Skull Modularity in Evolutionary Morphology

One of the questions in modern biology is how some of these most dramatic examples of morphological diversity can be explained. Two of these examples can be found in birds: one is Darwin’s finches, which have a famously very big diversity of beak shapes, which allows them to focus on different food types. Another similar example, which is in many ways even more dramatic, is birds called Hawaiian honeycreepers, which inhabit Hawaii. On Hawaii, a single ancestor came from Asia (so they’re probably related to rosefinches, which we find now in Japan and in Siberia) to the Hawaiian Islands about 10 million years ago and produced enormous variation. Historically, there were over 40 species. There were some finches which fed on seeds; some of them became creepers; they had elongated beaks to kind of catch insects from under the bark; and some from several lineages became what we call honeycreepers, that is, they evolved the super long beaks to feed on the nectar from the flowers.

So, this enormous diversity that you find in Hawaii among the Hawaiian honeycreepers is one of the great examples, one of the textbook examples of adaptive evolution in nature. How do you explain this? So recently, we decided to look at this from a more structuralist perspective; that is, we generated a full collection of high-definition 3D shapes using computed tomography scans, CT scans that are used in hospitals to produce stands of human organs by the surgeons, for example, by the physicians. We generated a collection of CT scans from all the species of Hawaiian honeycreepers and their relatives. We also wanted to compare the diversity of the skulls and beaks to that of Darwin’s finches, so we generated a similar collection of high-definition scans from Darwin’s finches and their relatives. We also scanned some of the species which were ancestral to both Darwin’s finches and Hawaiian honeycreepers.

We wanted to compare the skull diversity in these two groups (which are both very diverse) using the same landmarks within the same morphospace using a method called geometric morphometrics where we apply the same landmarks onto the skulls, and we use the computer to ask questions on how the diversity compares and what happened during the evolution of these two very diverse clades of organisms.

What we found was very surprising. We found that Darwin’s finches’ skull shapes were, as we expected, much more diverse than those of the ancestors; they occupied much more of the morphospace. The Hawaiian honeycreepers turned out to be even more diverse; they occupied the amount of morphospace which was even greater than that of Darwin’s finches, including some of the truly unique skull shapes and beak shapes, especially those which were adapted for feeding on the nectar. But the biggest surprise was when we compared how the different parts of the skulls evolved and developed relative to each other. This is referring to what we call skull modularity.

The skull can be divided into several domains, several parts which have somewhat distinct functions. For example, a beak is one such module; the cranial vault which protects the brain; the upper part of the skull is another module; the orbits, which protect the eyes, is another module. So when we applied landmarks, we applied them so that we could distinguish all these different modules in the skull and see how they changed during evolution relative to each other, that is, if all of them changed in the same way. For example, if, as a skull becomes bigger, all the modules become bigger, then it means that the skull all these modules are highly integrated; they are talking to each other very closely, and they behave in very similar ways. If these modules are more independent, then we talk about increased modularity, that is, increased independence of those different parts and lower integration.

So what we found is that in Darwin’s finches relative to the ancestral species there was increased modularity in the beak.

We already knew that we already knew that the beak program is highly modular in Darwin’s finches, so that was a nice confirmation of our previous studies. We found that in ancestral birds, the skull is highly integrated; that is, all the different parts change in a very close correlation with each other. However, in Hawaiian honeycreepers, we found that the integration was extremely low; most of the parts of the skull’s different modules of the skulls were incredibly flexibly connected to each other. It was truly like a Lego system in that different parts could be mixed and matched; they could change with relative ease during evolution, and this is what we think was the foundation of the diversity: the fact that they were able to change different parts of the skulls in different ways. This incredible flexibility and modularity in their skull design is what was probably foundational to the diversity, and that’s what’s underlying their ecological success.

We do not know yet how modularity is established; we do not know yet how the different modules separate from each other and how they talk to each other. We know they exist, and we know that this communication between different modules is critical to the development, but we do not yet know how this modularity is established, and we do not know yet how this modularity can change and how evolution can change the level of integration modularity. But we do see evidence now, for example, when we’re looking at the skull modularity in the Hawaiian honeycreepers, that the flexibility which they evolved in the designs correlates really strongly with the amount of diversity that they were able to generate during the evolution.

Skull modularity is important for two reasons. One is an evolutionary reason; that is, we would like to understand how diversity can be generated for structures which are otherwise thought to be hard to change, such as skulls and animal heads where you have multiple tissues and multiple organs such as the brain and the eyes, the musculature in the skull, and the skull has multiple different bones, they all have to talk to each other, and this integration is thought to be a limiting factor to their evolution because all these different things have to change together. The studies on Hawaiian honeycreepers, for example, suggest this integration can change; that is, one can increase the flexibility of individual elements and make them change relatively independently from each other. This provides us with a very important clue as to how the skull as a whole can evolve as well.

Another reason why skull modularity is important is developmental. As a developmental biologist, I would like to understand how modularity is established in the first place and how you, for example, establish different parts of the skull. The skull is made of multiple bone and cartilage elements. How are those elements established? How are they individually regulated in terms of their size and shape? How are they integrated into the overall whole? How do they talk to each other? Essentially, it’s like a very complex puzzle with all the pieces coming together to form a functional system. So, developmental mechanisms behind modularity integration are very poorly understood at the moment, and it is important to understand these mechanisms before we can understand how they can be altered during evolution.

It is important also to realize that these questions about integration are also important for human health. There are quite a few biomedical conditions where some of these parts, for example, some of the bones, are fused prematurely, or they don’t fuse where they should be, and this causes a number of different craniofacial abnormalities, which are essentially problems with the integration of the different parts of the cranium. So cranial modularity is important to understand in the future from all those perspectives: from an evolutionary perspective, how it can change to facilitate morphological evolution; from a developmental perspective, how the modularity and integration are established at the genetic molecular level, so what are the developmental, for example, genes and pathways involved that allowed these different modules to interact with each other, how this interaction can change, how can it become stronger or weaker and how that can facilitate, again, the evolution of the entire system. Finally, it is important for biomedical reasons because a lot of these interactions between different parts, between the brain and the skull and, again, between the skull and the musculature, are critical for the proper development of the head. When something goes wrong, when some of these mechanisms which allow for integration are affected, that can cause craniofacial abnormalities that have to be treated by surgical or other techniques.

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