116 Oral - Evolution II
Friday April 08, 5:30 PM - 5:45 PM

Investigating the evolution of new body parts in the rapidly evolution genitalia of Drosophila


Authors:
Gavin Rice 1; Kenechukwu Charles-Obi 1; Jean David 2; Nicolas Gompel 3; Amir Yassin 2,4; Julia Zeitlinger 5,6; Mark Rebeiz 1

Affiliations:
1) Department of Biology, University of Pittsburgh, Pittsburgh, PA; 2) Laboratoire Evolution, Génomes, Comportement, Ecologie (EGCE), UMR 9191, CNRS,IRD, Univ.Paris-Sud, Université Paris-Saclay, cedex, France; 3) Ludwig-Maximilians Universität München, Fakultät für Biologie, Biozentrum, Grosshaderner Strasse 2, 82152 Planegg-Martinsried, Germany; 4) Institut 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 ; 5) Stowers Institute for Medical Research, Kansas City, MO; 6) Department of Pathology and Laboratory Medicine, Kansas University Medical Center, Kansas City, MO

Keywords:
l. evo-devo; i. other imaginal discs

Recently evolved traits i.e., novelties, often represent key features that allow animals to exploit new ecological niches (e.g. feathers in birds) and can even help them find a mate (e.g. bioluminescence in fireflies). The rapidly evolving genitalia of Drosophila provides a powerful system to study the developmental basis of qualitative changes in morphology. However, this high morphological diversity also poses a distinct challenge, since it can be difficult to disentangle which structures are homologous and which represent novelties.

To determine whether genital structures of different species were homologous or novel, we compared the development of phallic outgrowths in the Oriental lineage, which contains Drosophila melanogaster. We found that most phallic outgrowths are formed by multicellular projections. However, several multicellular outgrowths that were thought to be homologous, are in fact formed by different tissues of the phallus in different species, indicating that they are heterologous structures. Furthermore, we uncovered evidence that phallic outgrowths found in the Drosophila eugracilis phallus are formed by large unicellular projections, suggesting that they have evolved convergently to the previously described multicellular outgrowths. These unicellular outgrowths are likely novel as they are absent the homologous tissue of five other species of the Oriental lineage. We found that the trichome genetic network is expressed in these unicellular phallic outgrowths, suggesting that the co-option of this network underlies this dramatic phenotype. In fact, activation of the trichome genetic network in the phallus of Drosophila melanogaster induces a phenocopy of the unicellular outgrowths found in Drosophila eugracilis.

Our work highlights that understanding development can be key to discern between homology vs heterology, allowing us to formulate testable evolutionary models (i.e. co-option vs convergence).