The role of the Hox genes in the development and evolution of insect wings

The diversification of appendages has played a critical role in animal evolution, but the genetic mechanisms underlying the changes in these structures are poorly understood. One way to analyze how homologous appendages have become different is through the study of the developmental regulation of insect wings. The role of the homeotic (Hox) genes in regulating pattern along the anteroposterior axis of many animals suggests that they may be involved in the specification of appendage identity. The genes controlling the formation and development of the Drosophila forewing (wing) and hindwing (haltere) were investigated to identify the role of the Hox genes in the specification of their unique identities. The Hox genes are not required for wing and haltere formation but they regulate the position of these structures along the trunk by repression of the wing program outside of the meso- and metathoracic segments. Further, the wing develops without Hox gene input while the Ultrabithorax (Ubx) Hox gene represses a number of genes in the wing developmental hierarchy to shape the haltere. Ubx is also expressed in, and specifies the identity of, hindwings in another insect (Lepidoptera: Precis coenia). Ubx target genes identified in Drosophila are not regulated by Ubx in the hindwings of this species. Thus, it appears that wings first arose in insects without any Hox gene input and that wing formation then fell under the negative control of individual Hox genes at different stages of pterygote evolution resulting in the two pairs of wings present in the modern body plan. Ubx also acts after flight appendage formation and controls genes at many levels of regulatory hierarchies to make hindwings different from forewings. The diversification of hindwings among insect species has involved the acquisition of specific sets of target genes by Ubx in different lineages. Changes in Hox-regulated target sets are likely to underlie the morphological divergence of other sets of homologous structures between animals.