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. 2013 Oct 2;280(1771):20131938.
doi: 10.1098/rspb.2013.1938. Print 2013 Nov 22.

Multiple Pathways Mediate the Sex-Peptide-Regulated Switch in Female Drosophila Reproductive Behaviours

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Free PMC article

Multiple Pathways Mediate the Sex-Peptide-Regulated Switch in Female Drosophila Reproductive Behaviours

Irmgard U Haussmann et al. Proc Biol Sci. .
Free PMC article

Abstract

Male-derived sex-peptide (SP) induces profound changes in the behaviour of Drosophila females, resulting in decreased receptivity to further mating and increased egg laying. SP can mediate the switch in female reproductive behaviours via a G protein-coupled receptor, SPR, in neurons expressing fruitless, doublesex and pickpocket. Whether SPR is the sole receptor and whether SP induces the postmating switch in a single pathway has not, to our knowledge been tested. Here we report that the SP response can be induced in the absence of SPR when SP is ectopically expressed in neurons or when SP, transferred by mating, can access neurons through a leaky blood brain barrier. Membrane-tethered SP can induce oviposition via doublesex, but not fruitless and pickpocket neurons in SPR mutant females. Although pickpocket and doublesex neurons rely on G(o) signalling to reduce receptivity and induce oviposition, G(o) signalling in fruitless neurons is required only to induce oviposition, but not to reduce receptivity. Our results show that SP's action in reducing receptivity and inducing oviposition can be separated in fruitless and doublesex neurons. Hence, the SP-induced postmating switch incorporates shared, but also distinct circuitry of fruitless, doublesex and pickpocket neurons and additional receptors.

Keywords: blood brain barrier; neurohormonal signalling; sex-peptide; sex-peptide targets; sexual behaviour.

Figures

Figure 1.
Figure 1.
Neuronally expressed SP reduces receptivity and increases oviposition in SPR mutant females. (a) Receptivity of wild-type and SPR/Df virgin and mated females and females expressing the SP gene under the yp1 promoter secreting SP to the haemolymph (YPhsSPg, haemolymph SP) or under the neuron-specific elav promoter secreting SP from neurons (elavSP, neuronal SP), or the non-functional SP-SA mutant under the elav promoter (elavSPmut) in wild-type and SPR/Df background was measured seven hours after mating or in virgins of YPhsSPg, elavSP and elavSPmut by counting mating females in a 1 h time period. Means with the standard error for three experiments with 18–21 females each are shown. Statistically significant differences are indicated by asterisks (***p < 0.0001). (b) Oviposition of wild-type and SPR/Df virgin and mated females and females expressing the SP gene under the yp1 promoter secreting SP to the haemolymph (YPhsSPg, haemolymph SP) or under the neuron-specific elav promoter secreting SP from neurons (elavSP, neuronal SP), or the non-functional SP-SA mutant under the elav promoter (elavSPmut) in wild-type and SPR/Df background is shown as means of eggs laid in 18 h for 20 females each with the standard error. Statistically significant differences are indicated by asterisks (***p ≤ 0.0001).
Figure 2.
Figure 2.
A leaky BBB rescues receptivity and oviposition in SPR mutant females after mating and SP injection. (a) Receptivity of wild-type and SPR/Df virgin and mated females with and without a leaky BBB (repoGAL4 UAS moody RNAi) was measured 7 h after mating with wild-type or SP-deficient males (SP0) by counting mating females in a 1 h time period. Means with the standard error for three experiments with 18–21 females each are shown. Statistically significant differences are indicated by asterisks (***p < 0.0001). (b) Oviposition of wild-type and SPR/Df virgin and mated females with and without a leaky BBB (repoGAL4 UAS moody RNAi) is shown as means of eggs laid in 18 h for 10 females each with the standard error, except for SPR/Df, which were 20 females. Statistically significant differences are indicated by asterisks (***p < 0.0001).
Figure 3.
Figure 3.
SP induces oviposition via dsx neurons in SPR mutant females. (a) Receptivity of virgin or mated wild-type females, and of virgin females expressing mSP in ppk, fru and dsx patterns in wild-type or SPR/Df background was measured 7 h after mating by counting mating females in a 1 h time period. Means with the standard error for three experiments with 15–21 females each are shown. Statistically significant differences are indicated by asterisks (***p < 0.0001). (b) Oviposition of virgin or mated wild-type females, and of virgin females expressing mSP in ppk, fru and dsx patterns in wild-type or SPR/Df background is shown as means of eggs laid in 18 h for 10 females each with the standard error, except for virgin and mated SPR/Df, which were 20 females. Statistically significant differences are indicated by asterisks (***p < 0.0001).
Figure 4.
Figure 4.
fru neurons are distinct from ppk and dsx neurons in regulating receptivity. (a) Receptivity of Ringer's and SP (3 pmol) injected mature virgin females (3–5 days) conditionally expressing PTX (induced by doxycycline for 1 day) in control (GMR) or in ppk, fru and dsx patterns was measured 5 h after injection by counting mating females in a 1 h time period. Means with the standard error for three experiments with 18–21 females each are shown. Statistically significant differences are indicated by asterisks (***p < 0.0001). (b) Oviposition of Ringer's and SP (3 pmol) injected mature virgin females (3–5 days) conditionally expressing PTX (induced by doxycycline for 1 day) in control (GMR) or in ppk, fru and dsx patterns is shown as means of eggs laid in 18 h for 10 females each with the standard error. Statistically significant differences are indicated by asterisks (***p < 0.0001).

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