The origin of asexual brine shrimps

Abstract

Determining 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, variation 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 last 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 asexuality "by transmission" scenarios. The methods developed are applicable to many other asexual taxa.

Transitions to asexuality and evolution of gene expression in Artemia brine shrimp

“…All sampled asexual lineages cluster with A. sp. Kazakhstan, with A. urmiana sexual being an outgroup to the cluster, consistent with [37]. These lineages (grey rectangle, figure 1a) are very closely related, and the lengths of the branches separating them are almost zero.…”

“…Because the lineages studied here are very closely related, there should be little divergence resulting from relaxed selection in asexuals, and this differentiation may be further eroded by ongoing gene flow among them [37,39]. Third, while some asexual species bypass meiosis altogether (e.g.…”

“…Kazakhstan, and probably originated through a complex demographic scenario involving a single origin of asexuality followed by backcrossing to A. sp. Kazakhstan [37]. To examine these relationships with genome-wide data, we sequenced RNA from multiple tissues for each lineage (electronic supplementary material, table S2), and assembled high-quality transcriptomes for each of them (electronic supplementary material, figure S1).…”

“…Asexual lineages are thought to have arisen multiple times as a result of 'contagious parthenogenesis': asexual females occasionally produce males that can fertilize females of closely related sexual populations, thereby giving rise to new asexual lineages [32][33][34][35][36]. However, the relationship between sexual and asexual lineages, and how diverged they are, are still questions under debate, which have mostly been investigated using a small number of mitochondrial and nuclear sequences [32,34,37]. How different these species and populations are at the gene expression level, and whether the asexual lineages share a single reproductive programme (as expected under contagious parthenogenesis), is still unknown.…”

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

“…Originally thought of as fairly ancient, these lineages turned out to have arisen recently through hybridization between asexual lineages and individuals from or closely related to A. sp. Kazakhstan (Baxevanis et al 2006;Maccari et al 2013b;Rode et al 2021). In Artemia, such contagious parthenogenesis can occur through the production of rare males by asexual lineages, which can fertilize closely related sexual females (Maccari et al 2013a;Abatzopoulos 2018).…”