Evolution of Mechanisms that Control Mating in Drosophila Males

Osama M Ahmed; Aram Avila-Herrera; Khin May Tun; Paula H Serpa; Justin Peng; Srinivas Parthasarathy; Jon-Michael Knapp; David L Stern; Graeme W Davis; Katherine S Pollard; Nirao M Shah

doi:10.1016/j.celrep.2019.04.104

Evolution of Mechanisms that Control Mating in Drosophila Males

Cell Rep. 2019 May 28;27(9):2527-2536.e4. doi: 10.1016/j.celrep.2019.04.104.

Authors

Affiliations

¹ Program in Neuroscience, University of California, San Francisco, San Francisco, CA 94143, USA; Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08540, USA.
² Integrative Program in Quantitative Biology, University of California, San Francisco, San Francisco, CA 94158, USA; Computation Directorate, Lawrence Livermore National Laboratory, Livermore, CA 94550, USA; Gladstone Institutes, San Francisco, CA 94158, USA.
³ Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143, USA.
⁴ Integrative Program in Quantitative Biology, University of California, San Francisco, San Francisco, CA 94158, USA.
⁵ Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, USA; L.E.K. Consulting, 75 State Street, Boston, MA 02109, USA.
⁶ Department of Neurobiology, Stanford University, Stanford, CA 94305, USA; Janelia Research Campus, HHMI Ashburn, Ashburn, VA 20147, USA.
⁷ Janelia Research Campus, HHMI Ashburn, Ashburn, VA 20147, USA.
⁸ Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA.
⁹ Institute for Human Genetics, University of California, San Francisco, San Francisco, CA 94143, USA; Department of Epidemiology and Biostatistics, University of California, San Francisco, San Francisco, CA 94158, USA; Gladstone Institutes, San Francisco, CA 94158, USA.
¹⁰ Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, USA; Department of Neurobiology, Stanford University, Stanford, CA 94305, USA; Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143, USA. Electronic address: nirao@stanford.edu.

Abstract

Genetically wired neural mechanisms inhibit mating between species because even naive animals rarely mate with other species. These mechanisms can evolve through changes in expression or function of key genes in sensory pathways or central circuits. Gr32a is a gustatory chemoreceptor that, in D. melanogaster, is essential to inhibit interspecies courtship and sense quinine. Similar to D. melanogaster, we find that D. simulans Gr32a is expressed in foreleg tarsi, sensorimotor appendages that inhibit interspecies courtship, and it is required to sense quinine. Nevertheless, Gr32a is not required to inhibit interspecies mating by D. simulans males. However, and similar to its function in D. melanogaster, Ppk25, a member of the Pickpocket family, promotes conspecific courtship in D. simulans. Together, we have identified distinct evolutionary mechanisms underlying chemosensory control of taste and courtship in closely related Drosophila species.

Keywords: Gr32a; Gr33a; Ppk25; chemosensation; courtship; evolution; mating; pheromones; reproduction; reproductive isolation.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Biological Evolution*
Cell Communication
Chemoreceptor Cells
Courtship / psychology*
Drosophila Proteins / genetics
Drosophila Proteins / metabolism*
Drosophila melanogaster / physiology*
Drosophila simulans / physiology*
Female
Male
Pheromones
Receptors, Cell Surface / genetics
Receptors, Cell Surface / metabolism*
Reproduction
Sexual Behavior, Animal*
Taste / physiology*

Substances

Drosophila Proteins
Gr32a protein, Drosophila
Pheromones
Receptors, Cell Surface

Grants and funding

R35 NS097212/NS/NINDS NIH HHS/United States