environmental influences that act on the skull of turtles.

The skull is an important body part of animals, as it interacts very directly with the environment, for example during food acquisition and processing. In turtles, this relationship may even be enhanced given that turtles do not use their hands for gathering or manipulating food. «Turtles are sometimes overlooked by evolutionary studies, which is in part because they have an odd body with the shell encasing so much of the animal. However, it is exactly this that makes turtles interesting from an evolutionary point of view.» says Senior researcher Serjoscha Evers. Turtles can tell a lot about how evolution acts on body shape. They live in different environments today, and their fossil record shows that turtles have repeatedly conquered different habitats on land and at sea throughout about 230 Million years of evolutionary history. These repeated environmental changes through time form an excellent case study to test the influence of adaptation on skulls.

Modern 3D analyses
The team used a state-of-the-art approach combining three-dimensional skull models of living and extinct turtles and statistical models that relate skull shape with ecology. «This is the first study that combines 3D skulls of turtles with sophisticated statistical tools. We could show that even groups without many species, like turtles, can be used as models to understand primary evolutionary concepts, such as adaptation», Guilherme Hermanson says about the approach. The results show that there are multiple influences that determine skull shape. One observation is that closely related turtles, on average, are more similar in their shapes than distantly related species – which is a central prediction of evolutionary theory. 

Big impact of diet and feeding modes
However, ecological adaptations can indeed overprint this background signal, and further change skull shape. The study finds a strong influence of diet and feeding modes. For example, aquatic turtles have long skulls and forward-facing eyes – which are useful in active hunting of prey underwater. Turtles that eat hard-shelled foods like snails have broad crushing surfaces of theirs mouths, which they use instead of teeth to break open shells. However, the researchers also found that different type of influences on shape affect different parts of the skull: While many feeding adaptations can be found in the mouth region, the eyes and the overall dimensions of the skull, differences in neck retraction affect the backside of the skull to which the neck muscles attach.

Ecological factors not decisive
Although all these influences have important measurable effects on skull shape, the team of Guilherme Hermanson also found that the ecological factors they considered explain only about a fourth of the skull shape differences between turtles: much of the visible shape difference must be accounted for by non-adaptive explanations, such as the family relationships of turtle species.

The researchers used their findings to predict the ecology of extinct turtles with well-preserved skull fossils. The skulls of fossil turtles indicate that neck retraction – the capability to fully withdraw the head under the protective shell – likely originated during the geological era of the Middle or Late Jurassic, about 150 million years ago. During this time period, turtles invaded aquatic habitats for the first time. The team thus suggests that the diversification of turtles into aquatic habitats was related to the acquisition of neck retraction, which allowed turtles to exploit new ecological niches in which they evolved the shape diversity we observe today. 

Thanks to a combination of different 3D models with statistical analysis, questions can now be explored that could not have been answered ten years ago. This unusual approach helps to break new scientific ground in evolutionary theory.

Study:
Hermanson G, Benson RBJ, Farina BM, Ferreira GS, Langer MC, Evers SW (2022): Cranial ecomorphology of turtles and neck retraction as a possible trigger of ecological diversification. Evolution, https://doi.org/10.1111/evo.14629