The development of a long, coiled, optic nerve in the stalk-eyed fly Cyrtodiopsis whitei

Abstract

In the stalk-eyed fly Cyrtodiopsis whitei (Diopsidae; Diptera), the relatively long optic nerve develops within the tight lumen of a very short eyestalk. Axonal growth is generally considered in terms of path finding, selective fasciculation, and towing. Physical forces that are necessary for axon lengthening are generated either by the growth cone or by the growth of surrounding tissues. Therefore, it is surprising to encounter a loosely coiled nerve apparently lacking any attachments that could allow for pull, or towing, of the nerve. In this study, we used histological sections and whole-mount preparations to confirm that the optic nerve of the stalk-eyed fly indeed elongates without the external application of tension to the nerve. Secondly, we examined the distribution of cytoskeletal elements and selected proteins that may be involved in axon extension. Staining against the vesicle fusion proteins SNAP-24 and SNAP-25 consistently results in stronger staining in the rapidly extending optic nerve than in a control nerve, suggesting a possible role of these proteins in the extension process. On a gross morphological level, SNAP-24/25 as well as the cytoskeletal elements actin and tubulin are uniformly distributed throughout the lengths of the growing nerve, suggesting that nerve elongation is distributed rather than localized. Finally, we identified glia as a possible source for tension within the nerve bundle. Glia proliferate rapidly in the optic nerve but not in the control nerve. Much work continues to focus on the growth of axons in culture, but this study is one of the few that considers the dynamics of nerve bundle extension as a whole.

Stalk‐eyed flies (Diopsidae): Modelling the evolution and development of an exaggerated sexual trait

“…(34) A further complication to consider is how placement of the eyes and antennae on the end of long stalks affects neural development. (40,41) For example, how is the growth of the optic nerve connecting the photoreceptors of the eye to the visual centres of the brain coordinated? Further work is clearly needed to characterise the morphogenetic movements involved in disc eversion and differentiation in Drosophila and in stalk-eyed flies.…”

Proximal fate marker homothorax marks the lateral extension of stalk‐eyed fly Cyrtodopsis whitei

“…To do this, we looked into the imaginal development of the stalk‐eyed flies and compared it to that of Drosophila . It has been reported that the stalk‐eye like pattern results from the extension of the optic vesicle (Buschbeck et al, ; Buschbeck & Hoy, ). It is interesting how this optic vesicle extension and lateral extension from the head contribute toward the generation of final stalk eye phenotype.…”

“…Most flies have characteristic compound eyes and antennae on their head, but the stalk‐eyed flies have their eye located at the end of long lateral extension, or stalks. Unlike other stalk‐eye flies where only the eye is located on the stalk, the stalk‐eyed fly from the Diopsidae family have the antenna, eye and optic lobe located at the end of the stalk (Buschbeck & Hoy, ; Buschbeck, Roosevelt, & Hoy, ). The “stalk‐eyed” morphology is a dramatic deviation from other dipterans, including Drosophila (Buschbeck & Hoy, ).…”

<b>Taxonomic status and additional description of White’s Stalked-eyed Fly <I>Cyrtodiopsis whitei</I> (Curran, 1936) (Diptera: Diopsidae) from India with a key to the allied species and note on its habitat</b>

“…It is, therefore, doubtful if the Malaysian specimens are really C. whitei. Extensive uses of laboratory-reared C. whitei in behavioral (Lorch et al 1993;Wilkinson et al 1998;Al-Khairulla et al 2003), physiological (Burkhardt & de la Motte 1983;Buschbeck & Hoy 2005) and genetic studies (Wilkinson et al 1997;Wilkinson & Sanchez 2001) has made this species name well known as an experimental object for molecular and behavioral studies of stalked-eyed flies in general.…”