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

Abstract

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.

Phylum Nematoda: trends in species descriptions, the documentation of diversity, systematics, and the species concept

“…In a mostly free-living, but opportunistically vertebrate-parasitic species (Halicephalobus gingivalis Stefanski 1954), intraspecific morphological variability in a single population of a single species started from a single individual can be greater than what is regarded as inter-specific variation (Anderson et al 1998, Fonderie et al 2013, Nadler et al 2003. Patterns of variability within the genera Caenorhabditis, Pristionchus, Bursaphelenchus, Globodera, Radopholus, Ascaris and Trichuris are similarly complex (Caenorhabditis- Crombie et al 2019, Dey et al 2012, Ferrari et al 2017, Kanzaki et al 2012, Kiontke et al 2011Pristionchus-Ragsdale et al 2013;Bursaphelenchus-Abad et al 1991, Beckenbach et al 1999, de Guiran & Bruguier 1989, de Guiran & Ritter 1984, Fukushige & Futai 1985, Kanzaki 2008, lange et al 2008, Mamiya 1986, Riga et al 1992, Schauer-Blume 1990, Webster et al 1990Globodera-Alenda et al 2013, Blanchard 2006, Boucher et al 2013, Handoo et al 2012, lax et al 2014, Madani et al 2010, Montary et al 2015, Thevenoux et al 2019Radopholus-Elbadri et al 1999a, b, 2002, Haegeman et al 2010, Hahn et al 1996, Huettel & yaegashi 1988, Huettel et al 1984, 1986, Plowright et al 2013, Valette et al 1998…”

Programmed-DNA Elimination in the free-living nematodes Mesorhabditis

“…Embryos were fixed with methanol and the freeze-cracking method, as described in (Launay et al, 2020). Embryos were stained with Hoechst (0.5 ug/ml 152).…”

“…The phylogenetic distance of Mesorhabditis to C. elegans is as far as Pristionchus pacificus or Oscheius tipulae to C. elegans (two other well-studied nematode genera (Haag et al, 2018)). Within Mesorhabditis , some species have an asexual reproductive system, whether others are male/female sexual species (Grosmaire et al, 2019; Launay et al, 2020). We analyzed several Mesorhabditis species and systematically found the pattern of DNA fragmentation and loss previously described in Ascaris , irrespective of their reproductive system.…”

“…In this study, we used a combination of cytological observation, genomic and transcriptomic analysis to describe the dynamics of elimination and the nature of the eliminated sequences in the asexual species M. belari and the sexual species M. spiculigera (Launay et al, 2020). Mesorhabditis nematodes have a small ∼150 Mb genome, share many experimental advantages with the model species C. elegans , including the ability to inactivate genes by RNAi and to modify the genome with CRISPR/Cas9 (Blanc & al.…”

Fisher vs. the Worms: Extraordinary Sex Ratios in Nematodes and the Mechanisms that Produce Them

“…Sperm typically comes from males of a related XX/XO or XX/XY species, as can be seen in laboratory hybrid crosses between Caenorhabditis becei males and C. nouraguensis females [ 166 ]. However, for the XX/XY genus Mesorhabditis these sperm are restricted to males of the same species, as attempted interspecies crosses are thwarted by blocks prior to sperm–oocyte fusion or incompatibilities with the paternal centrosome [ 167 ]. Natural populations of Mesorhabditis belari thus cannot be exclusively female, but are highly female-biased (91% XX female and 9% XY male).…”