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
Affiliations
Osama M. Ahmed
Program in Neuroscience, University of California, San Francisco, San Francisco, CA 94143, USA; Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08540, USA
Aram Avila-Herrera
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
Khin May Tun
Department of Anatomy, University of California, San Francisco, San Francisco, CA 94143, USA
Paula H. Serpa
Integrative Program in Quantitative Biology, University of California, San Francisco, San Francisco, CA 94158, USA
Justin Peng
Integrative Program in Quantitative Biology, University of California, San Francisco, San Francisco, CA 94158, USA
Srinivas Parthasarathy
Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, CA 94305, USA; L.E.K. Consulting, 75 State Street, Boston, MA 02109, USA
Jon-Michael Knapp
Department of Neurobiology, Stanford University, Stanford, CA 94305, USA; Janelia Research Campus, HHMI Ashburn, Ashburn, VA 20147, USA
David L. Stern
Janelia Research Campus, HHMI Ashburn, Ashburn, VA 20147, USA
Graeme W. Davis
Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA
Katherine S. Pollard
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
Nirao M. Shah
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; Corresponding author
Summary: 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. : Mechanisms that inhibit interspecies mating are critical to reproductive isolation of species. Ahmed et al. show that Gr32a, a chemoreceptor that inhibits interspecies courtship by D. melanogaster males, does not inhibit this behavior in the closely related D. simulans, indicating rapid evolution of peripheral sensory mechanisms that preclude interspecies breeding. Keywords: Gr32a, Gr33a, Ppk25, chemosensation, pheromones, evolution, reproduction, reproductive isolation, courtship, mating