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Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process

Spiders have evolved a unique male copulatory organ, the pedipalp bulb. The morphology of the bulb is species specific and plays an important role in species recognition and prezygotic reproductive isolation. Despite its importance for spider biodiversity, the mechanisms that control bulb developmen...

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Autores principales: Quade, Felix Simon Christian, Holtzheimer, Jana, Frohn, Jasper, Töpperwien, Mareike, Salditt, Tim, Prpic, Nikola-Michael
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6502807/
https://www.ncbi.nlm.nih.gov/pubmed/31061504
http://dx.doi.org/10.1038/s41598-019-43192-9
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author Quade, Felix Simon Christian
Holtzheimer, Jana
Frohn, Jasper
Töpperwien, Mareike
Salditt, Tim
Prpic, Nikola-Michael
author_facet Quade, Felix Simon Christian
Holtzheimer, Jana
Frohn, Jasper
Töpperwien, Mareike
Salditt, Tim
Prpic, Nikola-Michael
author_sort Quade, Felix Simon Christian
collection PubMed
description Spiders have evolved a unique male copulatory organ, the pedipalp bulb. The morphology of the bulb is species specific and plays an important role in species recognition and prezygotic reproductive isolation. Despite its importance for spider biodiversity, the mechanisms that control bulb development are virtually unknown. We have used confocal laser scanning microscopy (CLSM) and diffusible iodine-based contrast-enhanced micro computed tomography (dice-µCT) to study bulb development in the spider Parasteatoda tepidariorum. These imaging technologies enabled us to study bulb development in situ, without the use of destructive procedures for the first time. We show here that the inflated pedipalp tip in the subadult stage is filled with haemolymph that rapidly coagulates. Coagulation indicates histolytic processes that disintegrate tibia and tarsus, similar to histolytic processes during metamorphosis in holometabolous insects. The coagulated material contains cell inclusions that likely represent the cell source for the re-establishment of tarsus and tibia after histolysis, comparable to the histoblasts in insect metamorphosis. The shape of the coagulated mass prefigures the shape of the adult tarsus (cymbium) like a blueprint for the histoblasts. This suggests a unique role for controlled coagulation after histolysis in the metamorphosis-like morphogenesis of the male pedipalp.
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spelling pubmed-65028072019-05-20 Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process Quade, Felix Simon Christian Holtzheimer, Jana Frohn, Jasper Töpperwien, Mareike Salditt, Tim Prpic, Nikola-Michael Sci Rep Article Spiders have evolved a unique male copulatory organ, the pedipalp bulb. The morphology of the bulb is species specific and plays an important role in species recognition and prezygotic reproductive isolation. Despite its importance for spider biodiversity, the mechanisms that control bulb development are virtually unknown. We have used confocal laser scanning microscopy (CLSM) and diffusible iodine-based contrast-enhanced micro computed tomography (dice-µCT) to study bulb development in the spider Parasteatoda tepidariorum. These imaging technologies enabled us to study bulb development in situ, without the use of destructive procedures for the first time. We show here that the inflated pedipalp tip in the subadult stage is filled with haemolymph that rapidly coagulates. Coagulation indicates histolytic processes that disintegrate tibia and tarsus, similar to histolytic processes during metamorphosis in holometabolous insects. The coagulated material contains cell inclusions that likely represent the cell source for the re-establishment of tarsus and tibia after histolysis, comparable to the histoblasts in insect metamorphosis. The shape of the coagulated mass prefigures the shape of the adult tarsus (cymbium) like a blueprint for the histoblasts. This suggests a unique role for controlled coagulation after histolysis in the metamorphosis-like morphogenesis of the male pedipalp. Nature Publishing Group UK 2019-05-06 /pmc/articles/PMC6502807/ /pubmed/31061504 http://dx.doi.org/10.1038/s41598-019-43192-9 Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Quade, Felix Simon Christian
Holtzheimer, Jana
Frohn, Jasper
Töpperwien, Mareike
Salditt, Tim
Prpic, Nikola-Michael
Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title_full Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title_fullStr Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title_full_unstemmed Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title_short Formation and development of the male copulatory organ in the spider Parasteatoda tepidariorum involves a metamorphosis-like process
title_sort formation and development of the male copulatory organ in the spider parasteatoda tepidariorum involves a metamorphosis-like process
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6502807/
https://www.ncbi.nlm.nih.gov/pubmed/31061504
http://dx.doi.org/10.1038/s41598-019-43192-9
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