The evolution of patterning of serially homologous appendages in insects

Dev Genes Evol. 2004 Jul;214(7):324-38. doi: 10.1007/s00427-004-0412-6. Epub 2004 May 29.

Abstract

Arthropod bodies are formed by a series of appendage-bearing segments, and appendages have diversified both along the body axis within species and between species. Understanding the developmental basis of this variation is essential for addressing questions about the evolutionary diversification of limbs. We examined the development of serially homologous appendages of two insect species, the beetle Tribolium castaneum and the grasshopper Schistocerca americana. Both species retain aspects of ancestral appendage morphology and development that have been lost in Drosophila, including branched mouthparts and direct development of appendages during embryogenesis. We characterized the expression of four genes important in proximodistal axis development of Drosophila appendages: the secreted signaling factors wingless and decapentaplegic, and the homeodomain transcription factors extradenticle and Distal-less. Our comparisons focus on two aspects of appendage morphology: differentiation of the main axis of serial homologues and the appearance of proximal branches (endites) in the mouthparts. Although Distal-less expression is similar in endites and palps of the mouthparts, the expression of other genes in the endites does not conform to their known roles in axial patterning, leading us to reject the hypothesis that branched insect mouthparts develop by reiteration of the limb patterning network. With the exception of decapentaplegic, patterning of the main appendage axis is generally more similar in direct homologues than in serial homologues. Interestingly, however, phylogenetic comparisons suggest that patterning of serial homologues was more similar in ancestral insects, and thus that the observed developmental differences did not cause the evolutionary divergence in morphology among serial homologues.

Publication types

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

MeSH terms

  • Animals
  • Biological Evolution*
  • Body Patterning / genetics*
  • Coleoptera / embryology*
  • Extremities / embryology*
  • Gene Expression*
  • Genes, Insect / genetics
  • Grasshoppers / embryology*
  • Histological Techniques
  • In Situ Hybridization
  • Indoles
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Species Specificity
  • Transcription Factors / metabolism

Substances

  • Indoles
  • Intercellular Signaling Peptides and Proteins
  • Transcription Factors
  • DAPI