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The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae

Viviparity, a reproductive form that supplies nutrients to the embryo during gestation, has repeatedly and independently occurred in multiple lineages of animals. During the convergent evolution of viviparity, various modifications of development, structure, and physiology emerged. A new species of...

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Autores principales: Yamashita, Tatsuya, Ekino, Taisuke, Kanzaki, Natsumi, Shinya, Ryoji
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10325857/
https://www.ncbi.nlm.nih.gov/pubmed/37427410
http://dx.doi.org/10.3389/fphys.2023.1197477
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author Yamashita, Tatsuya
Ekino, Taisuke
Kanzaki, Natsumi
Shinya, Ryoji
author_facet Yamashita, Tatsuya
Ekino, Taisuke
Kanzaki, Natsumi
Shinya, Ryoji
author_sort Yamashita, Tatsuya
collection PubMed
description Viviparity, a reproductive form that supplies nutrients to the embryo during gestation, has repeatedly and independently occurred in multiple lineages of animals. During the convergent evolution of viviparity, various modifications of development, structure, and physiology emerged. A new species of nematode, Tokorhabditis tufae, was discovered in the alkaline, hypersaline, and arsenic-rich environment of Mono lake. Its reproductive form is viviparity because it is obligately live-bearing and the embryo increases in size during development. However, the magnitude of the increase in size and nutrient provisioning are unclear. We measured egg and embryo sizes at three developmental stages in T. tufae. Eggs and embryos of T. tufae at the threefold stage were respectively 2.6- and 3.6-fold larger than at the single-cell stage. We then obtained T. tufae embryos at the single-cell, lima bean, and threefold developmental stages and investigated the egg hatching frequency at three different concentrations of egg salt buffer. Removal of embryos from the uterus halted embryonic development at the single-cell and lima bean stages in T. tufae irrespective of the solution used for incubation, indicating the provision of nutrients within the uterus. Ultrastructural and permeability evaluation showed that the permeability barrier did not form during embryonic development, resulting in increased molecular permeability. This high permeability caused by the absence of the permeability barrier likely enables supply of nutrients from the mother. The structural and physiological modifications in T. tufae are like those in other viviparous animals. We conclude that T. tufae is a viviparous rather than an ovoviviparous nematode. T. tufae will facilitate investigation of the evolution of viviparity in animals.
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spelling pubmed-103258572023-07-07 The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae Yamashita, Tatsuya Ekino, Taisuke Kanzaki, Natsumi Shinya, Ryoji Front Physiol Physiology Viviparity, a reproductive form that supplies nutrients to the embryo during gestation, has repeatedly and independently occurred in multiple lineages of animals. During the convergent evolution of viviparity, various modifications of development, structure, and physiology emerged. A new species of nematode, Tokorhabditis tufae, was discovered in the alkaline, hypersaline, and arsenic-rich environment of Mono lake. Its reproductive form is viviparity because it is obligately live-bearing and the embryo increases in size during development. However, the magnitude of the increase in size and nutrient provisioning are unclear. We measured egg and embryo sizes at three developmental stages in T. tufae. Eggs and embryos of T. tufae at the threefold stage were respectively 2.6- and 3.6-fold larger than at the single-cell stage. We then obtained T. tufae embryos at the single-cell, lima bean, and threefold developmental stages and investigated the egg hatching frequency at three different concentrations of egg salt buffer. Removal of embryos from the uterus halted embryonic development at the single-cell and lima bean stages in T. tufae irrespective of the solution used for incubation, indicating the provision of nutrients within the uterus. Ultrastructural and permeability evaluation showed that the permeability barrier did not form during embryonic development, resulting in increased molecular permeability. This high permeability caused by the absence of the permeability barrier likely enables supply of nutrients from the mother. The structural and physiological modifications in T. tufae are like those in other viviparous animals. We conclude that T. tufae is a viviparous rather than an ovoviviparous nematode. T. tufae will facilitate investigation of the evolution of viviparity in animals. Frontiers Media S.A. 2023-06-22 /pmc/articles/PMC10325857/ /pubmed/37427410 http://dx.doi.org/10.3389/fphys.2023.1197477 Text en Copyright © 2023 Yamashita, Ekino, Kanzaki and Shinya. 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 Physiology
Yamashita, Tatsuya
Ekino, Taisuke
Kanzaki, Natsumi
Shinya, Ryoji
The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title_full The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title_fullStr The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title_full_unstemmed The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title_short The developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, Tokorhabditis tufae
title_sort developmental and structural uniqueness of the embryo of the extremophile viviparous nematode, tokorhabditis tufae
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10325857/
https://www.ncbi.nlm.nih.gov/pubmed/37427410
http://dx.doi.org/10.3389/fphys.2023.1197477
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