Co-option of an Ancestral Hox-Regulated Network Underlies a Recently Evolved Morphological Novelty

The evolutionary origins of complex morphological structures such as the vertebrate eye or insect wing remain one of the greatest mysteries of biology. Recent comparative studies of gene expression imply that new structures are not built from scratch, but rather form by co-opting preexisting gene networks. A key prediction of this model is that upstream factors within the network will activate their preexisting targets (i.e., enhancers) to form novel anatomies. Here, we show how a recently derived morphological novelty present in the genitalia of D. melanogaster employs an ancestral Hox-regulated network deployed in the embryo to generate the larval posterior spiracle. We demonstrate how transcriptional enhancers and constituent transcription factor binding sites are used in both ancestral and novel contexts. These results illustrate network co-option at the level of individual connections between regulatory genes and highlight how morphological novelty may originate through the co-option of networks controlling seemingly unrelated structures. [Display omitted] •Newly evolved Drosophila adult genital structure allows analysis of network history•The adult structure evolved by co-opting the network of a larval breathing structure•Ten genes, including seven transcription factors, are shared between both networks•Seven embryonic regulatory sequences are re-deployed during genital development Network reuse, or co-option, has been implicated in explaining the origins of many complex structures. Glassford et al. demonstrate that a newly evolved morphological structure in adult genitalia that is unique to the Drosophila melanogaster subgroup co-opted an embryonic transcriptional network that contributes to the development of a larval breathing structure.