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Are superficial neuromasts proprioceptors underlying fast copulatory behavior?

In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemi...

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Autores principales: Martinez-Rivera, Noraida, Serrano-Velez, Jose L., Torres-Vazquez, Irma I., Langerhans, R. Brian, Rosa-Molinar, Eduardo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446510/
https://www.ncbi.nlm.nih.gov/pubmed/36082109
http://dx.doi.org/10.3389/fncir.2022.921568
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author Martinez-Rivera, Noraida
Serrano-Velez, Jose L.
Torres-Vazquez, Irma I.
Langerhans, R. Brian
Rosa-Molinar, Eduardo
author_facet Martinez-Rivera, Noraida
Serrano-Velez, Jose L.
Torres-Vazquez, Irma I.
Langerhans, R. Brian
Rosa-Molinar, Eduardo
author_sort Martinez-Rivera, Noraida
collection PubMed
description In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemination. Therefore, the repositioning of these structures and organ relied on the reorganization of the efferent circuitry that controls spinal motor neurons innervating appendicular muscles critical for the movement of the gonopodium, including the fast and synchronous torque-trust motion during insemination attempts. Copulation occurs when a male positions himself largely outside a female’s field of view, circumducts his gonopodium, and performs a rapid, complex maneuver to properly contact the female urogenital sinus with the distal tip of the gonopodium and transfers sperm. Although understanding of the efferent circuitry has significantly increased in the last 24 years, nothing is known about the cutaneous receptors involved in gonopodium movement, or how the afferent signals are processed to determine the location of this organ during copulation. Using Western mosquitofish, Gambusia affinis, as our model, we attempt to fill this gap in knowledge. Preliminary data showed cutaneous nerves and sensory neurons innervating superficial neuromasts surrounding the base of adult male gonopodium; those cutaneous nerves projected ventrally from the spinal cord through the 14th dorsal root ganglion and its corresponding ventral root towards the base and fin rays of the gonopodium. We asked what role the cutaneous superficial neuromasts play in controlling the positioning and timing of the gonopodium’s fast and synchronous movements for effective sperm transfer. First, we found a greater number of superficial neuromasts surrounding the base of the male’s gonopodium compared to the base of the female’s anal fin. Second, we systemically removed superficial neuromasts surrounding the gonopodium base and observed significant impairment of the positioning and timing of gonopodial movements. Our findings provide a first step to supporting the following hypothesis: during radical reorganization of the Poeciliid body plan, superficial neuromasts have been partially co-opted as proprioceptors that allow the gonopodium to control precise positioning and timing during copulatory attempts.
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spelling pubmed-94465102022-09-07 Are superficial neuromasts proprioceptors underlying fast copulatory behavior? Martinez-Rivera, Noraida Serrano-Velez, Jose L. Torres-Vazquez, Irma I. Langerhans, R. Brian Rosa-Molinar, Eduardo Front Neural Circuits Neuroscience In male Poeciliid fishes, the modified anal fin (i.e., gonopodium) and its axial and appendicular support are repositioned within the axial skeleton, creating a novel sexually dimorphic ano-urogenital region. During copulation, the relative location of the gonopodium is crucial for successful insemination. Therefore, the repositioning of these structures and organ relied on the reorganization of the efferent circuitry that controls spinal motor neurons innervating appendicular muscles critical for the movement of the gonopodium, including the fast and synchronous torque-trust motion during insemination attempts. Copulation occurs when a male positions himself largely outside a female’s field of view, circumducts his gonopodium, and performs a rapid, complex maneuver to properly contact the female urogenital sinus with the distal tip of the gonopodium and transfers sperm. Although understanding of the efferent circuitry has significantly increased in the last 24 years, nothing is known about the cutaneous receptors involved in gonopodium movement, or how the afferent signals are processed to determine the location of this organ during copulation. Using Western mosquitofish, Gambusia affinis, as our model, we attempt to fill this gap in knowledge. Preliminary data showed cutaneous nerves and sensory neurons innervating superficial neuromasts surrounding the base of adult male gonopodium; those cutaneous nerves projected ventrally from the spinal cord through the 14th dorsal root ganglion and its corresponding ventral root towards the base and fin rays of the gonopodium. We asked what role the cutaneous superficial neuromasts play in controlling the positioning and timing of the gonopodium’s fast and synchronous movements for effective sperm transfer. First, we found a greater number of superficial neuromasts surrounding the base of the male’s gonopodium compared to the base of the female’s anal fin. Second, we systemically removed superficial neuromasts surrounding the gonopodium base and observed significant impairment of the positioning and timing of gonopodial movements. Our findings provide a first step to supporting the following hypothesis: during radical reorganization of the Poeciliid body plan, superficial neuromasts have been partially co-opted as proprioceptors that allow the gonopodium to control precise positioning and timing during copulatory attempts. Frontiers Media S.A. 2022-08-23 /pmc/articles/PMC9446510/ /pubmed/36082109 http://dx.doi.org/10.3389/fncir.2022.921568 Text en Copyright © 2022 Martinez-Rivera, Serrano-Velez, Torres-Vazquez, Langerhans and Rosa-Molinar. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Martinez-Rivera, Noraida
Serrano-Velez, Jose L.
Torres-Vazquez, Irma I.
Langerhans, R. Brian
Rosa-Molinar, Eduardo
Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title_full Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title_fullStr Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title_full_unstemmed Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title_short Are superficial neuromasts proprioceptors underlying fast copulatory behavior?
title_sort are superficial neuromasts proprioceptors underlying fast copulatory behavior?
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9446510/
https://www.ncbi.nlm.nih.gov/pubmed/36082109
http://dx.doi.org/10.3389/fncir.2022.921568
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