Evolution and development of insect wings: A comparative analysis of the genome wide targets of the Hox protein Ultrabithorax in Bombyx mori, Apis mellifera and Drosophila melanogaster.

Abstract

Insects are the first animals to have acquired flight during evolution. They represent the largest order with abundant species diversity in the animal kingdom. The variety in body forms is also evident in the flight appendages of the various different insect groups, which have remarkable diversity in the number and size of wings. Most insects have four wings, while beetles and flies have only one pair of wings. In beetles, the forewings are modified as thick protective cover called elytra and only hind-wings perform the flight function. In contrast, in flies only the forewings perform the flight function, while the hind-wings are modified to a small club-shaped balancing organ called haltere. Except in few early insect groups, they all show differences between forewing and hindwing morphology. The insect body is divided into segments in which the development and fate of different organs is mainly controlled by a set of master control genes of the Hox complex. The Hox genes are highly conserved across the animal kingdom and are the main players in generating morphological diversity along with body axis within an organism. Suppression of wing fate and specification of haltere fate in Drosophila melanogaster by the Hox gene Ultrabithorax (Ubx) is a classic example of Hox regulation of serial homology, which has served as a paradigm for understanding Hox gene function. The differential development of wing and haltere constitutes a good genetic system to study cell fate determination at different levels such as growth, cell shape, size and its biochemical and physiological properties. They also represent the evolutionary trend that has established the differences between fore and hindwings in insects Ubx, which is required to specify haltere development in Drosophila, is expressed in T3 segments during development of all insects studied so far. Furthermore, the Ubx protein itself has not evolved amongst the diverse insect groups, although there are significant differences in Ubx sequences between Drosophila and crustacean Arthropods. Interestingly, over-expression of Ubx from these organisms in T2 segment lead to wing to haltere transformations in Drosophila. This suggests that in the dipteran lineage, certain wing patterning genes may have come under the regulation of Ubx. We have identified targets of Ubx in the hindwing of Bombyx (lepidoptera) and then a comparative analysis was done with targets in Drosophila (diptera) and Apis (hymenoptera) in an attempt to understand the insect appendage diversity. We have observed that Ubx targets in all the three insects share similar biological functions in comparable proportions. Wing related genes are enriched among Ubx targets, and a comparison suggests that Bombyx is more diverged from Apis than Drosophila. These targets, however, do not show differential expression in the fore and the hind wing in Bombyx as opposed to wing and haltere in Drosophila. We are exploring the possibility that diversity in morphology in insect wings may be at the level of evolutionary changes in regulatory sequences of these targets. The comparative analysis of the targets of Ubx in different insects will allow us to understand the developmental mechanisms and the evolutionary path that has led to the modification of an ancestral wing to a dipteran haltere.