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Investigating the Arthropod Segmentation Clock that controls Sequential Segment Formation during Arthropod Development and its Potentially Ancient Evolutionary Origins

Final Report Summary - ARTHROPODSEGCLOCK (Investigating the Arthropod Segmentation Clock that controls Sequential Segment Formation during Arthropod Development and its Potentially Ancient Evolutionary Origins)

Over the past four years this Marie Curie Career Integration Grant has helped fund research into the way the red flour beetle, Tribolium castaneum, makes its thoracic and abdominal body segments. The fellow’s previous work as a Marie Curie funded post-doctoral researcher in Greece helped demonstrate striking similarities in the way this insect makes its trunk segments and the way vertebrates (including humans), make their internal reiterated structures, such as vertebrae and associated muscles (see Sarrazin, Peel & Averof, 2012. Science. Vol. 336, 338). Both insect body segments and human vertebrae are patterned using a dynamic gene network called the ‘segmentation clock’, in which repeated bursts of gene expression (i.e. developmental genes turning on and off repeatedly) ultimately gives rise to repeated structures along the anterior-to-posterior body axis. The objectives of the CIG-funded research were to gain a much deeper understanding of the scale and complexity of this insect segmentation clock, and to identify similarities or differences in the genetic components and/or organization of the insect and vertebrate segmentation clocks that provide insights into their independent or common evolutionary origins. The work also aimed to further develop Tribolium castaneum as a powerful invertebrate model system to study the principles underpinning molecular oscillators and their role in animal segmentation, and identify gene network changes that underpinned the evolution of segmentation mechanisms within the insects.

The work has successfully revealed some important insights into how the gene network controlling segment formation in insects might have been modified during insect evolution. We already know that the segmentation process has been speeded up during the evolution of some insect species, such that rather that segments forming sequentially from head-to-tail during embryogenesis in a relatively slow manner and under the control of a segmentation clock (as is seen in the beetle Tribolium and for human vertebrae), body segments instead form quickly and more-or-less simultaneously in the egg via an evolutionary novel clock-independent mechanism, as seen in the fruit fly Drosophila melanogaster: As a popular and powerful research model, the mechanism by which Drosophila forms its body segments rapidly and simultaneously has been intensively studied, allowing direct comparison with the more ancestral mode of segmentation seen in Tribolium. This Marie Curie-funded work has shown that the transition from Tribolium-like sequential segmentation to Drosophila-like simultaneous segmentation likely involved changes in the temporal order in which key developmental genes are expressed, and corresponding switches in the direction of regulatory interactions between these genes. The work has also helped identify three conserved ‘temporal factors’ that in both Drosophila and Tribolium control the segmentation process through developmental time, mediating changes in the way key segmentation genes interact with each other at different stages of the segmentation process. Comparisons between Tribolium and Drosophila suggest that shifts in the spatiotemporal pattern in which these three conserved ‘temporal factors’ are turned on during embryogenesis played a key role in the transition from sequential to simultaneous segmentation in insects.

Furthermore, these three temporal factors are all known to play a role in the formation of the growing body axis in vertebrates, suggesting more similarities between the developmental processes operating in insects and humans that likely have been inherited from a shared common ancestor that lived over 500 million years ago. In addition, it seems likely that these temporal factors form at least part of an insect/Tribolium ‘wavefront’ that converts the temporal information contained within molecular oscillations of the segmentation clock into the spatial pattern that ultimately gives rise to segments. This is analogous to a well-studied ‘wavefront’ that plays an equivalent role in vertebrates, albeit using a different set of genes. If this hypothesis proves correct following future functional analyses, Marie Curie funding supporting the fellow’s research as a post-doctoral researcher in Greece and then a reintegrated independent researcher in the U.K. will have funded experiments that helped identified the insect segmentation clock and the insect wavefront respectively, as well as developing an evolutionary model where insect segments and vertebrate vertebrae form via very similar developmental principles, but using quite different combinations of molecular parts.

This funding has also helped the fellow establish state-of-the-art CRISPR/Cas9 genome editing techniques in his laboratory. This powerful technique will result in a much more in-depth analysis of the Tribolium sequential segmentation mechanism in future, allowing more informative comparisons to be made to the segmentation mechanisms operating in Drosophila and vertebrates.

Finally, this Marie Curie funding played a key role in helping the fellow secure a permanent academic position at the University of Leeds, by facilitating his successful application for further research funds and helping him purchase key equipment (e.g. a fluorescent stereomicroscope for embryo dissection and imaging) that will allow research into evolutionary developmental biology to continue well into the future. Over the four years of funding, the fellow has informed and educated a range of different people about modern evolutionary research, including hundreds of school children via the annual University of Leeds Festival of Science, many members of the general public via university open days, 500 internationally-diverse undergraduate students per year via his role as a full time permanent lecturer and graduate students via hands on supervision, seminars as well as teaching on an international summer school. In addition to interesting research results and the successful career integration of the fellow, this Marie Curie CIG grant has therefore also facilitated the transfer of knowledge about evolutionary biology across the U.K. and Europe.

Fellow Contact Details:
Dr. Andrew D. Peel
Room 8.22 LC Miall Building
School of Biology
Faculty of Biological Sciences
University of Leeds