Evolution of the insect body plan as revealed by the Sex combs reduced expression pattern.
The products of the HOM/Hox homeotic genes form a set of evolutionarily conserved transcription factors that control elaborate developmental processes and specify cell fates in many metazoans. We examined the expression of the ortholog of the homeotic gene Sex combs reduced (Scr) of Drosophila melanogaster in insects of three divergent orders: Hemiptera, Orthoptera and Thysanura. Our data reflect how the conservation and variation of Scr expression has affected the morphological evolution of insects. Whereas the anterior epidermal expression of Scr, in a small part of the posterior maxillary and all of the labial segment, is found to be in common among all four insect orders, the posterior (thoracic) expression domains vary. Unlike what is observed in flies, the Scr orthologs of other insects are not expressed broadly over the first thoracic segment, but are restricted to small patches. We show here that Scr is required for suppression of wings on the prothorax of Drosophila. Moreover, Scr expression at the dorsal base of the prothoracic limb in two other winged insects, crickets (Orthoptera) and milkweed bugs (Hemiptera), is consistent with Scr acting as a suppressor of prothoracic wings in these insects. Scr is also expressed in a small patch of cells near the basitarsal-tibial junction of milkweed bugs, precisely where a leg comb develops, suggesting that Scr promotes comb formation, as it does in Drosophila. Surprisingly, the dorsal prothoracic expression of Scr is also present in the primitively wingless firebrat (Thysanura) and the leg patch is seen in crickets, which have no comb. Mapping both gene expression patterns and morphological characters onto the insect phylogenetic tree demonstrates that in the cases of wing suppression and comb formation the appearance of expression of Scr in the prothorax apparently precedes these specific functions.
Rogers
B T
BT
Howard Hughes Medical Institute, Department of Biology, Indiana University, Bloomington 47405, USA.
Peterson
M D
MD
Kaufman
T C
TC
D000595:Amino Acid Sequence; D000818:Animals; D001483:Base Sequence; D003001:Cloning, Molecular; D017931:DNA Primers; D029721:Drosophila Proteins; D004331:Drosophila melanogaster / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development; D019143:Evolution, Molecular; D018507:Gene Expression Regulation, Developmental; D005801:Genes, Homeobox; D017344:Genes, Insect; D007301:Insect Hormones / Q000096:biosynthesis* / Q000737:chemistry / Q000235:genetics; D007313:Insecta / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development*; D008969:Molecular Sequence Data; D009928:Organ Specificity; D010802:Phylogeny; D016133:Polymerase Chain Reaction; D017386:Sequence Homology, Amino Acid; D014157:Transcription Factors
D017931:DNA Primers; D029721:Drosophila Proteins; D007301:Insect Hormones; C059627:Scr protein, Drosophila; D014157:Transcription Factors