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. 2013 Jul 3;154(1):89-102.
doi: 10.1016/j.cell.2013.06.008. Epub 2013 Jun 27.

Genetic and neural mechanisms that inhibit Drosophila from mating with other species

Pu Fan  1 , Devanand S Manoli, Osama M Ahmed, Yi Chen, Neha Agarwal, Sara Kwong, Allen G Cai, Jeffrey Neitz, Adam Renslo, Bruce S Baker, Nirao M Shah
Affiliations

Genetic and neural mechanisms that inhibit Drosophila from mating with other species

Pu Fan et al. Cell. .

Abstract

Genetically hard-wired neural mechanisms must enforce behavioral reproductive isolation because interspecies courtship is rare even in sexually naïve animals of most species. We find that the chemoreceptor Gr32a inhibits male D. melanogaster from courting diverse fruit fly species. Gr32a recognizes nonvolatile aversive cues present on these reproductively dead-end targets, and activity of Gr32a neurons is necessary and sufficient to inhibit interspecies courtship. Male-specific Fruitless (Fru(M)), a master regulator of courtship, also inhibits interspecies courtship. Gr32a and Fru(M) are not coexpressed, but Fru(M) neurons contact Gr32a neurons, suggesting that these genes influence a shared neural circuit that inhibits interspecies courtship. Gr32a and Fru(M) also suppress within-species intermale courtship, but we show that distinct mechanisms preclude sexual displays toward conspecific males and other species. Although this chemosensory pathway does not inhibit interspecies mating in D. melanogaster females, similar mechanisms appear to inhibit this behavior in many other male drosophilids.

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Figures

Figure 1
Figure 1. The foreleg tarsi inhibit courtship of other species
(A)Overview of D. melanogaster male courtship behaviors and their likely sensory control. (B, G) WT D. melanogaster males were provided with either conspecific or D. virilis females. (C, H) Males lacking labellum, maxillary palps, antennae, or visible light court conspecific but not D. virilis females. Males lacking foreleg tarsi court conspecific and D. virilis females. (D, I) Males lacking foreleg tarsi show high levels of courtship towards conspecific and D. virilis females in the majority of assays. (E, J) Males lacking foreleg tarsi attempt to copulate with conspecific and D. virilis females. (F, K) Males lacking foreleg tarsi attempt copulation with conspecific and D. virilis females in most assays. Mean ± SEM; n ≥ 11/experimental cohort; ‡ p < 0.001.
Figure 2
Figure 2. Identification of Gr neurons in the male foreleg that inhibit interspecies courting
(A–H’) Expression of different Grs (A–H) and ablation of Gr neurons (A’–H’) in foreleg tarsi. Whole-mount preparation of tarsal segments 4 and 5 (t4, t5) (A, A’ and C–H’) and t2 (B, B’) shown. More distal tarsal segments are on the left. (I) Ablation of Gr32a or Gr33a neurons in D. melanogaster males permits courting of D. virilis females. All statistical comparisons in this and subsequent figures were performed between experimental and the corresponding control genotypes. Mean ± SEM; n = 5–10/genotype (A–H’) and n = 8–12/genotype (I); ‡ p < 0.001; scale bar = 50 µm. Please see Supplemental Figure S1 and Table S1.
Figure 3
Figure 3. Ablation of Gr32a or Gr33a neurons permits courting of females of other species
D. melanogaster males with ablation of Gr32a or Gr33a neurons (Gr:hid) were tested for courtship with females. Last common ancestor (Evolutionary Divergence) shared with D. melanogaster shown as mya (not to scale) above the bar graphs. (A–D) Ablation of Gr32a or Gr33a neurons does not alter courtship of conspecific females. (E–P) Ablation of Gr32a or Gr33a neurons permits courtship of D. simulans (E–H), D. yakuba (I–L), and D. virilis (M–P) females. Mean ± SEM; n = 10–24/genotype; * p < 0.05, ¶ p < 0.01, ‡ p < 0.001.
Figure 4
Figure 4. Gr32a inhibits interspecies courtship
Gr32a and Gr33a mutant and control D. melanogaster males were tested for courtship with females. (A–D) No difference in courting conspecific females between control and Gr32a or Gr33a mutants. (E–P) Gr32a, but not Gr33a, mutants court D. simulans (E–H), D. yakuba (I–L), and D. virilis (M–P) females. Mean ± SEM; n = 10–24/genotype; * p < 0.05, ‡ p < 0.001; NS = not significant. Please see Supplemental Figure S2 and Movies S1–S3.
Figure 5
Figure 5. Gr32a neurons inhibit interspecies courtship by recognizing cuticular hydrocarbons found on other species
D. melanogaster males WT (A, C) or mutant for Gr32a (B, D) were tested for courtship with conspecific or D. virilis females. (A) Inactivation of synaptic release by Gr32a neurons (Gr32a:shits) at the restrictive temperature (31°C) does not alter courtship of conspecific females. (B) Increase in electrical activity in Gr32a neurons (Gr32a:dTrpA1) at 31°C does not alter courtship of conspecific females. (C) Inactivation of synaptic release by Gr32a neurons permits courtship of D. virilis females by Gr32a:shits males. (D) Increase in electrical activity in Gr32a neurons abrogates courtship of D. virilis females by Gr32a−/−, Gr32a:dTrpA1 males. (E) Gr32a−/− males court oe– conspecific females coated with cuticular extracts from D. melanogaster (D.m.), simulans (D.s.), yakuba (D.y.), and virilis (D.v.) as well as with specific CHs present on these species. Mean ± SEM; n = 10–16/genotype; * p < 0.05, ‡ p < 0.001. Please see Supplemental Figure S3.
Figure 6
Figure 6. A cellular and molecular pathway that inhibits interspecies courtship
(A) fru1/fru4–40 males court conspecific females and females of other species. (B–D”) No co-expression of FruM and Gr32a in foreleg tarsi of D. melanogaster males (D). A cell that appears co-labeled for FruM and Gr32a in a Z-projected image (arrow in D) in fact represents two distinct cells in different optical slices expressing either FruM (B”–D”) or Gr32a (B’–D’) but not both. (Lines used: frulex, lexO-stingerGFP(line E,F) and Gr32a-GAL4, UAS-tdTomato; abbreviated to frulex:stingerGFP, Gr32a:tdTomato.) (E) Schematic of the fly central nervous system shows the location of the SOG and first thoracic segment (T1) VNC (red boxes). (F–I) Native GRASP fluorescence (green) in the vertical limb of the SOG and the T1 VNC in D. melanogaster males (Gr32a:spGFP1-10∷Nrx, frulex:spGFP11∷CD4) is lost upon T1 tarsectomy. The neuropil (magenta) is immunolabeled with nc82. (J) Knockdown of FruM in male aDT6 neurons (P52A:fruMIR) permits courtship of conspecific females and females of other species. Mean ± SEM; n = 10–31/experimental cohort; ¶ p < 0.01, ‡ p < 0.001; scale bar = 20 µm. Please see Supplemental Figure S4, Table S2, and Movie S4.
Figure 7
Figure 7. Sexually dimorphic but evolutionarily conserved regulation of interspecies courtship
(A, B) Tarsiless D. simulans and yakuba males court D. melanogaster females similar to conspecific males. (C–E) D. melanogaster females reject courtship by D. simulans males with wing flicks, kicks, and ovipositor extrusions. (F–H) D. melanogaster females reject courtship by D. yakuba males with wing flicks, kicks, and ovipositor extrusions. Mean ± SEM; n = 11–18/experimental cohort; * p < 0.05; ‡ p < 0.001. Please see Supplemental Movies S5–S7.
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Comment in

  • Interspecies sex and taste.
    Koh TW, Carlson JR. Koh TW, et al. Cell. 2013 Jul 3;154(1):20-1. doi: 10.1016/j.cell.2013.06.015. Cell. 2013. PMID: 23827670 Free PMC article.

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