Differential recruitment of limb patterning genes during development and diversification of beetle horns

• Published in: Proceedings of the National Academy of Sciences - PNAS 2009-06, Vol.106 (22), p.8992-8997
• Main Authors: Moczek, Armin P, Rose, Debra J
• Format: Article
• Language: English
• Subjects: Adult insects; Animals; Appendages; Beetles; Biodiversity; Biological Sciences; Body Patterning - genetics; Cloning, Molecular; Coleoptera - genetics; Coleoptera - growth & development; Developmental genetics; Drosophila; Evolution; Evolutionary biology; Evolutionary genetics; Extremities - growth & development; Female; gene expression; Gene Expression Regulation, Developmental; Gene Knockdown Techniques; Genes; Genes, Insect; Genetics; Genotype & phenotype; Homology; Horns; Horns - growth & development; Horns - metabolism; insect development; insect genetics; Insect larvae; insect morphology; Insects; Larval development; Limbs; Male; Male animals; messenger RNA; Molecular Sequence Data; Onthophagus binodis; Onthophagus taurus; Pattern formation; Phenotypes; Phylogeny; Radiation; Recruitment; RNA; RNA Interference; Sequence Analysis, Protein; Sex Characteristics; Sex Factors; Sexual dimorphism; Transcription
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0809668106

The origins of novel complex phenotypes represent one of the most fundamental, yet largely unresolved, issues in evolutionary biology. Here we explore the developmental genetic regulation of beetle horns, a class of traits that lacks obvious homology to traits in other insects. Furthermore, beetle horns are remarkably diverse in their expression, including sexual dimorphisms, male dimorphisms, and interspecific differences in location of horn expression. At the same time, beetle horns share aspects of their development with that of more traditional appendages. We used larval RNA interference-mediated gene function analysis of 3 cardinal insect appendage patterning genes,dachshund, homothorax, and Distal-less, to investigate their role in development and diversification of beetle horns within and between species. Transcript depletion of all 3 patterning genes generated phenotypic effects very similar to those documented in previous studies that focused on general insect development. In addition, we found that Distal-less and homothorax, but not dachshund, regulate horn expression in a species-, sex-, body region-, and body size-dependent manner. Our results demonstrate differential co-option of appendage patterning genes during the evolution and radiation of beetle horns. Furthermore, our results illustrate that regulatory genes whose functions are otherwise highly conserved nevertheless retain the capacity to acquire additional functions, and that little phylogenetic distance appears necessary for the evolution of sex- and species-specific differences in these functions.