Modularity and Metamorphosis: the effect of complex life history on cranial integration

What drives large-scale patterns of morphological evolution? Natural selection acts upon existing variation, the raw material of evolution, to shape the diverse organisms that we see and study today, but what shapes variation? Development is often presented as a major influence on morphological variation, but linking developmental effects into large-scale models of evolution is difficult because comparative developmental data is relatively uncommon. Quantitative data, specifically measurements of the shapes of organisms and the interactions among parts of an organism, has the potential unify disparate fields of evolutionary study, from genetics to development and morphology, into a single framework. Quantification of organismal shape (morphology), during development has been hindered by difficulties in obtaining measurements from small, immature specimens, which often can lose their shape during preparation. However, in recent years, increased access to high-resolution imaging machines, such as CT scanners, and advanced visualization and digitising software has improved the possibility of gathering large volumes for rigorous statistical analyses of changes during development.

The topic of morphological integration is among those that are highly quantitative and will benefit from the incorporation of comparative developmental data. These terms relate to the intuitive idea that complex organisms have many parts with varying interrelationships. Simply, a change in a foot bone would be expected to have more effect on other parts of the foot than they do on, for example, the nose. Delineating the relationships of different parts of an organism can provide novel and unpredicted information on the genetic, developmental, and functional influences on an organism's morphology, and these patterns of trait relationships are termed morphological integration.

Much research on morphological integration has focused on the mammalian skull and jaws and has shown a number of interesting results. First, mammal skulls are formed of six relatively distinct regions, and this pattern of skull integration is observed across mammals, from monkeys to mice. Second, this pattern may reflect developmental interactions, such as tissue origin, as the skull is a developmentally complex structure. Third, patterns of skull integration change through development, from the early stages immediately after birth until subadulthood or adulthood. This last feature is complicated, but there is some evidence that differences in reproductive strategies, specifically between marsupials (such as kangaroos) and placentals (such as dogs or humans) are reflected in the changes in skull integration that occur during ontogeny.

While most research on morphological integration in vertebrates has been conducted on mammals, especially primates and rodents, there is little comparative data on other vertebrates with which to judge whether mammalian patterns are unusual, or simply reflect a more ancestral condition. Furthermore, the diversity of developmental strategies in mammals is far less than that observed across vertebrates. In this study, we will examine morphological integration in the skull of a vertebrate with a very different developmental strategy to that seen in mammals: the African clawed frog, which undergoes metamorphosis from a larval tadpole to a froglet to an adult frog. We will use CT scanning to gather large numbers of specimens from three stages of development to test if skull integration is similar in frogs and mammals, if skull integration changes during frog development, including metamorphosis, and if skull integration in adult frogs reflects whether bones are formed before, during or after metamorphosis.

The results of this study, in comparison with existing data for mammals, will form the basis for a more comprehensive study of developmental integration across tetrapods.

We will engage with the academic community by publishing results in high-impact peer-reviewed journals (e.g Proceedings of the Royal Society, Evolution, Biology Letters), presentation of results at relevant conferences (e.g. Society of Integrative and Comparative Biology) and through active participation in an online web resource, recently developed by colleagues at UCL and Hull York Medical School for sharing of 3-D image data with the international community.

We will engage with the wider, non-academic community by using the familiar frog and its metamorphosis, a common topic in pre-university science education, to introduce the public to the cutting edge biological imaging methods and research bridging genetic and developmental to evolutionary questions.

We will disseminate our results and conclusions to the wider public via the following means
(1) Press releases. UCL has a very proactive press office, which links between researchers and the media. We will announce the results of our work via press releases through the UCL and NERC press offices. The PI's recent work has been featured in the international news, including the BBC and Washington Post.

(2) Presentations/talks. The PI has extensive experience of direct engagement with the general public via talks, open days and other events. For example, the PI has presented her work on mammalian evolution to the general public at 'Darwin Live' sessions at the Natural History Museum, at 'Brain Food' lunchtime lectures at UCL, and at public debates in the Grant Museum at UCL and the Horniman Museum. She has also been featured on National Geographic, Discovery, BBC News, BBCRadio4, and BBCWales to discuss various aspects of evolutionary biology, paleontology, and science funding. We will seek opportunities to continue this level of engagement, including offering talks during Science Week.

(3) Teaching. The results of our research will be integrated into existing lecture courses at UCL on vertebrate evolution and evolutionary development. This keeps the course content fresh and up-to-date, and inspires students to consider the links between fields and the utility of imaging methods to get more out of anatomical specimens. This research should also produce 'spin-off work that could form the basis for Masters and PhD projects.

(4) Museum workshop: We will use the reconstructed CT-scans to develop a museum workshop with Grant Museum professionals that clearly visualize in 3-D view the profound changes that occur during frog metamorphosis. This image-based workshop would be focused at primary to early secondary school children but would interest the general public as well. It could be easily transferred to other museums and schools, or even developed into an e-learning tool.