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

Facultative sex Fissiparous reproduction Meselson effect Mosaicism Muller’s ratchet Multilevel selection

Journal

BMC evolutionary biology
ISSN: 1471-2148
Titre abrégé: BMC Evol Biol
Pays: England
ID NLM: 100966975

Informations de publication

Date de publication:
20 06 2019
Historique:
received: 22 11 2018
accepted: 15 05 2019
entrez: 22 6 2019
pubmed: 22 6 2019
medline: 5 9 2019
Statut: epublish

Résumé

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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 31221097
doi: 10.1186/s12862-019-1440-1
pii: 10.1186/s12862-019-1440-1
pmc: PMC6587288
doi:

Banques de données

Dryad
['10.5061/dryad.c5f0ps6']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

130

Références

Curr Biol. 2011 Jul 12;21(13):1129-34
pubmed: 21683598
Genetics. 1995 Nov;141(3):1173-87
pubmed: 8582622
J Evol Biol. 2016 May;29(5):887-99
pubmed: 26864612
Nat Rev Genet. 2005 Nov;6(11):836-46
pubmed: 16304599
Dev Cell. 2016 Sep 26;38(6):621-34
pubmed: 27676435
Bioinformatics. 2006 Nov 1;22(21):2688-90
pubmed: 16928733
Genesis. 2015 Aug;53(8):535-46
pubmed: 26138588
Evolution. 2007 Nov;61(11):2728-35
pubmed: 17908244
J Hered. 2001 Jul-Aug;92(4):371-3
pubmed: 11535656
Mol Phylogenet Evol. 2009 Sep;52(3):835-45
pubmed: 19435604
Nat Plants. 2017 Dec;3(12):926-929
pubmed: 29209081
Am Nat. 2009 Jul;174 Suppl 1:S1-S14
pubmed: 19441962
Mol Biol Evol. 1999 Jan;16(1):37-48
pubmed: 10331250
Dev Genes Evol. 2007 May;217(5):403-11
pubmed: 17390146
Bioinformatics. 2009 Jun 1;25(11):1451-2
pubmed: 19346325
Curr Biol. 2016 Jun 6;26(11):1385-94
pubmed: 27161504
Nat Methods. 2012 Jul 30;9(8):772
pubmed: 22847109
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Mol Phylogenet Evol. 2003 Jan;26(1):1-7
pubmed: 12470932
PLoS One. 2014 Nov 19;9(11):e113268
pubmed: 25409516
Nucleic Acids Res. 2019 Jan 8;47(D1):D812-D820
pubmed: 30496475
Nature. 2006 Sep 7;443(7107):89-92
pubmed: 16957730
J Evol Biol. 2016 Jan;29(1):5-22
pubmed: 26431643
Mol Ecol. 2015 Mar;24(5):1007-18
pubmed: 25626726
Nat Rev Genet. 2002 Oct;3(10):748-58
pubmed: 12360233
Genes (Basel). 2014 Dec 11;5(4):1064-94
pubmed: 25513881
Mol Biol Evol. 2018 Jul 1;35(7):1668-1677
pubmed: 29659991
J Evol Biol. 2004 Nov;17(6):1167-77
pubmed: 15525396
Mol Ecol. 2015 Jun;24(11):2673-85
pubmed: 25872099
Dev Genes Evol. 2013 Mar;223(1-2):67-84
pubmed: 23138344
Genetica. 1998;102-103(1-6):507-24
pubmed: 9766963
Nature. 2005 Mar 31;434(7033):636-40
pubmed: 15800622
Evolution. 2014 Oct;68(10):2901-16
pubmed: 24975991
Annu Rev Cell Dev Biol. 2004;20:725-57
pubmed: 15473858
Annu Rev Genet. 2007;41:83-105
pubmed: 18076325
Proc Biol Sci. 2004 May 22;271(1543):1001-7
pubmed: 15293852
J Evol Biol. 2004 Nov;17(6):1187-8; discussion 1192-4
pubmed: 15525401
Mol Biol Evol. 2012 Jan;29(1):401-8
pubmed: 21940645
Annu Rev Genet. 2001;35:125-48
pubmed: 11700280
Science. 2018 May 25;360(6391):
pubmed: 29674432
Int J Dev Biol. 2012;56(1-3):83-91
pubmed: 22252539
Methods Mol Biol. 2018;1774:1-56
pubmed: 29916154
BMC Bioinformatics. 2009 Aug 11;10:247
pubmed: 19671163
Dev Growth Differ. 2006 Dec;48(9):615-28
pubmed: 17118016
Bioessays. 2000 Jun;22(6):578-90
pubmed: 10842312
Bioinformatics. 2012 Jun 15;28(12):1647-9
pubmed: 22543367
Mol Ecol Resour. 2010 May;10(3):564-7
pubmed: 21565059
Genetics. 1996 Sep;144(1):427-37
pubmed: 8878706
J Biol Res (Thessalon). 2017 Jan 31;24:2
pubmed: 28164041
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
Mol Phylogenet Evol. 2020 Feb;143:106496
pubmed: 31151789
Science. 2000 May 19;288(5469):1211-5
pubmed: 10817991
Cold Spring Harb Symp Quant Biol. 2008;73:573-81
pubmed: 19022767
Integr Zool. 2009 Sep;4(3):265-71
pubmed: 21392298
BMC Evol Biol. 2013 Dec 11;13:268
pubmed: 24330464
BMC Plant Biol. 2013 Feb 20;13:29
pubmed: 23421644
Proc Biol Sci. 2001 Nov 22;268(1483):2291-9
pubmed: 11703868
Mol Ecol. 2016 Jul;25(14):3356-69
pubmed: 27286413
Science. 2011 May 13;332(6031):811-6
pubmed: 21566185
Chromosoma. 2014 Jun;123(3):265-72
pubmed: 24402417
PLoS One. 2015 Nov 20;10(11):e0143525
pubmed: 26588467
Mol Biol Evol. 2015 Apr;32(4):896-905
pubmed: 25534028

Auteurs

Laia Leria (L)

Department de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, and Institut de Recerca de la Biodiversitat (IRBio), Barcelona, Catalonia, Spain.

Miquel Vila-Farré (M)

Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.

Eduard Solà (E)

Department de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, and Institut de Recerca de la Biodiversitat (IRBio), Barcelona, Catalonia, Spain.

Marta Riutort (M)

Department de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, and Institut de Recerca de la Biodiversitat (IRBio), Barcelona, Catalonia, Spain. mriutort@ub.edu.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH