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

Abstract

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.

Cooption of an appendage-patterning gene cassette in the head segmentation of arachnids

“…These data are consistent with the prediction of convergent assembly of the insect and arachnid GRNs, wherein Sp homologs mediate the regulation of Dll by Hox signaling (26). [46][47][48]. By comparison with the regionalization of the PD axis, evolution of the GRN underlying specification of arthropod leg fate is poorly understood from a functional standpoint ( Fig.…”

The evolution of selector gene function: Expression dynamics and regulatory interactions of tiptop/teashirt across Arthropoda

“…The proximo‐distal axis of panarthropod appendages in particular is patterned by a suite of transcription factors whose positional relationships are broadly conserved (Abu‐Shaar & Mann, ; Cohen, Brönner, Küttner, Jürgens, & Jäckle, ; Dong, Chu, & Panganiban, ; Dong, Dicks, & Panganiban, ; Janssen, Eriksson, Budd, Akam, & Prpic, ; Mardon, Solomon, & Rubin, ; Panganiban et al, ; Panganiban, Nagy, & Carroll, ; Panganiban, Sebring, Nagy, & Carroll, ; Prpic, Janssen, Wigand, Klingler, & Damen, ; Schoppmeier & Damen, ; Sharma, Schwager, Extavour, & Giribet, ). Similarly, the establishment of arthropod appendage types along the antero‐posterior axis is achieved by the activity of trunk Hox genes throughout the phylum (Emerald & Cohen, ; Liubicich et al, ; Martin et al, ; Pavlopoulos et al, ; Pechmann, Schwager, Turetzek, & Prpic, ; Struhl, ; Struhl & White, ) and homothorax (Casares & Mann, ; Ronco et al, ; Sharma et al, ).…”

Palaeontology: Clearing the Heads of Cambrian Arthropods

“…The answer is that 'heads' are a distraction, because it is the segmental match-ups that inform us about homologies across the front ends of arthropods. While these correspondences can nowadays be resolved by molecular biology [3,4], for palaeontologists trying to resolve homologies of head organization across stem-group arthropods Rempel's ''Endless Dispute'' is very much alive and kicking. Ascribing correspondence of parts of the head across fossil species is important because if wrongly identified, structures will be incorrectly coded for cladistics and lead to false phylogenetic relationships.…”