Cargando…

Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex

BACKGROUND: Predicted genetic consequences of asexuality include high intraindividual genetic diversity (i.e., the Meselson effect) and accumulation of deleterious mutations (i.e., Muller’s Ratchet), among others. These consequences have been largely studied in parthenogenetic organisms, but studies...

Descripción completa

Detalles Bibliográficos
Autores principales: Leria, Laia, Vila-Farré, Miquel, Solà, Eduard, Riutort, Marta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587288/
https://www.ncbi.nlm.nih.gov/pubmed/31221097
http://dx.doi.org/10.1186/s12862-019-1440-1
_version_ 1783429038055882752
author Leria, Laia
Vila-Farré, Miquel
Solà, Eduard
Riutort, Marta
author_facet Leria, Laia
Vila-Farré, Miquel
Solà, Eduard
Riutort, Marta
author_sort Leria, Laia
collection PubMed
description BACKGROUND: Predicted genetic consequences of asexuality include high intraindividual genetic diversity (i.e., the Meselson effect) and accumulation of deleterious mutations (i.e., Muller’s Ratchet), among others. These consequences have been largely studied in parthenogenetic organisms, but studies on fissiparous species are scarce. Differing from parthenogens, fissiparous organisms inherit part of the soma of the progenitor, including somatic mutations. Thus, in the long term, fissiparous reproduction may also result in genetic mosaicism, besides the presence of the Meselson effect and Muller’s Ratchet. Dugesiidae planarians show outstanding regeneration capabilities, allowing them to naturally reproduce by fission, either strictly or combined with sex (facultative). Therefore, they are an ideal model to analyze the genetic footprint of fissiparous reproduction, both when it is alternated with sex and when it is the only mode of reproduction. RESULTS: In the present study, we generate and analyze intraindividual cloned data of a nuclear and a mitochondrial gene of sexual, fissiparous and facultative wild populations of the species Dugesia subtentaculata. We find that most individuals, independently of their reproductive strategy, are mosaics. However, the intraindividual haplotype and nucleotide diversity of fissiparous and facultative individuals is significantly higher than in sexual individuals, with no signs of Muller’s Ratchet. Finally, we also find that this high intraindividual genetic diversity of fissiparous and facultative individuals is composed by different combinations of ancestral and derived haplotypes of the species. CONCLUSIONS: The intraindividual analyses of genetic diversity point out that fissiparous reproduction leaves a very special genetic footprint in individuals, characterized by mosaicism combined with the Meselson effect (named in the present study as the mosaic Meselson effect). Interestingly, the different intraindividual combinations of ancestral and derivate genetic diversity indicate that haplotypes generated during periods of fissiparous reproduction can be also transmitted to the progeny through sexual events, resulting in offspring showing a wide range of genetic diversity and putatively allowing purifying selection to act at both intraindividual and individual level. Further investigations, using Dugesia planarians as model organisms, would be of great value to delve into this new model of genetic evolution by the combination of fission and sex. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1440-1) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6587288
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-65872882019-06-27 Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex Leria, Laia Vila-Farré, Miquel Solà, Eduard Riutort, Marta BMC Evol Biol Research Article BACKGROUND: Predicted genetic consequences of asexuality include high intraindividual genetic diversity (i.e., the Meselson effect) and accumulation of deleterious mutations (i.e., Muller’s Ratchet), among others. These consequences have been largely studied in parthenogenetic organisms, but studies on fissiparous species are scarce. Differing from parthenogens, fissiparous organisms inherit part of the soma of the progenitor, including somatic mutations. Thus, in the long term, fissiparous reproduction may also result in genetic mosaicism, besides the presence of the Meselson effect and Muller’s Ratchet. Dugesiidae planarians show outstanding regeneration capabilities, allowing them to naturally reproduce by fission, either strictly or combined with sex (facultative). Therefore, they are an ideal model to analyze the genetic footprint of fissiparous reproduction, both when it is alternated with sex and when it is the only mode of reproduction. RESULTS: In the present study, we generate and analyze intraindividual cloned data of a nuclear and a mitochondrial gene of sexual, fissiparous and facultative wild populations of the species Dugesia subtentaculata. We find that most individuals, independently of their reproductive strategy, are mosaics. However, the intraindividual haplotype and nucleotide diversity of fissiparous and facultative individuals is significantly higher than in sexual individuals, with no signs of Muller’s Ratchet. Finally, we also find that this high intraindividual genetic diversity of fissiparous and facultative individuals is composed by different combinations of ancestral and derived haplotypes of the species. CONCLUSIONS: The intraindividual analyses of genetic diversity point out that fissiparous reproduction leaves a very special genetic footprint in individuals, characterized by mosaicism combined with the Meselson effect (named in the present study as the mosaic Meselson effect). Interestingly, the different intraindividual combinations of ancestral and derivate genetic diversity indicate that haplotypes generated during periods of fissiparous reproduction can be also transmitted to the progeny through sexual events, resulting in offspring showing a wide range of genetic diversity and putatively allowing purifying selection to act at both intraindividual and individual level. Further investigations, using Dugesia planarians as model organisms, would be of great value to delve into this new model of genetic evolution by the combination of fission and sex. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12862-019-1440-1) contains supplementary material, which is available to authorized users. BioMed Central 2019-06-20 /pmc/articles/PMC6587288/ /pubmed/31221097 http://dx.doi.org/10.1186/s12862-019-1440-1 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided 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 Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Leria, Laia
Vila-Farré, Miquel
Solà, Eduard
Riutort, Marta
Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title_full Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title_fullStr Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title_full_unstemmed Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title_short Outstanding intraindividual genetic diversity in fissiparous planarians (Dugesia, Platyhelminthes) with facultative sex
title_sort outstanding intraindividual genetic diversity in fissiparous planarians (dugesia, platyhelminthes) with facultative sex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6587288/
https://www.ncbi.nlm.nih.gov/pubmed/31221097
http://dx.doi.org/10.1186/s12862-019-1440-1
work_keys_str_mv AT lerialaia outstandingintraindividualgeneticdiversityinfissiparousplanariansdugesiaplatyhelmintheswithfacultativesex
AT vilafarremiquel outstandingintraindividualgeneticdiversityinfissiparousplanariansdugesiaplatyhelmintheswithfacultativesex
AT solaeduard outstandingintraindividualgeneticdiversityinfissiparousplanariansdugesiaplatyhelmintheswithfacultativesex
AT riutortmarta outstandingintraindividualgeneticdiversityinfissiparousplanariansdugesiaplatyhelmintheswithfacultativesex