The molecular genetics of head development in Drosophila melanogaster

‘It would be too bad if the question of head segmentation ever should be finally settled; it has been for so long such fertile ground for theorizing that arthropodists would miss it as a field for mental exercise’. Snodgrass, 1960 (cited by Rempel, 1975)The development of the Drosophila embryo has provided an excellent model system for the analysis of embryonic pattern formation. In little more than a decade, many of the elements of the molecular genetic cascade underlying early development have been identified. However, these studies have focused primarily on the development of the central, overtly segmented region of the fruitfly embryo. As the influential insect morphologist R. E. Snodgrass pointed out, understanding of the formation of the complex embryonic head region has advanced quite slowly. Recently, however, substantial progress has been made in the identification and analysis of the genes determining head development. These studies are generating increasing hope that both the structure of the head and how it is formed will soon be significantly clearer. What is perhaps most interesting is that there are already a number of hints that the rules governing head formation may differ from the paradigm established for the central region of the embryo.In this review, we will focus on the process of embryonic head development in Drosophila melanogaster. First, we will describe the evolution of the head, its formation, and some of the difficulties involved in analyzing its structure. We will then discuss what has been learned about the genes responsible for embryonic head development. Finally, the implications of this molecular genetic data for models of head development will be explored.The dipteran Drosophila embryo is one of the most highly evolved of the arthropod embryos. Arthropods, annelids, and other members of the articulate group (see Fig. 1) all show marked similarities in body plan. Most obviously, both arthropods and annelids are metameric in structure, consisting of a series of segmental units. An early definition of a metameric unit was proposed by Snodgrass (1935) as simply a body division of the embryo. This definition, however, was rather crude and was later supplanted by a series of more precise criteria. Rempel (1975), for example, summarized the attributes of a metamere as: (1) a pair of mesodermal somites (which give rise to the muscles) (2) a pair of appendages (3) a pair of apodemes (inner projections of the ectoderm which form muscle attachment sites) and (4) a neuromere (which produces a ganglion and its associated lateral nerves). Although these characteristics are easily recognizable in the metameres of most annelids, in many arthropod segments they are often less evident. In particular regions of arachnids and crustaceans, for example, metamerism is quite difficult to detect. This loss of segmental attributes (which as we shall see is an important issue in Drosophila head development) has occurred in several ways. In a number of cases, particular segments have been lost or fused together during evolution. In various species, segmental appendages are greatly reduced and apodemes and neuromeres difficult to discern.In addition to a metameric body plan, both arthropods and annelids have other similarities in general body structure. Both groups have dorsal hearts and related nervous systems, consisting of an anterior, dorsally located brain and a ventral nerve cord formed of a series of ganglia. Because of these structural similarities, present day articulates are thought to have evolved from a primitive annelid-like organism (see Fig. 1 and, for example, Anderson, 1973). This hypothesized ancestor consisted of an array of metameric units, which showed little evidence of functional or structural specialization. These metameres, as in present-day annelids, were likely to have been generated sequentially from a central growth zone. The ends of this animal were primitive non-segmented structures. The anterior end was probably most similar to the anterior ‘prostomial’ region of modem annelids, housing a simple brain (archicerebrum). This ‘head’ area was involved in sensory and feeding functions. The posterior ‘tail’ region most likely consisted of a nonsegmented area surrounding the anal opening.The evolutionary process of head formation involved the progressive incorporation of structures into the head region (see Fig. 2). In animals even more primitive than the annelids (e.g. the Platyhelminthes), there is already an increasing concentration of sensory and feeding structures (eyes, ganglia and tentacles) in the anterior region. A critical step in this process of ‘cephalization’ occurred when several of the anterior-most trunk segments became incorporated into the beginnings of a clearly recognizable head region. This process is already evident in certain annelid embryos (e.g. the polychaete Nereis) in which the head includes regions called the prostomium (anterior to the mouth opening) and the peristomium (surrounding the mouth). Although the precise origin of the peristomium is unclear, it is generally thought to include one or more former trunk segments. One piece of evidence for this is that the peristomium contains pairs of cirri, which are likely the remnants of the parapodia, the appendages present on annelid trunk metameres. Cephalization continued as evolution proceeded and is evident in present-day myriapods (centipedes and millipedes). The insect head, consisting of an asegmental terminal region and cephalized trunk segments, first appeared in primitive form during the Devonian period (Smart and Hughes, 1972). However, because of the scarcity of fossil material from this period, its structural form has been deduced largely through the comparative analysis of more recent species.As cephalization occurred, several of the anterior-most trunk segments shifted forward, so that they came to lie in of the mouth These segments became and of more example, the and anterior of the it to an important sensory The of the head is often to as the is in this region that segmental are most difficult to the mouth is the of the head as the In this cephalized trunk segments have for feeding functions. As evolution the trunk segments became into and clearly functional the embryo to the complex Drosophila body the Drosophila of this process of head has been the evolution of a series of complex which during of development. this a series of complex (which will be in the posterior anal region and of understanding of the process of head formation from the studies of and the of the embryo is and segmental are clearly and In the head a series of be identified. 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