Evolution of homeotic gene regulation and function in flies and butterflies

IT has been proposed that the evolution of homeotic genes parallels, and to some degree directs, the evolution of segment diversity in the myriapod–insect lineage1–3. But the discovery of discrete Antennapedia complex (ANT-C) and bithorax complex (BX-C) gene members in Crustacea4, chelicerates5, annelids6–8 and various insects9–11, as well as in vertebrates12, indicates that the expansion and diversification of homeotic genes preceded the diversification of arthropods and insects. How, then, have these genes influenced the evolution of body plans? To address this question, we now examine homeotic gene expression and regulation in butterflies (Lepidoptera), which, unlike flies, possess larval abdominal limbs and two pairs of wings. We show that the difference in larval limb number between these insects results from striking changes in BX-C gene regulation in the butterfly abdomen, and we deduce that the wing-patterning genes regulated by Ultrabithorax have diverged in the course of butterfly and fly evolution. These findings have gen-eral implications for the role of homeotic genes in animal evolution.

[1]  William Bateson,et al.  Materials for the study of variation , 1894 .

[2]  J. Stuart,et al.  Genetic analysis of the homeotic gene complex (HOM-C) in the beetle Tribolium castaneum. , 1989, Developmental biology.

[3]  E. Lewis,et al.  The abdominal region of the bithorax complex , 1985, Cell.

[4]  G. Morata,et al.  Expression and regulation of the abd-A gene of Drosophila. , 1990, Development.

[5]  R. Kelsh,et al.  An analysis of abdominal-B expression in the locust Schistocerca gregaria. , 1993, Development.

[6]  E. Lewis A gene complex controlling segmentation in Drosophila , 1978, Nature.

[7]  M. Akam,et al.  HOM/Hox genes of Artemia: implications for the origin of insect and crustacean body plans , 1993, Current Biology.

[8]  Prolegs, legs and wings of insects , 1994 .

[9]  M. Wilcox,et al.  Protein products of the bithorax complex in Drosophila , 1984, Cell.

[10]  A. Garcı́a-Bellido Homoeotic and atavic mutations in insects , 1977 .

[11]  M. Levine,et al.  Characterization of a homologue of bithorax-complex genes in the leech Hirudo medicinalis , 1989, Nature.

[12]  S. Carroll,et al.  The role of the Distal-less gene in the development and evolution of insect limbs , 1994, Current Biology.

[13]  F. Karch,et al.  abdA expression in Drosophila embryos. , 1990, Genes & development.

[14]  Michael Akam,et al.  Homeotic genes and the control of segment diversity , 1988 .

[15]  E. Lewis Genes and Developmental Pathways , 1963 .

[16]  G. Struhl Genes controlling segmental specification in the Drosophila thorax. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Juan Botas,et al.  Homeotic genes of the bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less , 1992, Cell.

[18]  Jordi Garcia-Fernàndez,et al.  Archetypal organization of the amphioxus Hox gene cluster , 1994, Nature.

[19]  C. Richardson,et al.  DNA sequence analysis with a modified bacteriophage T7 DNA polymerase. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[20]  R. Kelsh,et al.  Homeotic gene expression in the locust Schistocerca: an antibody that detects conserved epitopes in Ultrabithorax and abdominal-A proteins. , 1994, Developmental genetics.

[21]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[22]  L. Buss,et al.  A PCR-based survey of homeobox genes in Ctenodrilus serratus (Annelida: Polychaeta). , 1994, Molecular phylogenetics and evolution.

[23]  William McGinnis,et al.  Homeobox genes and axial patterning , 1992, Cell.

[24]  L. Buss,et al.  HOM/Hox type homeoboxes in the chelicerate Limulus polyphemus. , 1993, Molecular phylogenetics and evolution.

[25]  J. Stuart,et al.  The Tribolium homeotic gene Abdominal is homologous to abdominal-A of the Drosophila bithorax complex. , 1993, Development.

[26]  R. Goldschmidt,et al.  The material basis of evolution , 1941 .

[27]  D. Hogness,et al.  Segmental distribution of bithorax complex proteins during Drosophila development , 1985, Nature.