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Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)

BACKGROUND: Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is stron...

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Autores principales: Dederichs, Tim M., Huber, Bernhard A., Michalik, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127419/
https://www.ncbi.nlm.nih.gov/pubmed/37170331
http://dx.doi.org/10.1186/s40850-022-00148-3
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author Dederichs, Tim M.
Huber, Bernhard A.
Michalik, Peter
author_facet Dederichs, Tim M.
Huber, Bernhard A.
Michalik, Peter
author_sort Dederichs, Tim M.
collection PubMed
description BACKGROUND: Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies. RESULTS: Our data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor. CONCLUSIONS: Our data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00148-3.
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spelling pubmed-101274192023-04-26 Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata) Dederichs, Tim M. Huber, Bernhard A. Michalik, Peter BMC Zool Research BACKGROUND: Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies. RESULTS: Our data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor. CONCLUSIONS: Our data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40850-022-00148-3. BioMed Central 2022-09-26 /pmc/articles/PMC10127419/ /pubmed/37170331 http://dx.doi.org/10.1186/s40850-022-00148-3 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Dederichs, Tim M.
Huber, Bernhard A.
Michalik, Peter
Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title_full Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title_fullStr Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title_full_unstemmed Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title_short Evolutionary morphology of sperm in pholcid spiders (Pholcidae, Synspermiata)
title_sort evolutionary morphology of sperm in pholcid spiders (pholcidae, synspermiata)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127419/
https://www.ncbi.nlm.nih.gov/pubmed/37170331
http://dx.doi.org/10.1186/s40850-022-00148-3
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