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Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species.

ABSTRACT: In the last 240,000 years, males of the Drosophila simulans species clade have evolved striking differences in the morphology of their epandrial posterior lobes and claspers (surstyli). These appendages are used for grasping the female during mating and so their divergence is most likely driven by sexual selection. Mapping studies indicate a highly polygenic and generally additive genetic basis for these morphological differences. However, we have limited understanding of the gene regulatory networks that control the development of genital structures and how they evolved to result in this rapid phenotypic diversification. Here, we used new D. simulans/D. mauritiana introgression lines on chromosome arm 3L to generate higher resolution maps of posterior lobe and clasper differences between these species. We then carried out RNA-seq on the developing genitalia of both species to identify the expressed genes and those that are differentially expressed between the two species. This allowed us to test the function of expressed positional candidates during genital development in D. melanogaster. We identified several new genes involved in the development and possibly the evolution of these genital structures, including the transcription factors Hairy and Grunge. Furthermore, we discovered that during clasper development Hairy negatively regulates tartan (trn), a gene known to contribute to divergence in clasper morphology. Taken together, our results provide new insights into the regulation of genital development and how this has evolved between species.

SUBMITTER: Hagen JFD

PROVIDER: S-EPMC7826188 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:We generated RNA-seq data of Drosophila simulans and Drosophila mauritiana developing male genitalia in order to identify expression level differences between these species. These species are closely related, yet have dramatic differences in their male genital morphologies. Three independent RNA-seq library replicates were generated for Dsim w501 and Dmau D1 developing male genitalia. Flies were reared under the above conditions, and white pre-pupae collected. Males were selected using gonad size and allowed to develop in a humid container at 25ºC until stages 2 and 4.5 (see staging guide in (Hagen et al., 2019); tartan underlies the evolution of Drosophila male genital morphology). Between these stages, the claspers develop from a ridge structure to a distinct appendage separate from the surrounding tissue, and the posterior lobe has begun to extend outwards from the lateral plate primordia (Hagen et al., 2019). The heads of pupae were impaled with a needle onto a charcoal agar plate and submerged in 1xPBS. Dissection scissors were used to remove the distal tip of the pupal case and the outer membrane, and pressure applied to the abdomen to allow the developing genitalia to be quickly expelled from the pupal case and dissected away from the abdomen. Note that the entire genital arch, including internal genital organs (but not including abdominal tissue), was isolated for RNA extraction. The genitalia from fifteen males from each stage were collected and placed directly into TRIzol. RNA was then extracted using standard procedures. Quality and quantity of RNA was verified using a Qubit, and samples were sent to the Centre for Genomic Research at the University of Liverpool where dual-indexed, strand-specific RNA-seq libraries were prepared using NEBNext polyA selection and Ultra Directional RNA preparation kits. Samples were then sequenced using Illumina HiSeq 4000 (paired-end, 2x150 bp sequencing). Dsim w501 and Dmau D1 reads were mapped against reannotated reference coding sequences (Torres-Oliva et al., 2016).

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Unraveling the Genetic Basis for the Rapid Diversification of Male Genitalia between Drosophila Species.

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