Number, identity, and sequence of the Drosophila head segments as revealed by neural elements and their deletion patterns in mutants.

Abstract

The development of the insect head tagma involves massive rearrangements and secondary fusions of segment anlagen during embryogenesis. Due to the lack of reliable morphological markers, the number, identity, and sequence of the head segments, particularly in the pregnathal region, are still a matter of ongoing debates. We examined the complex array of internal structures of the embryonic Drosophila melanogaster head such as the sensory structures and nerves of the peripheral and stomatogastric nervous systems, and we used embryonic head mutations causing a lack of overlapping segment anlagen to unravel the segmental identity and the sequence of the neural elements. Our results provide evidence for seven distinct segments in the Drosophila head, each characterized by a specific set of sensory neurons, consistent with the proposal that insects, myriapods, and crustaceans share a monophyletic evolutionary tree from a common annelid-like ancestor.The insect body is composed of metamerically repeated units. While segmentation is obvious in the "trunk" region, the segmental organization of the head is still obscure (1-7). By distinct cuticular features, three gnathal segments (mandibula, maxilla, and labium) can be distinguished in the posterior head region. The anterior pregnathal region, however, is poor in diagnostic morphological structures (8). Morphological and evolutionary studies based on epidermal head structures (5, 8), coelomic cavities, or brain regions (1-4) have so far failed to unambiguously determine the number and identity of pregnathal segments in the insect head. Due to the evolutionary changes that resulted in the "acephalic" appearance of higher dipteran larvae, the segmental composition of the Drosophila head was analyzed only recently. The detailed fate map analysis of a few cuticular specializations of the larval Drosophila head by laser ablation studies suggested six segments-i.e., three pregnathal and three gnathal segments (5). This interpretation was questioned through a detailed analysis of the expression patterns of the segment polarity genes engrailed (en) and wingless (wg), which serve as molecular markers for metamers in the prospective trunk and gnathal regions of the Drosophila embryo. This analysis suggested the possibility of seven instead of only six head segments (7). Here we present additional and more substantial evidence for seven head segments which is based on detailed analysis of internal head structures such as sensory organs. Their axons fasciculate to give rise to seven distinct sensory projections to the brain. The analysis of the patterns of sense organs deleted in various head segmentation mutants allows us to make an assignment of the sense organs to their segments of origin.MATERIALS AND METHODS Drosophila melanogaster strains were kept under standard conditions; wild-type and mutant embryos were obtained as described (9). The en expression patterns of embryos lacking tor activity (collected from homozygous torPM females) (10, 11) and of embryos homozygous ...

Molecular markers for identified neuroblasts in the developing brain ofDrosophila

“…Accordingly, ems mutants show defects in the intercalary, antennal (Hirth et al, 1995;Younossi-Hartenstein et al, 1997), and the ocular segment (e.g. the en hs is missing) (Schmidt-Ott et al, 1994). Considering that ems is expressed in only a few trito-and deutocerebral NBs it is remarkable that ems mutants show a deletion of the tritoand deutocerebrum (Hirth et al, 1995).…”

Head patterning and Hox gene expression in an onychophoran and its implications for the arthropod head problem

“…Is it an appendage or structure of a pre ocular segment (Posnien et al, 2009;Schmidt-Ott et al, 1994;Schmidt-Ott and Technau, 1992), the ocular segment (Budd, 2002;Eriksson and Budd, 2000;Eriksson et al, 2003) and homologous to the great appendage or primary antenna of certain fossil stem-group arthropods (Budd, 2002;Scholtz and Edgecombe, 2005) or a limb belonging to a segment placed further posterior (Haas et al, 2001a;Haas et al, 2001b). There have been suggestions that the antenna of the onychophorans corresponds to the labrum of arthropods (Budd, 2002;Eriksson and Budd, 2000;Eriksson et al, 2003).…”

Ems and Nkx6 are central regulators in dorsoventral patterning of the Drosophila brain

“…This novel function is surprising because ems has hitherto been exclusively connected with patterning functions along the AP axis. It has been proposed that the combined activities of the gap genes ems, buttonhead and orthodenticle (ocelliless -FlyBase) generate head segments (Cohen and Jürgens, 1990;Grossniklaus et al, 1994) and that ems mutants exhibit defects in the formation of the intercalary and antennal segment (Cohen and Jürgens, 1990;Schmidt-Ott et al, 1994) as well as in the corresponding TC and DC (Hirth et al, 1995;YounossiHartenstein et al, 1997) in accordance with the early pattern of ems expression (Dalton et al, 1989;Walldorf and Gehring, 1992;Urbach and Technau, 2003b). ems probably also has a homeotic function in specifying aspects of intercalary segment identity (Schöck et al, 2000).…”