Repeated loss of function at HD mating-type genes and of recombination suppression without mating-type locus linkage in anther-smut fungi.

A wide diversity of mating systems occur in nature, with frequent evolutionary transitions in mating-compatibility mechanisms. Basidiomycete fungi typically have two mating-type loci controlling mating compatibility, HD and PR, usually residing on different chromosomes. In Microbotryum anther-smut fungi, there have been repeated events of linkage between the two mating-type loci through chromosome fusions, leading to large non-recombining regions. By generating high-quality genome assemblies, we found that two sister Microbotryum species parasitizing Dianthus plants, M. superbum and M. shykoffianum, as well as the distantly related M. scorzonarae, have their HD and PR mating-type loci on different chromosomes, but with the PR mating-type chromosome fused with part of the ancestral HD chromosome. Furthermore, progressive extensions of recombination suppression have generated evolutionary strata. In all three species, rearrangements suggest the existence of a transient stage of HD-PR linkage by whole chromosome fusion, and, unexpectedly, the HD genes lost their function. In M. superbum, multiple natural diploid strains were homozygous, and the disrupted HD2 gene was hardly expressed. Mating tests confirmed that a single genetic factor controlled mating compatibility (i.e. PR) and that haploid strains with identical HD alleles could mate and produce infectious hyphae. The HD genes have therefore lost their function in the control of mating compatibility in these Microbotryum species. While the loss of function of PR genes in mating compatibility has been reported in a few basidiomycete fungi, these are the first documented cases for the loss of mating-type determination by HD genes in heterothallic fungi. The control of mating compatibility by a single genetic factor is beneficial under selfing and can thus be achieved repeatedly, through evolutionary convergence in distant lineages, involving different genomic or similar pathways.

Asexual male production by ZW recombination in Artemia parthenogenetica.

In some asexual species, parthenogenetic females occasionally produce males, which may strongly affect the evolution and maintenance of asexuality if they cross with related sexuals and transmit genes causing asexuality to their offspring ("contagious parthenogenesis"). How these males arise in the first place has remained enigmatic, especially in species with sex chromosomes. Here, we test the hypothesis that rare, asexually produced males of the crustacean Artemia parthenogenetica are produced by recombination between the Z and W sex chromosomes during non-clonal parthenogenesis, resulting in ZZ males through loss of heterozygosity at the sex determination locus. We used RAD-sequencing to compare asexual mothers with their male and female offspring. Markers on several sex-chromosome scaffolds indeed lost heterozygosity in all male but no female offspring, suggesting that they correspond to the sex-determining region. Other sex-chromosome scaffolds lost heterozygosity in only a part of the male offspring, consistent with recombination occurring at a variable location. Alternative hypotheses for the production of these males (such as partial or total hemizygosity of the Z) could be excluded. Rare males are thus produced because recombination is not entirely suppressed during parthenogenesis in A. parthenogenetica. This finding may contribute to explaining the maintenance of recombination in these asexuals.

The Origin of Asexual Brine Shrimps.

AbstractDetermining how and how often asexual lineages emerge within sexual species is central to our understanding of sex-asex transitions and the long-term maintenance of sex. Asexuality can arise "by transmission" from an existing asexual lineage to a new one through different types of crosses. The occurrence of these crosses, cryptic sex, variations in ploidy, and recombination within asexuals greatly complicates the study of sex-asex transitions, as they preclude the use of standard phylogenetic methods and genetic distance metrics. In this study we show how to overcome these challenges by developing new approaches to investigate the origin of the various asexual lineages of the brine shrimp Artemia parthenogenetica. We use a large sample of asexuals, including all known polyploids, and their sexual relatives. We combine flow cytometry with mitochondrial and nuclear DNA data. We develop new genetic distance measures and methods to compare various scenarios describing the origin of the different lineages. We find that all diploid and polyploid A. parthenogenetica likely arose within the past 80,000 years through successive and nested hybridization events that involved backcrosses with different sexual species. All A. parthenogenetica have the same common ancestor and therefore likely carry the same asexuality gene(s) and reproduce by automixis. These findings radically change our view of sex-asex transitions in this group and show the importance of considering scenarios of asexuality by transmission. The methods developed are applicable to many other asexual taxa.

Digest: Evolution and maintenance of androdioecy in a haplodiploid insect.

The coexistence of hermaphrodites and males (androdioecy) is rare in both plants and animals and has hitherto remained unknown in insects. Mongue et al. report a new case of androdioecy in the invasive haplodiploid insect Icerya purchasi, in which hermaphrodites can only self-fertilize, but occasionally mate with males. Revealingly, I. purchasi shares several features with other androdioecious species such as the consequences of evolution from separate sexes, low outcrossing rates, and its colonizing habit.

Not so clonal asexuals: Unraveling the secret sex life of Artemia parthenogenetica.

The maintenance of sex is paradoxical as sexual species pay the "twofold cost of males" and should thus quickly be replaced by asexual mutants reproducing clonally. However, asexuals may not be strictly clonal and engage in "cryptic sex," challenging this simple scenario. We study the cryptic sex life of the brine shrimp Artemia parthenogenetica, which has once been termed an "ancient asexual" and where no genetic differences have ever been observed between parents and offspring. This asexual species rarely produces males, which can hybridize with sexual females of closely related species and transmit asexuality to their offspring. Using such hybrids, we show that recombination occurs in asexual lineages, causing loss-of-heterozygosity and parent-offspring differences. These differences cannot generally be observed in field-sampled asexuals because once heterozygosity is lost, subsequent recombination leaves no footprint. Furthermore, using extensive paternity tests, we show that hybrid females can reproduce both sexually and asexually, and transmit asexuality to both sexually and asexually produced offspring in a dominant fashion. Finally, we show that, contrary to previous reports, field-sampled asexual females also rarely reproduce sexually (rate ∼2‰). Overall, most previously known facts about Artemia asexuality turned out to be erroneous. More generally, our findings suggest that the evidence for strictly clonal reproduction of asexual species needs to be reconsidered, and that rare sex and consequences of nonclonal asexuality, such as gene flow within asexuals, need to be more widely taken into account in more realistic models for the maintenance of sex and the persistence of asexual lineages.