Localization of the genetic determinants of meiosis suppression in Daphnia pulex

Abstract

Although approximately 1 in 10,000 animal species is capable of parthenogenetic reproduction, the evolutionary causes and consequences of such transitions remain uncertain. The microcrustacean Daphnia pulex provides a potentially powerful tool for investigating these issues because lineages that are obligately asexual in terms of female function can nevertheless transmit meiosis-suppressing genes to sexual populations via haploid sperm produced by environmentally induced males. The application of association mapping to a wide geographic collection of D. pulex clones suggests that sex-limited meiosis suppression in D. pulex has spread westward from a northeastern glacial refugium, conveyed by a dominant epistatic interaction among the products of at least four unlinked loci, with one entire chromosome being inherited through males in a nearly nonrecombining fashion. With the enormous set of genomic tools now available for D. pulex, these results set the stage for the determination of the functional underpinnings of the conversion of meiosis to a mitotic-like mode of inheritance.

Figure 1.—

Schematic of the breeding systems of the alternative forms of Daphnia pulex. Note that (1) cyclical parthenogens are not truly “cyclical,” as they are capable of switching to sexual reproduction at any time, and (2) not all cyclical or obligate parthenogens produce males, although males are essential for resting-egg production by cyclical parthenogens and nonessential in obligate asexuals.

Figure 2.—

A phylogeny of cyclically parthenogenetic (dotted lines, regular type) vs. obligately asexual (solid lines, boldface type) lineages based on mitochondrial sequence (including both silent and replacement sites). The scale is in units of substitutions per nucleotide site, and the bootstrap support for individual nodes is given on internal branches (in percentage). Tree construction used the neighbor-joining method (Saitou and Nei 1987), as implemented in MEGA (Tamura et al. 2007). Ages of various clades are determined from silent-site divergence alone, as described in the text. The base of the tree is rooted with sequences from two clones of Daphnia melanica. Clone notation: state/province, clone number, breeding system (A, obligately asexual; S, cyclical parthenogen).

Figure 3.—

Estimates of the degree of average marker subdivision between the aggregated sets of sexual and asexual lineages.

Figure 4.—

Estimates of the average degrees of marker heterozygosity and allelic-size divergence for each chromosome with respect to the alternative breeding systems. The dashed line in the top denotes the level of heterozygosity expected in a purely asexual lineage under mutation–gene conversion equilibrium.

Figure 5.—

Chromosomal distribution of marker significance associated with obligate asexuality vs. cyclical parthenogenesis. Bars on the left denote regions containing markers with asexual–sexual G_st values significant at the level P < 0.001 and extend to the midpoints with the first flanking markers on both sides deemed as insignificant. The statistic D is a more conservative measure of significant phenotypic association, the number of standard errors by which the asexual–sexual measure of G_st exceeds the upper bound on the baseline value (0.08).

Figure 6.—

Dynamic takeover of a sexual population by the invasion of a male-producing obligate asexual, starting with an initial asexual frequency of 0.0001. n denotes the number of freely segregating loci containing dominant alleles essential to sex-limited meiosis suppression, with obligate asexuality being conferred only on individuals harboring such alleles at all n loci.