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  1. Abstract

    The evolution of gene expression viacis‐regulatory changes is well established as a major driver of phenotypic evolution. However, relatively little is known about the influence of enhancer architecture and intergenic interactions on regulatory evolution. We address this question by examining chemosensory system evolution inDrosophila.Drosophila prolongatamales show a massively increased number of chemosensory bristles compared to females and males of sibling species. This increase is driven by sex‐specific transformation of ancestrally mechanosensory organs. Consistent with this phenotype, thePox neurotranscription factor (Poxn), which specifies chemosensory bristle identity, shows expanded expression inD. prolongatamales.Poxnexpression is controlled by nonadditive interactions among widely dispersed enhancers. Although someD. prolongata Poxnenhancers show increased activity, the additive component of this increase is slight, suggesting that most changes inPoxnexpression are due to epistatic interactions betweenPoxnenhancers andtrans‐regulatory factors. Indeed, the expansion ofD. prolongata Poxnenhancer activity is only observed in cells that expressdoublesex(dsx), the gene that controls sexual differentiation inDrosophilaand also shows increased expression inD. prolongatamales due tocis‐regulatory changes. Although expandeddsxexpression may contribute to increased activity ofD. prolongata Poxnenhancers, this interaction is not sufficient to explain the full expansion ofPoxnexpression, suggesting thatcistransinteractions betweenPoxn, dsx, and additional unknown genes are necessary to produce the derivedD. prolongataphenotype. Overall, our results demonstrate the importance of epistatic gene interactions for evolution, particularly when pivotal genes have complex regulatory architecture.

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  2. Abstract

    Binary communication systems that involve sex‐specific signaling and sex‐specific signal perception play a key role in sexual selection and in the evolution of sexually dimorphic traits. The driving forces and genetic changes underlying such traits can be investigated in systems where sex‐specific signaling and perception have emerged recently and show evidence of potential coevolution. A promising model is found inDrosophila prolongata, which exhibits a species‐specific increase in the number of male chemosensory bristles. We show that this transition coincides with recent evolutionary changes in cuticular hydrocarbon (CHC) profiles. Long‐chain CHCs that are sexually monomorphic in the closest relatives ofD. prolongata(D. rhopaloa,D. carrolli,D. kurseongensis, andD. fuyamai) are strongly male‐biased in this species. We also identify an intraspecific female‐limited polymorphism, where some females have male‐like CHC profiles. Both the origin of sexually dimorphic CHC profiles and the female‐limited polymorphism inD. prolongatainvolve changes in the relative amounts of three mono‐alkene homologs, 9‐tricosene, 9‐pentacosene, and 9‐heptacosene, all of which share a common biosynthetic origin and point to a potentially simple genetic change underlying these traits. Our results suggest that pheromone synthesis may have coevolved with chemosensory perception and open the way for reconstructing the origin of sexual dimorphism in this communication system.

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