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Li and PopadicŁmandibles. However, in insects with piercing and suckingmouthparts, such as milkweed bugs, pb expression is mainlydetected in the labial appendages (Rogers and Kaufman1997). Thus, it has been proposed that loss of pb expression inthe maxillae was responsible for the transformation of themandibulate to the haustellate mouth type (Rogers et al.2002). More specifically, the loss of pb expression in milkweedbug embryos would ‘‘free’’ the maxillary appendages todiverge from their original labium-like phenotype. However,such change in pb regulation cannot account for thedevelopment of stylets in both maxillary and mandibularsegments. This suggests that other nonhomeotic genes areinvolved in the latter process.Consistent with the morphological diversification of headappendages, the sharpest difference of nub expression isobserved in this region. Patterns of expression show acoordinated change in association with particular mouthpartmorphology. In firebrat and cockroach embryos, which havetypical mandibulate mouthparts, nub is localized in themaxillary and labial appendages in a similar pattern (Fig.6B). This is particularly pronounced in Periplaneta embryos,which exhibit highly coordinated patterns of expression in thelabium and maxillae from early to late development. Such anobservation is consistent with the fact that these segments arestructurally very similar and differ from the mandibularsegment. Second, nub is generally not expressed in themandibles except locally and transiently in cockroaches(Fig. 6B). This suggests that in insects with biting andchewing mouthparts, mandibles were originally devoid of nubexpression.In milkweed bug embryos, which have the stylate–haustellate (sucking) mouthparts, nub is expressed in a verydifferent pattern. First, there is novel expression along themid-ventral region of the mandibular appendages. Second,this mandibular expression is similar to the maxillary pattern(Fig. 6B). Expression in the labium, however, is localized onlyin the distal portion of the appendage and exhibits acompletely different timing and pattern. This differentialexpression correlates with a change in the morphology of themaxillary and labial segments that is characteristic forpiercing and sucking mouthparts: Development and morphologyof the maxillary segment parallels that of themandibular segment. These observations provide the firstnonhomeotic gene example of a linkage between a change inexpression pattern and a corresponding change in themorphology of insect mouthparts. They also provide a strongindication that nub may function in the development ofhaustellate mouthparts.The emerging insight from this and other recent studiessuggests that the evolution of the maxillae and mandibles inOncopeltus and other hemipterans was governed by regulatorychanges at both higher (Hox genes such as pb and Dfd)and lower levels (genes such as nub) in the developmentalhierarchy. This underlines the critical importance of understandingthe functional roles and relationships between thesetwo classes of genes. For example, Dfd is expressed in themandibular segments in both Tribolium (which has mandibulatemouthparts) and in Oncopeltus (which has haustellatemouthparts). Functional studies have shown that in theabsence of Dfd, mandibles are transformed into antenna-likeappendages in these two insects (Brown et al. 2000; Hughesand Kaufman 2000). These findings show that Dfd orthologscontrol mandibular identity in both species. Yet the actualmorphology of mandibles in Tribolium and Oncopeltus is verydifferent, a result of distinct mandibulate and haustellatemodifications. Additional factors, either acting in parallelwith Dfd, or downstream targets, or independently of Dfd,must be involved in the establishment of these distinctmandibular morphologies. Based on this analysis of itsexpression patterns, nub is a good candidate for being sucha target gene in the mandibular segment (Fig. 6B). Furtherstudies of other genes at lower levels in the developmentalhierarchy will be necessary to fully understand the mechanismsunderlying the morphological diversification of insectmouthparts.AcknowledgmentsWe thank E. M. Golenberg for critical reading of the manuscript. Wealso thank two anonymous reviewers whose comments and expertisewere very helpful. This work was in part supported by NIH grantGM071927 to A. P.REFERENCESEvolution of nub expression in insects 323Abzhanov, A., and Kaufman, T. C. 2000. Homologs of Drosophilaappendage genes in the patterning of arthropod limbs. Dev. Biol. 227:673–689.Anderson, M. G., Perkins, G. L., Chittick, P., Shrigley, R. J., and Johnson,W. A. 1995. drifter, aDrosophila POU-domain transcription factor, isrequired for correct differentiation and migration of tracheal cells andmidline glia. 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