Investigating the developmental genetic mechanisms that control segment formation during animal development and their potentially ancient evolutionary origins

Three of the most speciose animal phyla exhibit segmented body plans. The arthropods (e.g. insects, crustaceans, millipedes, centipedes, spiders, mites etc.) and the annelids (e.g. earthworms, marine polychaete worms, leeches etc.) have segmental body units that are clearly visible to the naked eye. Our own phylum, the vertebrates, exhibits internal segmentation of some structures, such as reiterated ribs/vertebrae and muscles. Modern molecular phylogenies have revealed that these three phyla are not closely related to one another, each originating from a different early branch of the animal tree, and each more closely related to non-segmented phyla. This raises the question of whether body segmentation was an ancient ancestral trait that has been lost in many animal lineages, or a highly successful body design that has evolved independently multiple times. Either way, understanding the origin and evolution of animal segmentation is crucial for understanding the direction of evolutionary change in body plans in most animal lineages.

Two quite distinct paradigms for how body segments form have been described. The first is based on studies of model vertebrate embryos, such as zebrafish, chick and mouse. In vertebrates, the blocks of cells that later give rise to vertebrae/ribs, called somites, form sequentially in an anterior-to-posterior progression from an undifferentiated field of cells (for details see the review by Oates et al., 2012). The formation of somites occurs under the control of a complex developmental genetic network that includes around 40-100 genes that exhibit oscillatory expression. Each coordinated burst of expression of these genes helps give rise to one somite. This oscillating gene network is called the vertebrate ‘segmentation clock’. The second paradigm for segmentation is based on work on the arthropod fruit fly Drosophila melanogaster. Drosophila differs from vertebrates in that all segments form more-or-less simultaneously. Simultaneous segmentation occurs under the control of a cascade of genes that gradually divide the embryo into smaller and smaller units, eventually evenly sized segments (for details see Peel et al., 2005).

Such striking differences in the developmental mechanisms underlying the formation of body segments would seem to suggest that segmentation in arthropods and vertebrates evolved independently. However, the Drosophila mode of segmentation is not shared by all insects, or by other arthropod clades such as the myriapods (i.e. centipedes, millipedes) and chelicerates (e.g. spiders, scorpions, mites etc.) (see Peel et al., 2005). Ancestrally, arthropods formed their trunk segments sequentially in an analogous fashion to vertebrate somites, and many extant species of insect have retained this ancestral developmental trait. One such insect is the red flour beetle Tribolium castaneum. Recently, in collaboration with Andrés Sarrazin and Michalis Averof, I have shown that the formation of trunk segments in Tribolium occurs under the control of a segmentation clock (see Sarrazin, Peel & Averof, 2012, and the related review by Richmond and Oates, 2012). So far, we have only identified two genes that are definitely involved in this segmentation clock, and so it is too early to say how similar the arthropod and vertebrate segmentation clocks might be, and whether they were inherited from the arthropod/vertebrate common ancestor that lived over 550 million years ago.

I’d welcome applications from individuals interested in examining the mechanistic basis to the arthropod segmentation clock, using Tribolium as a laboratory model, with the aim of improving our understanding of the evolution of segmented animal body plans.