Beetle horns are regulated by the Hox gene, Sex combs reduced, in a species- and sex-specific manner

• Published in: Evolution & development 2010-07, Vol.12 (4), p.353-362
• Main Authors: Wasik, Bethany R, Rose, Debra J, Moczek, Armin P
• Format: Article
• Language: English
• Subjects: Animal reproduction; Animals; Body Patterning - genetics; Cloning, Molecular; Coleoptera - anatomy & histology; Coleoptera - genetics; Coleoptera - growth & development; Evolution; Female; Gene Expression Regulation, Developmental; Head; Homeodomain Proteins - antagonists & inhibitors; Homeodomain Proteins - genetics; Homeodomain Proteins - physiology; Horns; HOX gene; Insect Proteins - antagonists & inhibitors; Insect Proteins - genetics; Insect Proteins - physiology; Insects; Male; Onthophagus; Pattern formation; Prothorax; RNA Interference; Sequence Analysis, Protein; Sex; Sex Characteristics; Sexual dimorphism; Species Specificity; Thorax
• ISSN: 1520-541X; 1525-142X
• DOI: 10.1111/j.1525-142X.2010.00422.x

Discovering the mechanisms that underlie the origin of novel features represents a major frontier in developmental and evolutionary biology. Here we begin to characterize the role of the Hox gene Sex combs reduced (Scr) during the development and evolution of a morphologically novel trait: beetle horns. Beetle horns develop as epidermal outgrowths from the prothorax and/or head, and size and location vary dramatically across species and between sexes. Using both comparative gene expression and larval RNA interference in two species of the horned beetle genus Onthophagus, we show that Scr functions in patterning adult labial mouthpart identity and suppressing wing development in the prothorax. At the same time, however, our results illustrate that Scr has acquired, within its ancestral domain of expression, additional new functions including the regulation of prepupal growth and pupal remodeling of pronotal horn primordia. Furthermore, comparative analyses of our results across both Onthophagus species, which differ in location of horn development (thoracic horns vs. thoracic and head horns) as well as patterns of sexual dimorphism (traditional vs. reversed sexual dimorphism), reveal surprising differences in exactly when, where, and to what degree Scr regulates horn formation in different sexes. These observations suggest that the interactions between Scr and its targets in the regulation of horn development can diversify quickly over remarkably short phylogenetic distances. More generally, our results suggest that the Hox complex can play an integral role in the development and evolution of novel complex traits while maintaining traditional patterning responsibilities.