TY - JOUR
T1 - The evolution of patterning of serially homologous appendages in insects
AU - Jockusch, Elizabeth L.
AU - Williams, Terri A.
AU - Nagy, Lisa M.
N1 - Funding Information:
Acknowledgements We thank G. Panganiban and R. White for providing antibodies, M. Friedrich, J. Doctor and S. Newfeld for providing clones, D. Hahn for providing the founding Schistocerca colony, and I. Jones and J. Cooley for technical assistance. M. Palopoli kindly provided additional information on DLL expression in collembolans. The comments of two anonymous reviewers helped improve the manuscript. This work was funded by National Science Foundation grants to E.L.J/ (IBN 0091005), T.A.W. (IBN 0235917) and L.M.N. (IBN 9874624).
PY - 2004/7
Y1 - 2004/7
N2 - 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.
AB - 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.
KW - Appendage development and evolution
KW - Insects
KW - Mouthparts
KW - Schistocera americana
KW - Tribolium castaneum
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U2 - 10.1007/s00427-004-0412-6
DO - 10.1007/s00427-004-0412-6
M3 - Article
C2 - 15170569
AN - SCOPUS:4344581429
SN - 0949-944X
VL - 214
SP - 324
EP - 338
JO - Development Genes and Evolution
JF - Development Genes and Evolution
IS - 7
ER -