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Evidence of hermaphroditism and sex ratio distortion in the fungal feeding nematode Bursaphelenchus okinawaensis

Shinya, Ryoji and Hasegawa, Koichi and Chen, Anthony and Kanzaki, Natsumi and Sternberg, Paul W. (2014) Evidence of hermaphroditism and sex ratio distortion in the fungal feeding nematode Bursaphelenchus okinawaensis. G3, 4 (10). pp. 1907-1917. ISSN 2160-1836. PMCID PMC4199697. doi:10.1534/g3.114.012385. https://resolver.caltech.edu/CaltechAUTHORS:20140820-084833184

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Abstract

Nematodes have many different reproductive strategies along with their divergent life-histories; the ability of hermaphrodite to self- and cross-fertilize is useful for genetic manipulation. Here, we demonstrate the hermaphroditism of the fungal feeding nematode Bursaphelenchus okinawaensis, which was formerly described as a parthenogenetic nematode, and we show its other unique sexual characteristics. To determine that it is hermaphroditic, we performed the following experiments: 1) observation of the pronuclear and chromosome behavior during oogenesis and early embryogenesis; 2) observation of spermatogenesis during the fourth larval stage; 3) investigation of sperm utilization; and 4) investigation of phenotypic segregation after cross-mating using an chemically-induced visible mutant. We then investigated the mating preferences and spermatid size difference between males and hermaphrodites. B. okinawaensis males successfully mated only with sperm-depleted old hermaphrodites, and the spermatid sizes of males were almost the same as those of hermaphrodites. Moreover, the sex ratio of cross-fertilized progeny was highly skewed toward hermaphrodites. B. okinawaensis is phylogenetically distant from established model nematodes such as C. elegans and is more closely related to some economically relevant parasitic nematodes. This newly discovered hermaphroditic nematode has great potential for evolutionary and parasitological research.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://www.g3journal.org/content/early/2014/08/12/g3.114.012385.abstractPublisherArticle
http://dx.doi.org/10.1534/g3.114.012385DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4199697/PubMed CentralArticle
ORCID:
AuthorORCID
Chen, Anthony0000-0002-9578-4893
Kanzaki, Natsumi0000-0001-8752-1674
Sternberg, Paul W.0000-0002-7699-0173
Alternate Title:Hermaphroditism and sexual conflict
Additional Information:© 2014 Author et al. This is an open-access article distributed under the terms of the Creative Commons Attribution Unported License (http://creativecommons.org/licenses/by/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Received May 28, 2014. Accepted August 1, 2014. Early Online August 12, 2014. We thank Gladys Medina for technical assistance; Kazuki Sato and Sota Ozawa for help in collecting insects on Ishigaki Island; members of the Sternberg laboratory for helpful discussions; Hillel Schwartz and Daniel Leighton for critical review and helpful comments; Andres Collazo for help in confocal imaging; and Jonathan Hodgkin and Tim Schedl for nomenclature discussions. Imaging was performed in the Biological Imaging Facility, with the support of the Caltech Beckman Institute and the Beckman Foundation. This work was supported by a Grant-in-Aid for the Japan Society for the Promotion of Science Fellows (to R. S.), the Howard Hughes Medical Institute (with which P. W. S. is an investigator), and a Caltech Summer Undergraduate Research Fellowship (to A. C.).
Funders:
Funding AgencyGrant Number
Caltech Beckman InstituteUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Japan Society for the Promotion of Science (JSPS)UNSPECIFIED
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Caltech Summer Undergraduate Research Fellowship (SURF)UNSPECIFIED
Subject Keywords:hermaphroditism, nematode, early embryogenesis, genetics, satellite model
Issue or Number:10
PubMed Central ID:PMC4199697
DOI:10.1534/g3.114.012385
Record Number:CaltechAUTHORS:20140820-084833184
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20140820-084833184
Official Citation:Evidence of Hermaphroditism and Sex Ratio Distortion in the Fungal Feeding Nematode Bursaphelenchus okinawaensis Ryoji Shinya, Koichi Hasegawa, Anthony Chen, Natsumi Kanzaki, and Paul W. Sternberg G3 October 2014 4:1907-1917; Early Online August 12, 2014, doi:10.1534/g3.114.012385
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:48708
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:20 Aug 2014 20:22
Last Modified:10 Nov 2021 18:34

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