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

• Published in: BMC evolutionary biology Vol. 19; no. 1; p. 130
• Main Authors: Leria, Laia, Vila-Farré, Miquel, Solà, Eduard, Riutort, Marta
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 20-06-2019; BioMed Central; BMC
• Subjects: Animals; Biodiversity; Biological evolution; Dugesia; Evolution; Evolution, Molecular; Facultative sex; Fissiparous reproduction; Footprints; Gene expression; Gene mutation; Genes; Genetic analysis; Genetic aspects; Genetic diversity; Genetic research; Genetic Variation; Haplotypes; Homeostasis; Meselson effect; Mitochondria; Mitochondrial DNA; Mosaicism; Mosaics; Muller’s ratchet; Multilevel selection; Mutation; Nucleotides; Offspring; Organisms; Physiological aspects; Planarians - genetics; Planarians - physiology; Ploidies; Progeny; Regeneration; Reproduction; Reproduction (biology); Reproduction, Asexual; Reproductive strategy; Reproductive system; Sex; Species; Species diversity; Sperm; Stem cells; Turbellaria; Turbellarians; Facultative sex; Mosaicism; Fissiparous reproduction; Multilevel selection; Muller’s ratchet; Meselson effect
• ISSN: 1471-2148; 1471-2148
• DOI: 10.1186/s12862-019-1440-1

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.