Eye stalks or no eye stalks: a structural comparison of pupal development in the stalk-eyed fly Cyrtodiopsis and in Drosophila.

After emergence from the puparium, stalk-eyed flies of the family Diopsidae rapidly expand their head capsule so that the eyes and optic lobes are displaced at the ends of stalks that extend from the central head. Because the expansion takes place in only 15 minutes, we are especially interested in ontogenetic modifications that may facilitate such a rapid and dramatic change. To examine the pupal development of the brain, we used Bodian staining in the stalk-eyed fly, Cyrtodiopsis whitei and compared it with development in the fruit fly, Drosophila melanogaster, which serves as a "typical" dipteran example without eye stalks. Early in pupal development, the neuropil organization of the two species is fairly similar. In both species, columns are present in the outer medulla and giant fibers are discernible in the lobula plate. In contrast to D. melanogaster, C. whitei shows a small, neck-like constriction between the optic lobes and the rest of the brain. By 20% of pupal development, the divergence is more apparent, and by 30%, the future eye stalk and optic nerve of C. whitei has started to form. During the remaining 70% of development, the initially thick optic nerve narrows, and becomes gradually elongated, eventually coiling and folding throughout the short eye stalk. Similarly, the cuticle of the surrounding region becomes constricted, slightly elongated, and gradually appears more and more densely corrugated, like an accordion bellows. However, except for the formation of the optic nerve, the dense aggregation of cuticle around it, and a shift in orientation of the neuropils, the developmental programs of the two species are remarkably similar. This suggests that only a few aspects of development have been modified during the course of evolution to generate the stalk-eyed phenotype. At eclosion, the imago of C. whitei goes through a pumping process to inflate the eye stalks to their full length. Measurements of the diameter of the optic nerve before and after the expansion reveal only a small decrease. We propose that the cuticular folding of the eye stalk as well as the coiling of the optic nerve prepare the pupa well for the rapid and dramatic eye-stalk inflation after eclosion.