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, 201 (3), 1143-55

Uncovering Cryptic Asexuality in Daphnia Magna by RAD Sequencing

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Uncovering Cryptic Asexuality in Daphnia Magna by RAD Sequencing

Nils Svendsen et al. Genetics.

Abstract

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: Daphnia magna; automixis; breeding system; genome-wide heterozygosity; inbreeding; nonmale producers; tychoparthenogenesis.

Figures

Figure 1
Figure 1
Expected interchromosomal (A) and intrachromosomal patterns (B) of heterozygosity reduction in automictic offspring. (A) The proportion of individuals that retain parental heterozygosity at a given number (out of 10) centromeric regions. Solid bars represent automictic offspring, which should always have either 0 or 10 heterozygous centromeric regions (the relative proportion of individuals with heterozygous vs. homozygous regions depends on the proportion of offspring produced by central vs. terminal fusion; here 2/3 central fusion is assumed). The open bars represent self-fertilized controls. (B) Expected offspring heterozygosity as a function of the genetic distance from the centromere under central (dashed) and terminal (solid) fusion and different degrees of crossover interference (File S2). ν = 1 corresponds to no interference, and the two gray lines correspond to complete interference. The dashed gray line gives the expected heterozygosity for centromere–distal markers (2/3).
Figure 2
Figure 2
Observed number of individuals that retained parental heterozygosity at a given number (out of 10) of centromeric regions. Solid bars represent offspring of the AST-01-04 NMP clone, open bars, offspring of the RM1-18 MP clone. For LG3 only the region at 90.8 cM was considered.
Figure 3
Figure 3
Heterozygosity as a function of the distance from the centromere under (A) automixis (terminal fusion only, N = 7 offspring) and (B) self-fertilization (N = 27 offspring). Dark blue lines represent averages across all chromosome arms with N chromosome arms (gray dots) according to the secondary y-axis. Light blue lines represent the 95% confidence limits, and the dashed lines, the expected heterozygosity and asymptotes under different degrees of recombination interference (see Figure 1). (C) Realized heterozygosity along linkage group 6 (automictic offspring, left; self-fertilized offspring, right) for illustration. The black triangle shows the presumed centromere position. The patterns of all linkage groups are shown in Figure S1. All heterozygosities are expressed in percentage of parental heterozygosity.

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