Co-option of the trichome-forming network initiated the evolution of a morphological novelty in Drosophila eugracilis.

Abstract

Identifying the molecular origins by which new morphological structures evolve is one of the long-standing problems in evolutionary biology. To date, vanishingly few examples provide a compelling account of how new morphologies were initially formed, thereby limiting our understanding of how diverse forms of life derived their complex features. Here, we provide evidence that the large projections on the Drosophila eugracilis phallus that are implicated in sexual conflict have evolved through the partial co-option of the trichome genetic network. These unicellular apical projections on the phallus postgonal sheath are reminiscent of trichomes that cover the Drosophila body but are up to 20-fold larger in size. During their development, they express the transcription factor Shavenbaby, the master regulator of the trichome network. Consistent with the co-option of the Shavenbaby network during the evolution of the D. eugracilis projections, somatic mosaic CRISPR-Cas9 mutagenesis shows that shavenbaby is necessary for their proper length. Moreover, misexpression of Shavenbaby in the sheath of D. melanogaster, a naive species that lacks these projections, is sufficient to induce small trichomes. These induced projections rely on a genetic network that is shared to a large extent with the D. eugracilis projections, indicating its partial co-option but also some genetic rewiring. Thus, by leveraging a genetically tractable evolutionary novelty, our work shows that the trichome-forming network is flexible enough that it can be partially co-opted in a new context and subsequently refined to produce unique apical projections that are barely recognizable compared with their simpler ancestral beginnings.