Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects

Angelini, David R.

doi:10.1016/j.ydbio.2004.04.005

Cited by 106 publications

(105 citation statements)

References 42 publications

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“…Among hemimetabolous insects, in the cricket G. bimaculatus, parental RNAi-mediated knockdown of hth resulted in similar transformation of all cephalic appendages towards leg identity in some embryos, and comparable fusion of adjacent segments in stronger phenotypes [26]. In parental RNAi experiments with the milkweed bug O. fasciatus, weaker hth phenotypes consisted of distal labium (second maxilla)-to-leg transformations, and truncation of antennae [24]. The similar range of phenotypes observed upon knockdown of hth orthologues in multiple insects and the chelicerate exemplar P. opilio suggests evolutionary conservation of hth function in proximo-distal patterning and cephalic appendage specification over 550 million years of arthropod evolution.…”

Section: Resultsmentioning

confidence: 99%

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

et al. 2015

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The segmental architecture of the arthropod head is one of the most controversial topics in the evolutionary developmental biology of arthropods. The deutocerebral (second) segment of the head is putatively homologous across Arthropoda, as inferred from the segmental distribution of the tripartite brain and the absence of Hox gene expression of this anterior-most, appendage-bearing segment. While this homology statement implies a putative common mechanism for differentiation of deutocerebral appendages across arthropods, experimental data for deutocerebral appendage fate specification are limited to winged insects. Mandibulates (hexapods, crustaceans and myriapods) bear a characteristic pair of antennae on the deutocerebral segment, whereas chelicerates (e.g. spiders, scorpions, harvestmen) bear the eponymous chelicerae. In such hexapods as the fruit fly, Drosophila melanogaster, and the cricket, Gryllus bimaculatus, cephalic appendages are differentiated from the thoracic appendages (legs) by the activity of the appendage patterning gene homothorax (hth). Here we show that embryonic RNA interference against hth in the harvestman Phalangium opilio results in homeonotic chelicera-to-leg transformations, and also in some cases pedipalp-to-leg transformations. In more strongly affected embryos, adjacent appendages undergo fusion and/ or truncation, and legs display proximal defects, suggesting conservation of additional functions of hth in patterning the antero-posterior and proximodistal appendage axes. Expression signal of anterior Hox genes labial, proboscipedia and Deformed is diminished, but not absent, in hth RNAi embryos, consistent with results previously obtained with the insect G. bimaculatus. Our results substantiate a deep homology across arthropods of the mechanism whereby cephalic appendages are differentiated from locomotory appendages.

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Section: Resultsmentioning

confidence: 99%

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

et al. 2015

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“…Most of the recent expression and functional analyses on Dll's role in mandible development collectively suggest that Dll does not play a significant role in the mandibular development of insects (Panganiban et al 1994, Popadic et al 1998, Beermann et al 2001, Angelini & Kaufman 2004, Angelini & Kaufman 2005, Simonnet & Moczek 2011, Coulcher & Telford 2013, and our a priori assumption was that Dll would not be not expressed in stag beetle mandibles. However, it is known that Dll has been independently co-opted during the development of novel traits, especially epidermal outgrowths in insects (Panganiban et al 1994, Moczek & Nagy 2005, Moczek & Rose 2009, Toga et al 2012, raising the possibility that distal patterning, including Dll expression, might have been restored in the evolution of extreme mandible size in these beetles.…”

Section: Distal-less (Dll)mentioning

confidence: 86%

The function of appendage patterning genes in mandible development of the sexually dimorphic stag beetle

Gotoh

Zinna

Ishikawa

et al. 2017

Developmental Biology

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One of the defining features of the evolutionary success of insects is the morphological diversification of their appendages, especially mouthparts. Although most insects share a common mouthpart ground plan, there is remarkable diversity in the relative size and shapes of these appendages among different insect lineages. One of the most prominent examples of mouthpart modification can be found in the enlargement of mandibles in stag beetles (Coleoptera, Insecta). In order to understand the proximate mechanisms of mouthpart modification, we investigated the function of appendage-patterning genes in mandibular enlargement during extreme growth of the sexually dimorphic mandibles of the stag beetle Cyclommatus metallifer. Based on knowledge from Drosophila and Tribolium studies, we focused on seven appendage patterning genes (Distal-less (Dll), aristaless (al), dachshund (dac), homothorax (hth), Epidermal growth factor receptor (Egfr), escargot (esg), and Keren (Krn). In order to characterize the developmental function of these genes, we performed functional analyses by using RNA interference (RNAi).Importantly, we found that RNAi knockdown of dac resulted in a significant mandible size reduction in males but not in female mandibles. In addition to reducing the size of mandibles, dac knockdown also resulted in a loss of the serrate teeth structures on the mandibles of males and females. We found that al and hth play a significant role during morphogenesis of the large male-specific inner mandibular tooth.On the other hand, knockdown of the distal selector gene Dll did not affect mandible development, supporting the hypothesis that mandibles likely do not contain the distal-most region of the ancestral appendage and therefore co-option of Dll expression is unlikely to be involved in mandible enlargement in stag beetles. In addition to mandible development, we explored possible roles of these genes in controlling the divergent antennal morphology of Coleoptera.

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“…It has been suggested that patterns of Hox gene expression are correlated with the evolution of novel mouthpart morphologies [37][38][39]. In Protura, Collembola and Diplura, Hox gene expression in developing mouthparts has not been studied yet; therefore, the influence of these regulatory mechanisms on the general principle is unclear.…”

Section: (C) the Evolution Of Structural Mouthpart Interactions In Inmentioning

confidence: 99%

Structural mouthpart interaction evolved already in the earliest lineages of insects

et al. 2015

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In butterflies, bees, flies and true bugs specific mouthparts are in close contact or even fused to enable piercing, sucking or sponging of particular food sources. The common phenomenon behind these mouthpart types is a complex composed of several consecutive mouthparts which structurally interact during food uptake. The single mouthparts are thus only functional in conjunction with other adjacent mouthparts, which is fundamentally different to biting-chewing. It is, however, unclear when structural mouthpart interaction (SMI) evolved since this principle obviously occurred multiple times independently in several extant and extinct winged insect groups. Here, we report a new type of SMI in two of the earliest wingless hexapod lineagesDiplura and Collembola. We found that the mandible and maxilla interact with each other via an articulatory stud at the dorsal side of the maxillary stipes, and they are furthermore supported by structures of the hypopharynx and head capsule. These interactions are crucial stabilizing elements during food uptake. The presence of SMI in these ancestrally wingless insects, and its absence in those crustacean groups probably ancestral to insects, indicates that SMI is a groundplan apomorphy of insects. Our results thus contradict the currently established view of insect mouthpart evolution that biting-chewing mouthparts without any form of SMI are the ancestral configuration. Furthermore, SMIs occur in the earliest insects in a high anatomical variety. SMIs in stemgroup representatives of insects may have triggered efficient exploitation and fast adaptation to new terrestrial food sources much earlier than previously supposed.

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Functional analyses in the hemipteran Oncopeltus fasciatus reveal conserved and derived aspects of appendage patterning in insects

Cited by 106 publications

References 42 publications

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

A conserved genetic mechanism specifies deutocerebral appendage identity in insects and arachnids

The function of appendage patterning genes in mandible development of the sexually dimorphic stag beetle

Structural mouthpart interaction evolved already in the earliest lineages of insects

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