Most of our knowledge about the mechanisms of segmentation in arthropods comes from work on Drosophila melanogaster. In recent years it has become clear that this mechanism is far from universal, and different arthropod groups have distinct modes of segmentation that operate through divergent genetic mechanisms. We review recent data from a range of arthropods, identifying which features of the D. melanogaster segmentation cascade are present in the different groups, and discuss the evolutionary implications of their conserved and divergent aspects. A model is emerging, although slowly, for the way that arthropod segmentation mechanisms have evolved.

Vertebrate segmentation relies on a mechanism characterized by oscillating gene expression. Whether this mechanism is used by other segmented animals has been controversial. Rigorous proof of cyclic expression during arthropod segmentation has been lacking. We find that the segmentation gene odd-skipped (Tc-odd) oscillates with a two-segment periodicity in the beetle Tribolium castaneum. By bisecting embryos and culturing the two halves over different time intervals, we demonstrate that Tc-odd cycles with a period of about 95 minutes at 30°C. Using live imaging and cell tracking in green fluorescent protein-expressing embryos, we can exclude that cell movements explain this dynamic expression. Our results show that molecular oscillators represent a common feature of segmentation in divergent animals and help reconcile the contrasting paradigms of insect and vertebrate segmentation.

There is now compelling evidence that many arthropods pattern their segments using a clock-and-wavefront mechanism, analogous to that operating during vertebrate somitogenesis. In this Review, we discuss how the arthropod segmentation clock generates a repeating sequence of pair-rule gene expression, and how this is converted into a segment-polarity pattern by 'timing factor' wavefronts associated with axial extension. We argue that the gene regulatory network that patterns segments may be relatively conserved, although the timing of segmentation varies widely, and doublesegment periodicity appears to have evolved at least twice. Finally, we describe how the repeated evolution of a simultaneous (Drosophila-like) mode of segmentation within holometabolan insects can be explained by heterochronic shifts in timing factor expression plus extensive pre-patterning of the pair-rule genes.

Summary The eggs of insects are unusual in that they often have clear bilateral symmetry when they are laid, indicating that both anterior-posterior (AP) and dorsal-ventral (DV) symmetry is broken during oogenesis[1]. The molecular basis of this process is well understood in the fly Drosophila melanogaster, where symmetry breaking events for both axes depend on the asymmetric position of the oocyte nucleus and on germline-soma signaling mediated by the Tgfα-like EGF ligand Gurken [2, 3]. Germline-soma signaling interactions centered around the oocyte nucleus have been proposed in other insect species[4, 5], but the molecular nature of these interactions had not been elucidated. We have examined the behavior of the oocyte nucleus, and the expression, activity, and function of EGF signaling components in the ovaries of the wasp Nasonia vitripennis, the beetle Tribolium castaneum, and the cricket Gryllus bimaculatus. We have found that EGF signaling has broadly conserved roles in mediating the encapsulation of oocytes by the somatic follicle cell layer, in establishing polarity of the egg chambers, and, at least in the Holometabola, in setting up the DV axis of the embryo. These results provide insights into the evolutionary origins of the unique strategy employed by insects to establish embryonic axial polarity during oogenesis.

Long-germ insects, such as the fruit fly Drosophila melanogaster, pattern their segments simultaneously, whereas short-germ insects, such as the beetle Tribolium castaneum, pattern their segments sequentially, from anterior to posterior. Although the two modes of segmentation at first appear quite distinct, much of this difference might simply reflect developmental heterochrony. We now show here that, in both Drosophila and Tribolium, segment patterning occurs within a common framework of sequential Caudal, Dichaete and Odd-paired expression. In Drosophila, these transcription factors are expressed like simple timers within the blastoderm, whereas in Tribolium they form wavefronts that sweep from anterior to posterior across the germband. In Drosophila, all three are known to regulate pair-rule gene expression and influence the temporal progression of segmentation. We propose that these regulatory roles are conserved in short-germ embryos, and that therefore the changing expression profiles of these genes across insects provide a mechanistic explanation for observed differences in the timing of segmentation. In support of this hypothesis, we demonstrate that Odd-paired is essential for segmentation in Tribolium, contrary to previous reports.