Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex

Hiruta, Chizue; Nishida, Chizuko; Tochinai, Shin

doi:10.1007/s10577-010-9159-2

Cited by 78 publications

(88 citation statements)

References 21 publications

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“…Although we lack comparable sources of expression data in Daphnia, the apparent increase in Cdc20 expression we observe here in parthenogenic individuals is consistent with current model of parthenogenic oogenesis in D. pulex, which is known to consist of abortive Meiosis I followed by a normal, Meiosis II-like division (Hiruta et al 2010). The apparent differential regulation of meiotic and cell cycle genes observed here may provide a glimpse of the transcriptional changes that accompany parthenogenesis in D. pulex.…”

Section: Discussionsupporting

confidence: 86%

Promoter Architecture and Sex-Specific Gene Expression in Daphnia pulex

et al. 2016

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Large-scale transcription start site (TSS) profiling produces a high-resolution, quantitative picture of transcription initiation and core promoter locations within a genome. However, application of TSS profiling to date has largely been restricted to a small set of prominent model systems. We sought to characterize the cis-regulatory landscape of the water flea Daphnia pulex, an emerging model arthropod that reproduces both asexually (via parthenogenesis) and sexually (via meiosis). We performed Cap Analysis of Gene Expression (CAGE) with RNA isolated from D. pulex within three developmental states: sexual females, asexual females, and males. Identified TSSs were utilized to generate a "Daphnia Promoter Atlas," i.e., a catalog of active promoters across the surveyed states. Analysis of the distribution of promoters revealed evidence for widespread alternative promoter usage in D. pulex, in addition to a prominent fraction of compactly-arranged promoters in divergent orientations. We carried out de novo motif discovery using CAGEdefined TSSs and identified eight candidate core promoter motifs; this collection includes canonical promoter elements (e.g., TATA and Initiator) in addition to others lacking obvious orthologs. A comparison of promoter activities found evidence for considerable statespecific differential gene expression between states. Our work represents the first global definition of transcription initiation and promoter architecture in crustaceans. The Daphnia Promoter Atlas presented here provides a valuable resource for comparative study of cis-regulatory regions in metazoans, as well as for investigations into the circuitries that underpin meiosis and parthenogenesis.

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Section: Discussionsupporting

confidence: 86%

Promoter Architecture and Sex-Specific Gene Expression in Daphnia pulex

et al. 2016

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“…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.…”

Section: (C) Meiosis Modifications and Loss Of Sexmentioning

confidence: 99%

Evolutionary mysteries in meiosis

Lenormand

Engelstädter

Johnston

et al. 2016

Phil. Trans. R. Soc. B

135

133

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One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Meiosis is a key event of sexual life cycles in eukaryotes. Its mechanistic details have been uncovered in several model organisms, and most of its essential features have received various and often contradictory evolutionary interpretations. In this perspective, we present an overview of these often 'weird' features. We discuss the origin of meiosis (origin of ploidy reduction and recombination, two-step meiosis), its secondary modifications (in polyploids or asexuals, inverted meiosis), its importance in punctuating life cycles (meiotic arrests, epigenetic resetting, meiotic asymmetry, meiotic fairness) and features associated with recombination (disjunction constraints, heterochiasmy, crossover interference and hotspots). We present the various evolutionary scenarios and selective pressures that have been proposed to account for these features, and we highlight that their evolutionary significance often remains largely mysterious. Resolving these mysteries will likely provide decisive steps towards understanding why sex and recombination are found in the majority of eukaryotes.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

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“…According to this hypothesis, rare automictic reproduction (tychoparthenogenesis) with mixed fusion may become more frequent, with subsequent selection for increased rates of central fusion and repression of recombination. Parthenogenetic reproduction in Daphnia has indeed been termed an intermediate between clonal and automictic reproduction because subitaneous, parthenogenetic eggs are produced by a modified meiosis rather than by mitosis (Hiruta et al 2010;Hiruta and Tochinai 2012). Specifically, the homologs pair and start to separate, but meiosis I is not completed, and sister chromatids of a diploid set of chromosomes are separated during meiosis II (Hiruta et al 2010).…”

Section: Automixis and Diversity Of Breeding Systems In Daphniamentioning

confidence: 99%

“…Parthenogenetic reproduction in Daphnia has indeed been termed an intermediate between clonal and automictic reproduction because subitaneous, parthenogenetic eggs are produced by a modified meiosis rather than by mitosis (Hiruta et al 2010;Hiruta and Tochinai 2012). Specifically, the homologs pair and start to separate, but meiosis I is not completed, and sister chromatids of a diploid set of chromosomes are separated during meiosis II (Hiruta et al 2010). In other words, meiosis I is suppressed, which is identical to central fusion (Asher 1970), but it is also indistinguishable from purely clonal reproduction as long as no recombination occurs during the paring of homologs (a low degree of exchange occurs in D. pulex, Omilian et al 2006;Tucker et al 2013).…”

Section: Automixis and Diversity Of Breeding Systems In Daphniamentioning

confidence: 99%

“…Hence it may be necessary to more explicitly account for the mechanism of this transition to fully understand the selection pressures acting during the evolution of parthenogenesis from sexuality. Furthermore, the same processes may also be important for understanding the maintenance of asexuality: If clonal parthenogenesis is indeed meiosis derived, there may be residual rates of recombination during homolog pairing (Hiruta et al 2010), such that transitions to homozygosity and loss of complementation may occur at higher rates than under purely mitotic parthenogenesis (Archetti 2004(Archetti , 2010Nougué et al 2015).…”

Section: Automixis and Diversity Of Breeding Systems In Daphniamentioning

confidence: 99%

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Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

et al. 2015

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The breeding systems of many organisms are cryptic and difficult to investigate with observational data, yet they have profound effects on a species' ecology, evolution, and genome organization. Genomic approaches offer a novel, indirect way to investigate breeding systems, specifically by studying the transmission of genetic information from parents to offspring. Here we exemplify this method through an assessment of self-fertilization vs. automictic parthenogenesis in Daphnia magna. Self-fertilization reduces heterozygosity by 50% compared to the parents, but under automixis, whereby two haploid products from a single meiosis fuse, the expected heterozygosity reduction depends on whether the two meiotic products are separated during meiosis I or II (i.e., central vs. terminal fusion). Reviewing the existing literature and incorporating recombination interference, we derive an interchromosomal and an intrachromosomal prediction of how to distinguish various forms of automixis from self-fertilization using offspring heterozygosity data. We then test these predictions using RAD-sequencing data on presumed automictic diapause offspring of so-called nonmale producing strains and compare them with "self-fertilized" offspring produced by within-clone mating. The results unequivocally show that these offspring were produced by automixis, mostly, but not exclusively, through terminal fusion. However, the results also show that this conclusion was only possible owing to genome-wide heterozygosity data, with phenotypic data as well as data from microsatellite markers yielding inconclusive or even misleading results. Our study thus demonstrates how to use the power of genomic approaches for elucidating breeding systems, and it provides the first demonstration of automictic parthenogenesis in Daphnia.KEYWORDS genome-wide heterozygosity; breeding system; inbreeding; automixis; tychoparthenogenesis; Daphnia magna; nonmale producers W HILE humans and most other mammals reproduce exclusively by sexual reproduction with sexes being determined by the well-known XY sex-chromosome system, the breeding systems of many other organisms, including many pests and parasites, remain unknown (Bell 1982;Normark 2003). The breeding system sensu lato, (including details of meiosis, e.g., recombination patterns and syngamy, e.g., levels of inbreeding, as well as their variants, e.g., modified meiosis in parthenogens) represents a key for understanding the biology of a species and has profound effects on its ecology, evolution, and genomics. Yet investigating breeding systems is often far from straightforward: Many species cannot easily be cultured and bred in the laboratory and observations of breeding behavior in nature are difficult. Even in species than can be bred in the laboratory, parts of the breeding system may be cryptic and not directly observable.The advent of high-throughput genotyping methods opens an alternative possibility that can be used on a much larger array of species: indirect inference of the breeding system usi...

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Abortive meiosis in the oogenesis of parthenogenetic Daphnia pulex

Cited by 78 publications

References 21 publications

Promoter Architecture and Sex-Specific Gene Expression in Daphnia pulex

Promoter Architecture and Sex-Specific Gene Expression in Daphnia pulex

Evolutionary mysteries in meiosis

Uncovering Cryptic Asexuality in Daphnia magna by RAD Sequencing

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