CE02 - Terre vivante

Origin and consequences of asexuality in Mesorhabditis nematodes – Pseudogamy

Origin and consequences of asexuality within Mesorhabditis nematodes

We discovered the previously unrecognized reproductive strategy of the nematode Mesorhabitis belari, called auto-pseudogamy, which features progressive loss of males and sexuality. We will use species of the Mesorhabditus genus, with or without sexual reproduction, to explore the cellular origins and the genomic consequences of auto-pseudogamy. We will use our combined expertise in evolutionary cell biology and population genetics, on a study system that offers many experimental advantages.

Mesorhabditis species are ideal to i) contrast the evolutionary consequences of sex and asex within and between species, ii) explore the cellular and molecular origins of asex

1) Which type of meiosis allows the production of asexual females of M. belari,. This will lead to specific theoretical expectation on the evolutionary consequences. We will combine cytological description and genomic studies. <br />2) Identify the factors that allow the production of asexual (female) or sexual (male) embryos by a given female. We will do comparative transcriptomics on sorted embryos<br />3) Uncover the mechanism of fertilization drive: why Y-bearing sperm are more competent to fertilize? Candidate gene approach<br />4) Explore from a theoritical point of view the link between the evolution of pseudogamy and of sex chromosomes<br />5) Build a phylogeny of species and genes (from RNAseq data on all species) to define the number and age of transitions to pseudogamy, the hybrid origin and is there a selfish Y chromosome<br />6) Population genomic data: mutation load, level of polymorphism, heterozygosity etc.<br />7) Evolution of sex specific genes: expression ,degeneration and RedQueen hypothesis

Whole genome and transcriptome analysis
Population genomics methods
Cytological description using immunostainings
RNA interference
CRISRP/Cas9 mutants and transgenes
Genetics, genotyping
Electron microscopy

1) We uncovered which type of meiotic division allows the production of unreduced oocytes, i.e asexual females in M. belari. By ctyological observations we found evidence that all chromosome pairs recombine and form stable bivalents at diakinesis. We found that meiosis I is abortive. Consequently, there is a single equational division. Thus, diploid oocytes contain an assortment of non-sister chromatid (equivalent to automixis central fusion) . On the long term, such meiotic division should lead to genome wide homozygosity, except on the center of chromosomes where recombination is absent. In parallel, we measured the level of heterozygosity in a given animal, based on the RNAseq performed on single males or females. Our previous results suggest high levels of heterozygosity, which contradicts our cytological observations. We are currently exploring this discrepancy. One possibility is that chiasmata are not the results of a real cross over event. Alternatively, recombined chromatids may be systematically discarded into the polar body due to meiotic drive. We are currently measuring the actual rate of recombination by linkage disequilibrium in 10 strains of a sexual species M. spiculigera and 10 strains of an asexual species M. belari. Beforehand, we performed high coverage DNAseq f(Illumina and Nanopore) or one representative strain of M. spiculigera and M. belari to obtain an assembled reference genome. RNAseq was also performed for annotation. Genomes are ready.
2) We managed to perform manual sorting of eggs, being either gynogenetic (asexual) or amphimictic (sexual) soon after fertilization and sequenced their transcriptome. We identified differentially expressed genes and concentrated on 30 candidates. smiFISH and single embryo q-RTPCR are used to confirm candidates. Next, functional analysis on these candidates will be performed
For the other tasks, raw data (RNA and DNAseq) have been obtained and analysis are underway

We are conducting the rest of the project as initially planned. Currently we are focusing on the establishment of transgenic lines expressing fluorescent markers (for Task 2 and 3) and on population genomic data. As new results come, informations are incorporated into the theoritical models.

none yet

Why is sexuality so common compared to asexuality? Although there are theoretical long-term advantages offered by genetic mixing, whether this is sufficient to overcome all the direct costs of sex remains debated. Instead of a particular advantage of sex over asexuality, asexual species could be rare because the proximal mechanisms for a transition from sex to asex are complex and evolutionary constrained. Because these fundamental questions are still unresolved, the paradox of sex remains one of the most exciting challenges of current evolutionary biology.
Studying the transition to asexuality is a fruitful way to make progress with these intriguing questions. There is clearly a need for further exploration of the asexual world in a way that combines genetic and experimental approaches. This will allow to identify the constraints that prevent the emergence and maintenance of asexuality and thus to understand the adaptive value of sex.
The team of Delattre has recently uncovered the unique reproductive system of the nematode Mesorhabditis belari. Here, males are required to fertilize all the eggs, and Y-bearing sperm cells are much more competent than X-bearing ones for fertilizing. However, because most eggs develop by gynogenesis without using the sperm DNA, the species is mainly composed of asexual females. Only in 10% of the cases is the sperm DNA utilized, to produce sexual males by amphimixis. Although other examples of species with mixed sex/asex systems exist (haplo-diploid, cyclical parthenogens,…), none of them features exclusive asexual females and a progressive loss of males and sexuality, where the male genes never re-enter the female pool. Delattre's team has also established a collection of sexual and other asexual species from the Mesorhabditis genus, which share many of the experimental advantages offered by C. elegans. This makes Mesorhabditis an ideal study system to explore the cellular and molecular origins of asex (Aim1) and contrast the evolutionary consequences of sex and asex within and between species (Aim2). We will specifically address the following questions:
Aim1_ Task 1.1: which modification to meiosis entails the production of diploid sexual females in M. belari, and what are the genetic consequences? (cytological description and genomic studies)
Aim1_ Task 1.2: which factors control the determination of the two type of eggs? (comparative transcriptomics)
Aim1_Task 1.3: what are the mechanisms responsible for the fertilization drive towards Y-bearing sperm? (candidate gene approach)
Aim1_Task 1.4: what is the link between the origin of pseudogamy and the evolution of sex chromosomes, i.e., is the fertilization drive a consequence or a cause of the emergence of pseudogamy? (theoretical modelling)
Aim2_Task 2.1: what is the number of transitions to/from pseudogamy in the genus? is pseudogamy an ancient evolutionarily stable system? did a selfish Y spread across species via adaptive introgression? (phylogenomics, RNAseq of males and females in multiple species)
Aim2_Task 2.2: contrast the empirical analysis of the genome dynamics (heterozygosity, mutation load, inbreeding) to the theoretical expectations. (population genomics, genome resequencing of wild samples)
Aim2_Task 2.3: explore the evolution of sex-specific genes compared to sexual ancestors, using the RNAseq data obtained in Task 2.1.
Our project is ambitious, interdisciplinary and original as it aims at i) exploring a new and remarkable reproductive system and ii) bridging complementary and interdisciplinary approaches (evolutionary cell biology (Delattre), modelling of reproductive systems (Glemin) and evolutionary genomics (Galtier)) that are rarely combined, because of the lack of experimental asexual systems.

Project coordinator


The author of this summary is the project coordinator, who is responsible for the content of this summary. The ANR declines any responsibility as for its contents.


ISEM Institut des Sciences de l'Evolution de Montpellier

Help of the ANR 510,364 euros
Beginning and duration of the scientific project: October 2019 - 48 Months

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