The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes

Rogers, Bryan T.; Peterson, A.; Kaufman, Thomas C.

doi:10.1046/j.1525-142x.2002.01065.x

Cited by 83 publications

(75 citation statements)

References 41 publications

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“…Selector genes encode transcription factors that, in combinations, define the body plan by controlling the development of specific regions of the embryo, and have been implicated in the evolution of body plan variations (Averof and Akam, 1995;Carroll et al, 2001;Duboule, 1994;Gellon and McGinnis, 1998;Manak and Scott, 1994;Panganiban et al, 1995;Rogers et al, 2002;Warren et al, 1994). In insects, selector genes are thought to modify the development of a default, or 'ground state', appendage into a tagma-specific appendage such as a mouthpart, antenna or leg.…”

Section: Introductionmentioning

confidence: 99%

Functional analyses oftiptopandAntennapediain the embryonic development ofOncopeltus fasciatussuggests an evolutionary pathway from ground state to insect legs

2005

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In insects, selector genes are thought to modify the development of a default, or `ground state', appendage into a tagma-specific appendage such as a mouthpart, antenna or leg. In the best described example, Drosophila melanogaster, the primary determination of leg identity is thought to result from regulatory interactions between the Hox genes and the antennal-specifying gene homothorax. Based on RNA-interference, a functional analysis of the selector gene tiptop and the Hox gene Antennapedia in Oncopeltus fasciatus embryogenesis is presented. It is shown that, in O. fasciatus, tiptop is required for the segmentation of distal leg segments and is required to specify the identity of the leg. The distal portions of legs with reduced tiptopdevelop like antennae. Thus, tiptop can act as a regulatory switch that chooses between antennal and leg identity. By contrast, Antennapedia does not act as a switch between leg and antennal identity. This observation suggests a significant difference in the mechanism of leg specification between O. fasciatus and D. melanogaster. These observations also suggest a significant plasticity in the mechanism of leg specification during insect evolution that is greater than would have been expected based on strictly morphological or molecular comparisons. Finally, it is proposed that a tiptop-like activity is a likely component of an ancestral leg specification mechanism. Incorporating a tiptop-like activity into a model of the leg-specification mechanism explains several mutant phenotypes, previously described in D. melanogaster, and suggests a mechanism for the evolution of legs from a ground state.

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Section: Introductionmentioning

confidence: 99%

Functional analyses oftiptopandAntennapediain the embryonic development ofOncopeltus fasciatussuggests an evolutionary pathway from ground state to insect legs

2005

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“…Finally, both mRNA expression and functional analyses in Oncopeltus (Hughes and Kaufman, 2000;Rogers et al, 1997;Rogers et al, 2002) have shown that Scr governs the formation of the sex combs on the distal tibia of the T1 leg (Fig. 3F inset, top).…”

Section: Scr Patterning In the T1 Leg Is Very Dynamic And Characterizmentioning

confidence: 93%

“…Numerous studies have shown that changes in the expression and function of homeotic (hox) genes were pivotal in the evolution of the insect bauplan (Beeman et al, 1993;Beeman et al, 1989;Carroll et al, 2001;Hughes and Kaufman, 2000;Hughes and Kaufman, 2002;Mahfooz et al, 2007;Mahfooz et al, 2004;Rogers et al, 1997;Rogers et al, 2002;Struhl, 1982;Tomoyasu et al, 2005). This insight was primarily based on mRNA expression patterns, however, data on protein accumulation are much more limited.…”

Section: Introductionmentioning

confidence: 99%

“…In insects, Scr functions in two distinct body regions, the head and the thorax. Previous insights from mRNA expression and functional studies have indicated that this gene is crucial in establishing the identity of the labial segment, suppressing wing formation on the prothorax (T1), and directing the development of T1 leg combs (Beeman et al, 1993;Beeman et al, 1989;Curtis et al, 2001;Hughes and Kaufman, 2000;Rogers et al, 1997;Rogers et al, 2002;Shippy et al, 2006). The data on protein expression in two model systems (Drosophila and Tribolium) show that, in general, mRNA patterns closely coincide with the protein pattern (Curtis et al, 2001;Mahaffey and Kaufman, 1987).…”

Section: Introductionmentioning

confidence: 99%

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Evolving expression patterns of the homeotic gene Scr in insects

et al. 2010

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While the mRNA expression patterns of homeotic genes have been examined in numerous arthropod species, data on their protein accumulation is extremely limited. To address this gap, we analyzed the protein expression pattern of the hox gene Sex combs reduced (Scr) in six hemimetabolous insects from four divergent orders (Thysanura, Orthoptera, Dictyoptera and Hemiptera). Our comparative analysis reveals that the original domain of SCR expression was likely confined to the head and then subsequently moved into the prothorax (T1) in winged insect lineages. The data also show a trend toward the posteriorization of the anterior boundary of SCR expression in the head, which starts in the mandibles (Thysanura) and then gradually shifts to the maxillary (Orthoptera) and labial segments (Dictyoptera and Hemiptera), respectively. In Thermobia (firebrat) and Oncopeltus (milkweed bug) we also identify instances where SCR protein is not detected in regions where mRNA is expressed. This finding suggests the presence of a posttranscriptional regulatory mechanism of Scr in these species. Finally, we show that SCR expression in insect T1 legs is highly variable and exhibits divergent patterning even among related species. In addition, signal in the prothoracic legs of more basal insect lineages cannot be associated with any T1 specific features, indicating that the acquisition of SCR in this region preceded any apparent gain of function. Overall, our results show that Scr expression has diverged considerably among hemimetabolous lineages and establish a framework for subsequent analyses to determine its role in the evolution of the insect head and prothorax.

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“…First, we test the hypothesis that the main axis of the adult maxillary and labial appendages is patterned using genes also required in the leg development network. Key aspects of this network are conserved in the legs of numerous arthropods, suggesting that they were likely components of the leg patterning network of ancestral arthropods (e.g., Palopoli and Patel 1998;Abzhanov and Kaufman 2000;Jockusch et al 2000;Beermann et al 2001;Schoppmeier and Damen 2001;Inoue et al 2002;Rogers et al 2002;Angelini and Kaufman 2005b;Prpic and Damen 2009;Angelini et al 2012). Second, we test several hypotheses about the mechanism that governs branching of the PD axis to give rise to endites.…”

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confidence: 97%

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

et al. 2012

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Specialized insect mouthparts, such as those of Drosophila, are derived from an ancestral mandibulate state, but little is known about the developmental genetics of mandibulate mouthparts. Here, we study the metamorphic patterning of mandibulate mouthparts of the beetle Tribolium castaneum, using RNA interference to deplete the expression of 13 genes involved in mouthpart patterning. These data were used to test three hypotheses related to mouthpart development and evolution. First, we tested the prediction that maxillary and labial palps are patterned using conserved components of the leg-patterning network. This hypothesis was strongly supported: depletion of Distal-less and dachshund led to distal and intermediate deletions of these structures while depletion of homothorax led to homeotic transformation of the proximal maxilla and labium, joint formation required the action of Notch signaling components and odd-skipped paralogs, and distal growth and patterning required epidermal growth factor (EGF) signaling. Additionally, depletion of abrupt or pdm/nubbin caused fusions of palp segments. Second, we tested hypotheses for how adult endites, the inner branches of the maxillary and labial appendages, are formed at metamorphosis. Our data reveal that Distal-less, Notch signaling components, and odd-skipped paralogs, but not dachshund, are required for metamorphosis of the maxillary endites. Endite development thus requires components of the limb proximal-distal axis patterning and joint segmentation networks. Finally, adult mandible development is considered in light of the gnathobasic hypothesis. Interestingly, while EGF activity is required for distal, but not proximal, patterning of other appendages, it is required for normal metamorphic growth of the mandibles.

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The development and evolution of insect mouthparts as revealed by the expression patterns of gnathocephalic genes

Cited by 83 publications

References 41 publications

Functional analyses oftiptopandAntennapediain the embryonic development ofOncopeltus fasciatussuggests an evolutionary pathway from ground state to insect legs

Functional analyses oftiptopandAntennapediain the embryonic development ofOncopeltus fasciatussuggests an evolutionary pathway from ground state to insect legs

Evolving expression patterns of the homeotic gene Scr in insects

Patterning of the Adult Mandibulate Mouthparts in the Red Flour Beetle, Tribolium castaneum

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