Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila

Abstract Peripheral sensory neurons are the gateway to the environment across species. In Drosophila, olfactory and gustatory senses are required to initiate courtship, as well as for the escalation of courtship patterns that lead to copulation. To be successful, copulation must last long enough to...

Full description

Bibliographic Details
Main Authors: Shreyas Jois, Yick-Bun Chan, Maria Paz Fernandez, Narsimha Pujari, Lea Joline Janz, Sarah Parker, Adelaine Kwun-Wai Leung
Format: Article
Language:English
Published: Nature Portfolio 2022-04-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-022-10247-3
_version_ 1818480585350316032
author Shreyas Jois
Yick-Bun Chan
Maria Paz Fernandez
Narsimha Pujari
Lea Joline Janz
Sarah Parker
Adelaine Kwun-Wai Leung
author_facet Shreyas Jois
Yick-Bun Chan
Maria Paz Fernandez
Narsimha Pujari
Lea Joline Janz
Sarah Parker
Adelaine Kwun-Wai Leung
author_sort Shreyas Jois
collection DOAJ
description Abstract Peripheral sensory neurons are the gateway to the environment across species. In Drosophila, olfactory and gustatory senses are required to initiate courtship, as well as for the escalation of courtship patterns that lead to copulation. To be successful, copulation must last long enough to ensure the transfer of sperm and seminal fluid that ultimately leads to fertilization. The peripheral sensory information required to regulate copulation duration is unclear. Here, we employed genetic manipulations that allow driving gene expression in the male genitalia as a tool to uncover the role of these genitalia specific neurons in copulation. The fly genitalia contain sex-specific bristle hairs innervated by mechanosensory neurons. To date, the role of the sensory information collected by these peripheral neurons in male copulatory behavior is unknown. We confirmed that these MSNs are cholinergic and co-express both fru and dsx. We found that the sensory information received by the peripheral sensory neurons from the front legs (GRNs) and mechanosensory neurons (MSNs) at the male genitalia contribute to the regulation of copulation duration. Moreover, our results show that their function is required for copulation persistence, which ensures copulation is undisrupted in the presence of environmental stress before sperm transfer is complete.
first_indexed 2024-12-10T11:25:25Z
format Article
id doaj.art-0f9e613ec7c941e0abaf321a0bfd3cbd
institution Directory Open Access Journal
issn 2045-2322
language English
last_indexed 2024-12-10T11:25:25Z
publishDate 2022-04-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj.art-0f9e613ec7c941e0abaf321a0bfd3cbd2022-12-22T01:50:45ZengNature PortfolioScientific Reports2045-23222022-04-0112111210.1038/s41598-022-10247-3Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male DrosophilaShreyas Jois0Yick-Bun Chan1Maria Paz Fernandez2Narsimha Pujari3Lea Joline Janz4Sarah Parker5Adelaine Kwun-Wai Leung6Department of Veterinary Biomedical Sciences, WCVM, University of SaskatchewanDepartment of Neurobiology, Harvard Medical SchoolDepartment of Neuroscience and Behavior, Barnard CollegeDepartment of Veterinary Biomedical Sciences, WCVM, University of SaskatchewanDepartment of Veterinary Biomedical Sciences, WCVM, University of SaskatchewanCentre for Applied Epidemiology, Large Animal Clinical Science, WCVM, University of SaskatchewanDepartment of Veterinary Biomedical Sciences, WCVM, University of SaskatchewanAbstract Peripheral sensory neurons are the gateway to the environment across species. In Drosophila, olfactory and gustatory senses are required to initiate courtship, as well as for the escalation of courtship patterns that lead to copulation. To be successful, copulation must last long enough to ensure the transfer of sperm and seminal fluid that ultimately leads to fertilization. The peripheral sensory information required to regulate copulation duration is unclear. Here, we employed genetic manipulations that allow driving gene expression in the male genitalia as a tool to uncover the role of these genitalia specific neurons in copulation. The fly genitalia contain sex-specific bristle hairs innervated by mechanosensory neurons. To date, the role of the sensory information collected by these peripheral neurons in male copulatory behavior is unknown. We confirmed that these MSNs are cholinergic and co-express both fru and dsx. We found that the sensory information received by the peripheral sensory neurons from the front legs (GRNs) and mechanosensory neurons (MSNs) at the male genitalia contribute to the regulation of copulation duration. Moreover, our results show that their function is required for copulation persistence, which ensures copulation is undisrupted in the presence of environmental stress before sperm transfer is complete.https://doi.org/10.1038/s41598-022-10247-3
spellingShingle Shreyas Jois
Yick-Bun Chan
Maria Paz Fernandez
Narsimha Pujari
Lea Joline Janz
Sarah Parker
Adelaine Kwun-Wai Leung
Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
Scientific Reports
title Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
title_full Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
title_fullStr Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
title_full_unstemmed Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
title_short Sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male Drosophila
title_sort sexually dimorphic peripheral sensory neurons regulate copulation duration and persistence in male drosophila
url https://doi.org/10.1038/s41598-022-10247-3
work_keys_str_mv AT shreyasjois sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT yickbunchan sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT mariapazfernandez sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT narsimhapujari sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT leajolinejanz sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT sarahparker sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila
AT adelainekwunwaileung sexuallydimorphicperipheralsensoryneuronsregulatecopulationdurationandpersistenceinmaledrosophila