Abstract
BackgroundPseudogamy 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.ResultsTo 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.ConclusionsWe 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.
Highlights
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 Deoxyribonucleic acid (DNA)
We previously showed that M. belari females are unable to mate with males from three other Mesorhabditis species, including two standard sexual species
We established a frozen culture collection of 66 strains of Mesorhabditis and use it to answer several pending questions: 1) Did pseudogamy arise once or repeatedly in the genus? 2) Did speciation occur in the pseudogamous state? 3) Can the sperm of males of other species be used at least to produce females by gynogenesis? 4) If not, at which stage does the species barrier block embryonic development? We identified 11 distinct auto-pseudogamous species that appear to form a single clade within the Mesorhabditis genus and explored the mechanisms of barrier between these species
Summary
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. Populations of M. belari are mainly composed of females and of a lower frequency of males (9% in strain JU2817) These males are needed because their sperm trigger oocyte activation. Most eggs do not use the sperm DNA after fertilization and develop into females by gynogenesis. Two rounds of female meiotic division give rise to a haploid female genome (reduced oocytes), which mixes with the haploid male DNA, producing a diploid male [5]. The fact that amphimictic eggs always give rise to males is explained by the fact that sex determination is through a XY system, an almost complete Y-bearing sperm drive occurs at fertilization [5]
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