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Resolving Between Novelty and Homology in the Rapidly Evolving Phallus of Drosophila

View ORCID ProfileGavin R. Rice, Jean R. David, View ORCID ProfileNicolas Gompel, Amir Yassin, View ORCID ProfileMark Rebeiz
doi: https://doi.org/10.1101/2021.04.14.439817
Gavin R. Rice
1Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA
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Jean R. David
2Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), UMR 9191, CNRS, IRD, Univ.Paris-Sud, Université Paris-Saclay, cedex, France
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Nicolas Gompel
3Ludwig-Maximilians Universität München, Fakultät für Biologie, Biozentrum, Grosshaderner Strasse 2, 82152 Planegg-Martinsried, Germany
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Amir Yassin
2Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), UMR 9191, CNRS, IRD, Univ.Paris-Sud, Université Paris-Saclay, cedex, France
4Institut de Systématique, Evolution et Biodiversité, UMR7205, Centre National de la Recherche Scientifique, MNHN, Sorbonne Université, EPHE, Université des Antilles, 57 rue Cuvier, 75005 Paris, France
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Mark Rebeiz
1Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA, USA
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  • For correspondence: rebeiz@pitt.edu
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Abstract

The genitalia present some of the most rapidly evolving anatomical structures in the animal kingdom, possessing a variety of parts that can distinguish recently diverged species. In the Drosophila melanogaster group, the phallus is adorned with several processes, pointed outgrowths, that are similar in size and shape between species. However, the complex three-dimensional nature of the phallus can obscure the exact connection points of each process. Previous descriptions based upon adult morphology have primarily assigned phallic processes by their approximate positions in the phallus and have remained largely agnostic regarding their homology relationships. In the absence of clearly identified homology, it can be challenging to model when each structure first evolved. Here, we employ a comparative developmental analysis of these processes in eight members of the melanogaster species group to precisely identify the tissue from which each process forms. Our results indicate that adult phallic processes arise from three pupal primordia in all species. We found that in some cases the same primordia generate homologous structures whereas in other cases, different primordia produce phenotypically similar but remarkably non-homologous structures. This suggests that the same gene regulatory network may have been redeployed to different primordia to induce phenotypically similar traits. Our results highlight how traits diversify and can be redeployed, even at short evolutionary scales.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 14, 2021.
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Resolving Between Novelty and Homology in the Rapidly Evolving Phallus of Drosophila
Gavin R. Rice, Jean R. David, Nicolas Gompel, Amir Yassin, Mark Rebeiz
bioRxiv 2021.04.14.439817; doi: https://doi.org/10.1101/2021.04.14.439817
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Resolving Between Novelty and Homology in the Rapidly Evolving Phallus of Drosophila
Gavin R. Rice, Jean R. David, Nicolas Gompel, Amir Yassin, Mark Rebeiz
bioRxiv 2021.04.14.439817; doi: https://doi.org/10.1101/2021.04.14.439817

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