Beetle horns evolved from wing serial homologs

Understanding how novel complex traits originate is a foundational challenge in evolutionary biology. Yet how descent with modification in developmental evolution may lead to morphological innovation remains poorly understood. We investigated the origin of thoracic horns in scarabaeine beetles, one of the most dramatic classes of secondary sexual traits in the animal kingdom. We show that thoracic horns derive from bilateral source tissues, that diverse wing genes are functionally required for instructing this process, and that in the absence of Hox-input thoracic horn primordia transform to contribute to ectopic wings. Once induced, however, the transcriptional profile of thoracic horns diverges markedly from that of wings and other wing serial homologs. Our results provide evidence for the serial homology between thoracic horns and insects wings, and suggest that other insect innovations may similarly derive from wing serial homologs and the concomitant recruitment of diverse genes from outside a wing formation context. This RNAseq project includes eight distinct epidermal regions from O. taurus including: left and right T2 wings as well as five distinct T1 regions: the anterior, posterior, and carinated margin (left and right), the dorso-central prothorax, and the thoracic horn. We further included abdominal support structures from the 3rd-6th abdominal segment (bilateral projections found on the abdominal segments) as well as the dorsal head epidermis. Every tissue possesses six biological replicates, although the carinated margin and T2 wings have an additional six replicates that are derived from left and right tissues from the same individual. The dorsal head epidermis and the dorso-central prothorax are two tissues we chose to include that, currently, have no published relationship to wings - and thus serve as contrasts to the other, wing-related tissues.