Not so clonal asexuals: Unraveling the secret sex life ofArtemia parthenogenetica

Abstract

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.

The origin of asexual brine shrimps

“…Understanding why sexual reproduction is so widespread among eucaryotes, despite the wellknown costs of sex (Maynard Smith 1978;Otto and Lenormand 2002;Meirmans et al 2012), requires an understanding of how and how often sex-asex transitions can occur (Delmotte et al 2001;Simon et al 2003;Archetti 2004;Lenormand et al 2016;Engelstädter 2017;Haag et al 2017;Boyer et al 2021). Most theoretical models on this question adopt a simplistic view of these transitions, assuming that an asexual clone can emerge immediately from a sexual ancestror.…”

“…While the absence of recombination in apomicts maintains heterozygosity levels across generations (except for mutation, gene conversion, and mitotic recombination events), the presence of recombination under automixis can result in a loss of heterozygosity (LOH) between generations. Depending on the precise mode of automixis and recombination rate, the rate of LOH may range from 0% to 100% and may vary among loci, depending on the distance from the centromere (Nougué et al 2015b;Svendsen et al 2015;Boyer et al 2021). When LOH is heterogeneously distributed along the chromosome, different genomic regions will coalesce at different points in time, providing different phylogenetic signals.…”

“…Indeed, meiosis might sometimes occur normally in asexual females (e.g. De Meester et al 2004;Rey et al 2013;Boyer et al 2021). Haploid eggs produced through regular meioses can be fertilized by a haploid sperm from a rare male or a male from related sexual species.…”

“…Cytogenetic studies in diploids have yielded contradictory results by reporting almost all known forms of automixis (Narbel-Hofstetter 1964;Nougué et al 2015b), while most cytogenetic studies in polyploids have reported that they reproduce through apomixis (Barigozzi 1974). Recent genetic studies showed that Ap2n reproduces through a mechanism genetically equivalent to central fusion automixis (Nougué et al 2015b;Boyer et al 2021), which leads to loss of heterozygosity in centromere-distal chromosomal regions due to recombination (Svendsen et al 2015). A. parthenogenetica has a ZW sex-determination system and produces males at low frequency (Stefani 1964).…”

“…These rare males are thought to arise through rare recombination events between the Z and W chromosomes in Ap2n females, which results in a LOH at the sex locus and the production of ZZ males (Browne and Hoopes 1990;Abreu-Grobois and Beardmore 2001;Boyer et al 2021). Last, for a long time, rare males have been thought to be useless and irrelevant to Ap2n reproduction (MacDonald and Browne 1987;Simon et al 2003), but experiments showed they can transmit asexuality when crossed with Aurm and Akaz sexual females (Maccari et al 2014;Boyer et al 2021). Moreover, recent experiments have shown that some Ap2n females can engage very rarely in sex in the laboratory, with normal meiosis and recombination (Boyer et al 2021).…”