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

Proc Biol Sci. 2015 Jun 7;282(1808):20150698. doi: 10.1098/rspb.2015.0698.

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 proximo-distal 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.

Keywords: Arthropoda; antenna; chelicera; deutocerebrum; opiliones; serial homology.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Arachnida / embryology
  • Arachnida / genetics*
  • Arthropod Proteins / genetics*
  • Arthropod Proteins / metabolism
  • Body Patterning*
  • Extremities / embryology
  • Gene Expression Regulation, Developmental*
  • Horseshoe Crabs / embryology
  • Horseshoe Crabs / genetics
  • Insecta / embryology
  • Insecta / genetics
  • Molecular Sequence Data
  • RNA Interference
  • Scorpions / embryology
  • Scorpions / genetics
  • Sequence Analysis, DNA

Substances

  • Arthropod Proteins

Associated data

  • GENBANK/KP129111
  • GENBANK/KP129112
  • GENBANK/KP129113