Asexual male production by ZW recombination in Artemia parthenogenetica

Abstract

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.

ZW sex-chromosome evolution and contagious parthenogenesis in Artemia brine shrimp

“…11), arguing against the accidental occurrence of a version of automixis that eliminates variants across the genome (another hypothesis for the origin of rare males, Nougué et al 2015). Taken together, these results support rare ZW recombination as the source of the Aibi Lake rare male (Nougué et al 2015;Boyer et al 2022). sp.…”

“…Two genome assemblies and a high density linkage map are currently available for the American A. franciscana (Jo et al 2021a;Han et al 2021;De Vos et al 2021), but resources for the Eurasian clade are more limited, with only an A. sp. Kazakhstan draft genome assembly recently described in Boyer et al (2022). The median dS between the two clades is ~0.2.…”

“…Kazakhstan sexual female, confirming that asexual females carry the same pair of ZW chromosomes. Boyer et al (2022) recently showed that Artemia rare males can be produced by ZW recombination events at variable locations near the sex-determining locus. We obtained a rare male from an A. parthenogenetica line from Aibi Lake (which we use in the next section to explore the transmission of asexuality).…”

“…Because A. parthenogenetica reproduce through central fusion automixis (Nougué et al 2015), a modified form of meiosis, which allows for loss of heterozygosity when recombination between chromosomes occurs, rare recombination events between the Z and W (which replace part of the W with its Z-linked homologous region) can lead to the creation of rare males (Nougué et al 2015;Boyer et al 2022). Finally, the genetic mechanisms behind asexuality, and whether the sex chromosomes play any further role in its evolution, have not yet been explored in detail.…”

“…2015), a modified form of meiosis, which allows for loss of heterozygosity when recombination between chromosomes occurs, rare recombination events between the Z and W (which replace part of the W with its Z-linked homologous region) can lead to the creation of rare males (Nougué et al . 2015; Boyer et al . 2022).…”