Automixis in Artemia: solving a century‐old controversy

Abstract

Parthenogenesis (reproduction through unfertilized eggs) encompasses a variety of reproduction modes with (automixis) or without (apomixis) meiosis. Different modes of automixis have very different genetic and evolutionary consequences but can be particularly difficult to tease apart. In this study, we propose a new method to discriminate different types of automixis from population-level genetic data. We apply this method to diploid Artemia parthenogenetica, a crustacean whose reproductive mode remains controversial despite a century of intensive cytogenetic observations. We focus on A. parthenogenetica from two western Mediterranean populations. We show that they are diploid and that markers remain heterozygous in cultures maintained up to ~36 generations in the laboratory. Moreover, parallel patterns of population-wide heterozygosity levels between the two natural populations strongly support the conclusion that diploid A. parthenogenetica reproduce by automictic parthenogenesis with central fusion and low, but nonzero recombination. This settles a century-old controversy on Artemia, and, more generally, suggests that many automictic organisms harbour steep within-chromosome gradients of heterozygosity due to a transition from clonal transmission in centromere-proximal regions to a form of inbreeding similar to self-fertilization in centromere-distal regions. Such systems therefore offer a new avenue for contrasting the genomic consequences of asexuality and inbreeding.

What does the geography of parthenogenesis teach us about sex?

“…Some forms of parthenogenesis similarly involve the ploidy-restoring fusion of two products of meiosis, and if the fusion occurs late in the process of oogenesis (terminal fusion automixis [56]), the genetic consequences of parthenogenesis and selfing are identical. Total homozygosity, on the other hand, can instantly occur in lineages using gamete duplication to restore ploidy [51].…”

Evolutionary mysteries in meiosis

“…as with vegetative reproduction), secondary asexuality is likely to evolve via modification of meiosis, keeping much of the cell signalling and machinery intact ( [65,76,80,81], see also §4). Indeed, detailed cytological and genetic investigations in several asexual species thought to reproduce clonally by mitotic apomixis have uncovered remnants of meiosis [73,[84][85][86]. In Daphnia, meiosis I is aborted mid-way and a normal meiosis II follows.…”

“…This raises two connected mysteries: why are some types of modifications much more frequent than others, and how can mitotic (or mitosis-like) asexual reproduction ('apomixis' or 'clonal parthenogenesis' in animals, 'mitotic apomixis' in plants) evolve from meiosis? Examples of meiosis-derived modes of asexual reproduction include chromosome doubling prior to meiosis ('endomitosis' or 'pre-meiotic doubling'), fusion of two of the four products of a single meiosis ('automixis' in animals, 'within-tetrad mating' in fungi), and suppression of one of the two meiotic divisions (included under 'automixis' or 'meiotic apomixis', depending on the author; see [68][69][70][71][72][73][74] for detailed descriptions of these processes).…”

Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

“…Several other forms of automixis are defined and discussed elsewhere (Bell 1982;Mogie 1986;Suomalainen et al 1987;Stenberg and Saura 2009;Archetti 2010;Lutes et al 2010;Neiman et al 2014;Nougué et al 2015). Their effects on genome-wide heterozygosity reduction are often very different from self-fertilization (e.g., complete loss or complete retention of parental heterozygosity).…”

“…However, the initial slope of the change in heterozygosity close to the centromere is 2d (where d is the genetic distance in Morgan) under terminal fusion and -d under central fusion (Figure 1, File S2), irrespectively of the degree of interference. In contrast, under self-fertilization, expected heterozygosity is 50% of the parental heterozygosity and does not depend on the distance from the centromere nor on the level of crossover interference.Several other forms of automixis are defined and discussed elsewhere (Bell 1982;Mogie 1986;Suomalainen et al 1987;Stenberg and Saura 2009;Archetti 2010;Lutes et al 2010;Neiman et al 2014;Nougué et al 2015). Their effects on genome-wide heterozygosity reduction are often very different from self-fertilization (e.g., complete loss or complete retention of parental heterozygosity).…”