Evolutionary mysteries in meiosis

Abstract

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'.

Keywords: automixis; epigenetics; genetic conflict; modified meiosis; origin of meiosis; recombination hotspots.

Figure 1.

Schematic of the different steps in standard meiosis. The top panel illustrates the different phases of a typical female meiosis for each of the two meiotic divisions: prophase (P, with early and late prophase distinguished), metaphase (M), anaphase (A) and telophase (T). The nuclear membrane is indicated by the green contour (dashed when it starts fragmenting). The small black circles represent microtubule organizing centres and the black lines represent microtubules of the meiotic spindle. First and second polar bodies are shown as grey circles next to the oocyte (chromosomes inside the polar bodies are not shown). Homologous chromosomes are represented with the same colour with slightly different shades (e.g. orange and light orange). Homologues pair and segregate in meiosis I, then sister chromatids segregate in meiosis II. The middle panel shows the meiotic cell cycle. The timing of the primary meiotic arrest is indicated by a red star, while the timing of the most common secondary arrests in different organisms is indicated by green stars (see §4a). The lower panel indicates the important steps (DSB formation, crossing overs) occurring during prophase I. The synaptonemal complex is shown in yellow. Chromatin condenses in chromosomes throughout prophase I (only one pair of homologues is illustrated). In most species, telomeres attach to the nuclear envelope. The attachment plate is indicated by a grey bar. MSCI, meiotic sex chromosome inactivation (see §4d).

Figure 2.

Schematic of meiosis and some of its modifications. (a) Regular meiosis. Following DNA replication, homologous chromosomes are separated in the first meiotic division, whereas sister chromatids are separated in the second division. COs result in chromosomes in the final meiotic products that carry genetic material from both homologous chromosomes. (b) Hypothetical ‘one-step’ meiosis, in which DNA replication before entering meiosis is suppressed and, therefore, only a single meiotic division is required. (c) Multivalent formation in a neo-tetraploid. Blue and orange chromosome pairs are assumed to be identical or very similar so that pairing can occur. Chiasmata of one chromosome with three other chromosomes leads to mis-segregation. (d) Bivalent formation in a tetraploid with exactly one CO per chromosome. Chromosomes may pair randomly (leading to polysomic inheritance), but segregation proceeds normally. (e) Inverted meiosis, in which sister chromatids are separated in the first division and homologous chromosomes in the second division. Note that although centromeres are shown here for clarity, all described species consistently using inverted meiosis are holokinetic (no centromeres). (f) Central fusion automixis, a mechanism of producing diploid eggs that can then develop parthenogenetically without fertilization. As a consequence of COs, heterozygosity may be lost with this mechanism in regions distal to the centromere.

Figure 3.

Hypothetical genome sequence containing three genes showing the distribution of ancient recombination hotspots in most model species (a) compared with derived PRDM9-mediated recombination hotspots (b). Studies in fungi, plants, birds and dogs indicate that ancestral hotspots are stable over long evolutionary timescales (up to millions of years) and concentrate at promoter regions and transcription start sites (and at stop sites in some species). These start and stop sites for each gene are indicated in yellow and red blocks, with their introns and exons represented by lines and black blocks, respectively. PRDM9-mediated hotspots are found in some mammals, including humans and mice, and are directed away from promotor regions. The DNA-binding zinc-finger in the PRDM9 protein targets specific sequence motifs; mutations in the zinc-finger array change the targeted motif, leading to rapid evolution of hotspot positions and an absence of hotspot conservation over short evolutionary timescales (at the population and species level).