Distinct Neuronal Circuits in the Brain and Ventral Nerve Cord Sense Sex Peptide to Induce Post-Mating Responses in Drosophila Females

Core Concepts

Distinct sets of interneurons in the central brain and ventral nerve cord sense the male-derived sex peptide to induce the main post-mating responses in female Drosophila, including reduced receptivity to re-mate and increased egg-laying.

Abstract

The study identifies distinct neuronal populations in the central brain and ventral nerve cord of female Drosophila that can sense the male-derived sex peptide and induce the main post-mating responses.
Key highlights:

Expression of membrane-tethered sex peptide (mSP) in the head or trunk of females can separately induce reduced receptivity or increased egg-laying, respectively, indicating distinct neuronal circuits control these two post-mating responses.
Analysis of regulatory regions in the sex peptide receptor (SPR), fruitless (fru), and doublesex (dsx) genes identified a few restricted neuronal populations in the brain and ventral nerve cord that can induce post-mating responses when expressing mSP.
Intersectional expression using split-GAL4 further refined these neuronal populations, revealing five distinct sets of interneurons in the central brain and ventral nerve cord that can sense sex peptide and induce post-mating responses.
Mapping the pre- and post-synaptic connections of these sex peptide-responsive neurons using retro- and trans-Tango techniques showed they integrate higher-order sensory processing in the brain and converge onto common output pathways.
The results indicate sex peptide interferes with the integration of diverse sensory inputs at the level of interneurons to generate the stereotyped post-mating behavioral outputs.

Stats

"Expression of membrane-tethered SP (mSP) in the head or trunk either reduces receptivity or increases oviposition, respectively."
"From all the 74 lines that we have analyzed for PMRs from SPR, fru and dsx genes, we also analysed expression in genital tract sensory neurons as they had been postulated to be the primary targets of SP."
"Again, intersection of SPR8 with fru11/12, dsx or FD6, and fru11/12 with dsx or FD6 expression robustly reduced receptivity and increased egg laying upon expression of mSP."
"When we inhibited neuronal activity by expression of TNT, we observed a significant reduction of receptivity for all split-Gal4 combinations, though only partially for inhibition in fru11/12 ∩ FD6 neurons."

Quotes

"Essentially, these results are consistent with previous findings that inhibitory neurons prevail (Nallasivan et al., 2021), possibly as input from trunk neurons as found for ppk expressing neurons (see below)."
"Taken together, circuitries identified via retro- and trans-Tango place SP target neurons at the interface of sensory processing interneurons connecting to two commonly shared post-synaptic processing neuronal populations in the brain. Hence, our data indicate that SP interferes with sensory input processing from multiple modalities that are canalized to higher order processing centres to generate a behavioural output."
"Hence, the architecture of female PMRs contrasts with male-courtship behavior consisting of a sequel of behavioral elements that once initiated will always follow stereotypically to the end culminating in mating, or start from the beginning when interrupted."

Key Insights Distilled From

Sex-peptide targets distinct higher order processing neurons in the brain to induce the female post-mating response

by Nallasivan,M... at www.biorxiv.org 04-28-2024

https://www.biorxiv.org/content/10.1101/2024.04.24.590874v1

Deeper Inquiries

How do the identified neuronal circuits integrate and process sensory information from different modalities to coordinate the post-mating responses?

The identified neuronal circuits integrate and process sensory information from different modalities to coordinate post-mating responses by operating as key integrators of sensory information for decision-making in behavioral outputs. The study revealed that distinct interneurons in the brain and abdominal ganglion play a crucial role in controlling receptivity and oviposition in response to sex peptide (SP) signaling. These interneurons receive sensory inputs from various modalities, such as vision, hearing, smell, taste, and touch, and process this information to generate a coordinated behavioral response. The intersectional expression of membrane-tethered SP in specific neuronal populations allows for the modulation of sensory cues and the integration of diverse inputs to produce a stereotyped output, including reducing receptivity and inducing egg laying. The circuitry identified in the study suggests that SP interferes with the interpretation of sensory cues at different sites in the brain, leading to the coordination of post-mating responses.

How do females modulate the post-mating responses under varying physiological and environmental conditions to maximize their reproductive success?

Females modulate post-mating responses under varying physiological and environmental conditions to maximize their reproductive success by adjusting SP-mediated male manipulation based on specific factors. The study indicates that females have the ability to counteract male manipulation at the level of sensory perception to adapt to different physiological states and environmental cues. For example, females may adjust their response to SP signaling based on the availability of suitable egg-laying substrates or the presence of potential threats, such as parasitoid wasps. The multi-modularity of SP target neurons allows females to fine-tune their behavioral responses to ensure optimal reproductive success. By modulating the post-mating responses, females can prioritize egg laying, reject courting males, and adjust their behavior based on external conditions to enhance their reproductive fitness. This adaptive flexibility in response to SP signaling enables females to optimize their reproductive outcomes in dynamic and changing environments.

What are the potential mechanisms by which sex peptide signaling interferes with the activity of these interneurons to induce the post-mating behavioral changes?

Sex peptide signaling interferes with the activity of interneurons to induce post-mating behavioral changes through a complex mechanism involving the modulation of sensory processing and integration in the brain. The study identified specific neuronal populations that are responsive to SP signaling and play a critical role in coordinating post-mating responses. SP likely acts on these interneurons by binding to the Sex Peptide Receptor (SPR), triggering a cascade of intracellular events that alter neuronal activity and neurotransmitter release. By targeting distinct interneurons in the brain and ventral nerve cord, SP can modulate the processing of sensory information from different modalities, such as visual, auditory, olfactory, gustatory, and tactile cues.
The interference of SP with sensory processing likely involves the modulation of synaptic transmission, neurotransmitter release, and neuronal excitability within the identified circuits. SP may influence the synaptic connectivity and plasticity of these interneurons, leading to changes in their responsiveness to sensory stimuli and the generation of appropriate behavioral outputs. Additionally, SP signaling may involve the activation or inhibition of specific signaling pathways within the interneurons, altering their firing patterns and activity levels to drive the post-mating responses. Overall, the mechanisms by which SP interferes with interneuronal activity likely involve complex interactions at the molecular, cellular, and circuit levels to coordinate the behavioral changes observed in response to mating.