Evolution of Mechanisms that Control Mating in Drosophila Males

doi:10.1016/j.celrep.2019.04.104

. 2019 May 28;27(9):2527-2536.e4.

doi: 10.1016/j.celrep.2019.04.104.

Evolution of Mechanisms that Control Mating in Drosophila Males

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.

PMID: 31141679
PMCID: PMC6646047
DOI: 10.1016/j.celrep.2019.04.104

Evolution of Mechanisms that Control Mating in Drosophila Males

Osama M Ahmed et al. Cell Rep. 2019.

. 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.

PMID: 31141679
PMCID: PMC6646047
DOI: 10.1016/j.celrep.2019.04.104

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.

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Conflict of interest statement

DECLARATION OF INTERESTS

The authors declare no competing interests.

Figures

**Figure 1. *D. simulans* Male Foreleg Tarsi Inhibit Courtship of Other Species and Are Not Essential for Courtship of Conspecific Females**
(A) We tested whether, similar to *D. melanogaster* males, foreleg tarsi also inhibited interspecies courtship by *D. simulans* males. (B) *D. simulans* males lacking foreleg tarsi court conspecific, *D. melanogaster*, and *D. virilis* females. (C) *D. simulans* males lacking foreleg tarsi are more likely to show intense courtship toward *D. melanogaster* and *D. virilis* females. (D) *D. simulans* males lacking foreleg tarsi show more courtship toward conspecific males. (E) *D. simulans* males lacking foreleg tarsi are more likely to show intense courtship toward conspecific males. Mean ± SEM. CI, fraction time spent courting target fly. Each circle denotes CI of one male. n = 14–41 per cohort. ***p < 0.001. See also Figure S1.

**Figure 2. A Regulatory Region in the *Gr32a* Locus Is Functionally Conserved**
(A) We sought to determine whether, similar to *D. melanogaster*, Gr32a was expressed in *D. simulans* foreleg tarsi. (B) Schematic of transgenic constructs using a DNA sequence 5´ of Gr32a start codon from *D. simulans* (orange) and *D. melanogaster* (blue) to drive GAL4 expression. Sequence identity in this region between the two species is noted by solid orange color. (C–F) Gr32a^sim-GAL4 (C and D) and Gr32a^mel-GAL4 (E and F) each drive comparable citrine expression in distal tarsal segments T4 and T5 in both *D. simulans* (C and E) and *D. melanogaster* (D and F) male forelegs. (G) Quantification of data shown in histological panels (C–F). Mean ± SEM. Each circle denotes the number of citrine+ cells per male foreleg tarsi per genotype. n = 11–18 per genotype. Scale bar, 50 µm. See also Table S1 and Figure S1.

Figure 3. Gr32a Is Not Required to Inhibit Interspecies Courtship but Is Essential for Quinine Sensing in *D. simulans*
(A) We tested whether, similar to *D. melanogaster* males, Gr32a inhibits interspecies courtship by *D. simulans* males. (B and C) WT and Gr32a mutant *D. simulans* males court conspecific but not *D. melanogaster* or *D. virilis* females. (D and E) WT and Gr32a mutant *D. simulans* males show similar low levels of courtship toward conspecific males. (F) We tested whether, similar to *D. melanogaster*, Gr32a inhibits feeding on quinine-containing food in *D. simulans*. (G) Schematic of feeding assay for starved *D. simulans* given choice of colored food containing sucrose or sucrose and quinine. Flies with blue, red, purple, or no food dye colored abdomens were enumerated after exposure to food for 90 min. (H) Significant decrease in preference by *Gr32a* mutant *D. simulans* for food containing only sucrose. Mean ± SEM. In (B)–(E), each circle denotes CI of one male, and n = 11–34 per genotype. In (G) and (H), preference index = {(# flies that ate sucrose-only food + 0.5*(purple flies)}/(number of flies that ate). Each circle denotes the preference index for one experiment. For each experiment, 106 ± 6 *D. simulans* of each genotype were used. n = 11–15 experiments/genotype. ***p < 0.001. See Tables S1–S3 and Figures S2 and S3.

**Figure 4. Ppk25 Promotes Conspecific Courtship by *D. simulans* Males**
(A) We tested whether, similar to *D. melanogaster*, Ppk25 promotes conspecific courtship by *D. simulans* males. (B–D) *Ppk25* mutant *D. simulans* males show decreased courtship index (C.I.) in dark (B) and bright illumination (D) and a reduction in high levels of C.I. in dark (C) but not bright illumination (E) toward conspecific females. (E) No difference between WT and *Ppk25* mutant *D. simulans* males in percentage assays with high levels of courtship of conspecific females. (F) Summary of the roles of Gr32a, Gr33a, and Ppk25 in *D. melanogaster* and *D. simulans*. Mean ± SEM. Each circle denotes CI for one male. n = 12–24 per genotype. ***p < 0.001. See Tables S1 and S3 and Figure S4.

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References

1. Allaire JJ, Cheng J, Xie Y, McPherson J, Chang W, Allen J, Wickham H, Atkins A, Hyndman R, and Arslan R (2017). rmarkdown: Dynamic Documents for R https://cran.r-project.org/web/packages/rmarkdown/index.html.
1. Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40, W597–W603. - PMC - PubMed
1. Baldwin MW, Toda Y, Nakagita T, O’Connell MJ, Klasing KC, Misaka T, Edwards SV, and Liberles SD (2014). Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345, 929–933. - PMC - PubMed
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1. Billeter J-C, Atallah J, Krupp JJ, Millar JG, and Levine JD (2009). Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987–991. - PubMed

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[1] Allaire JJ, Cheng J, Xie Y, McPherson J, Chang W, Allen J, Wickham H, Atkins A, Hyndman R, and Arslan R (2017). rmarkdown: Dynamic Documents for R https://cran.r-project.org/web/packages/rmarkdown/index.html.

[2] Allaire JJ, Cheng J, Xie Y, McPherson J, Chang W, Allen J, Wickham H, Atkins A, Hyndman R, and Arslan R (2017). rmarkdown: Dynamic Documents for R https://cran.r-project.org/web/packages/rmarkdown/index.html.

[3] Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40, W597–W603. - PMC - PubMed

[4] Artimo P, Jonnalagedda M, Arnold K, Baratin D, Csardi G, de Castro E, Duvaud S, Flegel V, Fortier A, Gasteiger E, et al. (2012). ExPASy: SIB bioinformatics resource portal. Nucleic Acids Res 40, W597–W603. - PMC - PubMed

[5] Baldwin MW, Toda Y, Nakagita T, O’Connell MJ, Klasing KC, Misaka T, Edwards SV, and Liberles SD (2014). Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345, 929–933. - PMC - PubMed

[6] Baldwin MW, Toda Y, Nakagita T, O’Connell MJ, Klasing KC, Misaka T, Edwards SV, and Liberles SD (2014). Sensory biology. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345, 929–933. - PMC - PubMed

[7] Bastock M, and Manning A (1955). The courtship of Drosophila melanogaster. Behaviour 8, 85–111.

[8] Bastock M, and Manning A (1955). The courtship of Drosophila melanogaster. Behaviour 8, 85–111.

[9] Billeter J-C, Atallah J, Krupp JJ, Millar JG, and Levine JD (2009). Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987–991. - PubMed

[10] Billeter J-C, Atallah J, Krupp JJ, Millar JG, and Levine JD (2009). Specialized cells tag sexual and species identity in Drosophila melanogaster. Nature 461, 987–991. - PubMed

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Evolution of Mechanisms that Control Mating in Drosophila Males

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Evolution of Mechanisms that Control Mating in Drosophila Males

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