Reverse homeosis in homeotically reconstructed ribbonworms

Homeosis is the replacement of one body part by another, which may be caused by either developmental or genetic variations. It is particularly obvious in segmented animals, like insects, in which one body segment may be transformed into another. However, homeosis also occurs in animals without overt segmentation that also have detailed positional information specifying their body plan. By grafting, we have artificially generated homeotic ribbonworms of the species Lineus ruber with a duplicated ocellar region replacing the postocellar region anterior to the brain. Such chimeric animals are capable of complete morphogenetic regulation of the anterior–posterior (A–P) pattern. The missing postocellar region is restored by intercalary regeneration, and the anterior duplicated ocellar region is eliminated by a process called transgeneration. Thus, homeosis is reversed, and a completely normal pattern along the A–P axis is restored. This reverse homeosis involves the elimination of the syngeneic eyes and the survival of the grafted allogeneic eye region. LsPax-6, the Lineus sanguineus ortholog of the mammalian Pax-6 gene, which is considered to be a master control gene for eye morphogenesis, is expressed specifically in regenerating, regenerated, and intact eye regions. Our data show that ribbonworm eyes are either maintained or they regress according to their position along the A–P axis, even though there are no obvious segmental boundaries. This system allows us to test the function of LsPax-6 protein not only during eye regeneration but also during maintenance and regression of the eyes.