Males as somatic investment in a parthenogenetic nematode

Grosmaire, Manon; Launay, Caroline; Siegwald, Marion; Brugière, Thibault; Estrada-Virrueta, Lilia; Berger, Duncan; Burny, Claire; Modolo, Laurent; Blaxter, Mark; Meister, Peter; Félix, Marie‐Anne; Gouyon, Pierre‐Henri; Delattre, Marie

doi:10.1126/science.aau0099

Cited by 26 publications

(59 citation statements)

References 29 publications

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“…We previously showed that M. belari females are unable to mate with males from three other Mesorhabditis species, including two standard sexual species. M. belari is thus auto-pseudogamous, a reproductive strategy that we showed to be evolutionary stable [5]. The fact that amphimictic eggs always give rise to males is explained by the fact that although sex determination is through a XY system, an almost complete Y-bearing sperm drive occurs at fertilization [5].…”

Section: Introductionmentioning

confidence: 61%

“…This reproductive system, although rare, has been described in several plant and animal taxa, including vertebrates [3,4]. In the nematode Mesorhabditis belari, a special type of pseudogamy is found, which we call auto-pseudogamy, where, as a source of sperm, females produce their own males at low frequency [5,6]. Populations of M. belari are thus mainly composed of females but also of a lower frequency of males (9% in strain JU2817).…”

Section: Introductionmentioning

confidence: 99%

“…In oocytes that give rise to gynogenetic embryos, a single round of meiotic division is observed and a single polar body is formed (unreduced oocytes), thus compensating for the lack of the paternal haplome. In amphimictic embryos, two rounds of female meiotic division give rise to a haploid female genome (reduced oocytes), which then mixes with the haploid male DNA, producing a diploid male [5]. The males never further transmit their mother's genes back to females.…”

Section: Introductionmentioning

confidence: 99%

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Diversification and hybrid incompatibility in auto-pseudogamous species of Mesorhabditis nematodes

et al. 2020

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Background: Pseudogamy is a reproductive system in which females rely on the sperm of males to activate their oocytes, generally parasitizing males of other species, but do not use the sperm DNA. The nematode Mesorhabditis belari uses a specific form of pseudogamy, where females produce their own males as a source of sperm. Males develop from rare eggs with true fertilization, while females arise by gynogenesis. Males thus do not contribute their genome to the female offspring. Here, we explored the diversity of reproductive mode within the Mesorhabditis genus and addressed species barriers in pseudogamous species. Results: To this end, we established a collection of over 60 Mesorhabditis strains from soil and rotting vegetal matter. We found that males from pseudogamous species displayed a reduced size of their body, male tail and sperm cells compared to males of sexual Mesorhabditis species, as expected for males that face little competition. Using rDNA sequences and crosses, we could define 11 auto-pseudogamous biological species, with closely related species pairs and a possible single origin of pseudogamy in the Mesorhabditis genus. Most crosses between males and females of different species did not even produce female progeny. This surprising species barrier in pseudogamous egg activation was pre or postcopulatory depending on the species pair. In the latter case, when hybrid embryos were produced, most arrested before the first embryonic cell division. Hybrid incompatibility between auto-pseudogamous species was due to defective interaction between sperm and oocyte as well as defective reconstitution of zygotic centrosomes. Conclusions: We established a collection of sexual and pseudo-sexual species which offer an ideal framework to explore the origin and consequences of transition to asexuality. Our results demonstrate that speciation occurs in the pseudogamous state. Whereas genomic conflicts are responsible for hybrid incompatibility in sexual species, we here reveal that centrosomes constitute key organelles in the establishment of species barrier.

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Section: Introductionmentioning

confidence: 61%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Diversification and hybrid incompatibility in auto-pseudogamous species of Mesorhabditis nematodes

et al. 2020

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“…Generating males at a low frequency can theoretically aid the spread and maintenance of gynogenesis by transmitting alleles required for diploid maternal inheritance into neighboring sexual populations [53]. The production of males even at a low frequency can also help propagate an intraspecific gynogenetic lineage by enabling the activation of the egg and inheritance of centrioles without relying on males from a related species, as seen in Mesorhabditis belari [54]. Thus, it is notable that gynogenetic reproduction in C. nouraguensis x C. becei hybridizations already exhibits the ability to produce males.…”

Section: Characteristics Of Incipient Gynogenesismentioning

confidence: 99%

Hybridization promotes asexual reproduction inCaenorhabditisnematodes

Lamelza

Young

Noble

et al. 2019

Preprint

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Although most unicellular organisms reproduce asexually, most multicellular eukaryotes are obligately sexual. This implies that there are strong barriers that prevent the origin or maintenance of asexuality arising from an obligately sexual ancestor. By studying rare asexual animal species we can gain a better understanding of the circumstances that facilitate their evolution from a sexual ancestor. Of the known asexual animal species, many originated by hybridization between two ancestral sexual species. The balance hypothesis predicts that genetic incompatibilities between the divergent genomes in hybrids can modify meiosis and facilitate asexual reproduction, but there are few instances where this has been shown. Here we report that hybridizing two sexual Caenorhabditis nematode species (C. nouraguensis females and C. becei males) alters the normal inheritance of the maternal and paternal genomes during the formation of hybrid zygotes. Most offspring of this interspecies cross die during embryogenesis, exhibiting inheritance of a diploid C. nouraguensis maternal genome and incomplete inheritance of C. becei paternal DNA. However, a small fraction of offspring develop into viable adults that can be either fertile or sterile. Fertile offspring are produced asexually by sperm-dependent parthenogenesis (also called gynogenesis or pseudogamy); these progeny inherit a diploid maternal genome but fail to inherit a paternal genome. Sterile offspring are hybrids that inherit both a diploid maternal genome and a haploid paternal genome. Whole-genome sequencing of individual viable worms shows that diploid maternal inheritance in both fertile and sterile offspring results from an altered meiosis in C. nouraguensis oocytes and the inheritance of two randomly selected homologous chromatids. We hypothesize that hybrid incompatibility between C. nouraguensis and C. becei modifies maternal and paternal genome inheritance and indirectly induces gynogenetic reproduction. This system can be used to dissect the molecular mechanisms by which hybrid incompatibilities can facilitate the emergence of asexual reproduction.AUTHOR SUMMARYEukaryotes employ two major reproductive strategies: sexual and asexual reproduction. Both types of reproduction have distinct theoretical costs and benefits, and most unicellular eukaryotes can switch between both modes. However, most multicellular eukaryotes are obligately sexual, implying that there are barriers to the evolution of asexuality from a sexual ancestor. Of the few asexual animal species, many are hybrids of two ancestral sexual species, suggesting that novel genetic interactions in hybrids facilitate the evolution of asexuality. One model suggests that genetic incompatibilities between divergent genomes in hybrids can modify female meiosis and paternal genome inheritance to facilitate asexual reproduction. While studying interspecies hybridizations of Caenorhabditis nematodes, we found that crossing two sexual species (C. nouraguensis and C. becei) disrupts female meiosis and paternal genome inheritance. Most offspring die during embryogenesis, but on rare occasions develop into viable and fertile adults that are produced asexually. This asexual reproduction involves the unusual production of eggs carrying two sets of maternal chromosomes and the loss of the paternal set of chromosomes. We hypothesize that genetic incompatibility between these two species disrupts maternal and paternal genome inheritance. This interspecies hybridization may serve as a model to study how genetic incompatibilities facilitate the emergence of asexuality.

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“…Variation in mating systems is especially familiar in plants, but has also been one of the longstanding attractions of nematode biology (Nigon & Félix, 2017) . Just within Rhabditidae, this aspect of life-history now spans systems with separate males and females (gonochorism), males and self-fertile hermaphrodites (androdioecy; Kanzaki et al, 2017;Mayer et al, 2007) , males, females, and hermaphrodites (trioecy; Chaudhuri et al, 2015;Kanzaki et al, 2017) , asexual reproduction where sperm does not contribute genetic material (parthenogenesis, gynogenesis; Fradin et al, 2017;Grosmaire et al, 2019) , and alternating generations of hermaphroditism and dioecy (heterogony; Kiontke, 2005) .…”

Section: Introductionmentioning

confidence: 99%

Selfing is the safest sex forCaenorhabditis tropicalis

Noble

Yuen

Stevens³

et al. 2020

Preprint

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Mating systems have profound effects on genetic diversity and compatibility. The convergent evolution of self-fertilization in three Caenorhabditis species provides a powerful lens to examine causes and consequences of mating system transitions. Among the selfers, C. tropicalis is the least genetically diverse and most afflicted by outbreeding depression. We generated a chromosomal-scale genome for C. tropicalis and surveyed global diversity. Population structure is very strong, and islands of extreme divergence punctuate a genomic background that is highly homogeneous around the globe. Outbreeding depression in the laboratory is caused largely by multiple gene drive elements, genetically consistent with maternal toxin/zygotic antidote systems. Driver loci harbor novel and duplicated genes, and their activity is modified by mito-nuclear background. Segregating drivers dramatically reduce fitness, and simulations show that selfing limits their spread. Frequent selfing in C. tropicalis may therefore be a strategy to avoid drive-mediated outbreeding depression.

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Males as somatic investment in a parthenogenetic nematode

Cited by 26 publications

References 29 publications

Diversification and hybrid incompatibility in auto-pseudogamous species of Mesorhabditis nematodes

Diversification and hybrid incompatibility in auto-pseudogamous species of Mesorhabditis nematodes

Hybridization promotes asexual reproduction inCaenorhabditisnematodes

Selfing is the safest sex forCaenorhabditis tropicalis

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