# Cracking the meiotic secrets behind animals asexuality: when cytology seduces genomics to decode asexual meiosis

Caroline Blanc, Marie Delattre, Karine van Doninck

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Caroline Blanc, Marie Delattre, Karine van Doninck. Cracking the meiotic secrets behind animals asexuality: when cytology seduces genomics to decode asexual meiosis. 2025. hal-05393558

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# Cracking the meiotic secrets behind animals asexuality: when cytology seduces genomics to decode asexual meiosis

Caroline S. Blanc<fnref n="1" />, Marie Delattre<fnref n="2" />, Karine Van Doninck<fnref n="3" />

Handling editor: Richard Meisel, Associate editor: Denis Roze

Corresponding author: Caroline S. Blanc, Department of Ecology and Evolution, University of Lausanne, Biophore, CH-1015 Lausanne, Switzerland. Email: Caroline.blanc@unil.ch

## Abstract

Asexuality is a derived character, and asexual species have emerged multiple times independently throughout evolution. In animals, parthenogenesis, whereby a zygote inherits only its mother genome, requires female meiosis modification to produce unreduced gametes and compensate for the lack of outcrossing. Various changes in the meiotic steps have been identified. Here, we propose a simplified nomenclature when discussing asexuality in animals, as the existing terminology has caused many misinterpretations and may impede interdisciplinary collaboration. We also shed light on the constraints related to these meiotic modifications in asexual animals and their consequences on their genome. When recombination is preserved in parthenogens, most meiotic modifications should, according to Mendel's second law, result in a loss of heterozygosity (LOH). On the other hand, LOH can be prevented if recombination is either abolished or strongly reduced during meiotic prophase. Surprisingly, several recent examples have demonstrated that LOH can be prevented despite recombination. We will describe these examples in detail as they illustrate the constraints underlying the origin and evolution of asexuality. We also emphasize that the majority of mechanisms remain unknown in many species. This highlights the need to revisit the old literature using state-of-the-art cytological imaging and genomic techniques to shed light on these unexplored processes.

**Keywords:** meiosis, animal asexuality, parthenogenesis, loss of heterozygosity, recombination

## Introduction

Meiosis is a universal and specific type of cell division that allows all sexual eukaryotes to reproduce. This mechanism is highly conserved as it is found in unicellular eukaryotes, metazoans, plants, and fungi. During meiosis, chromosomes are randomly segregated during a two-step cell division process (following the second law of Mendel), which results in the production of gametes with reduced ploidy. Ploidy is re-established upon fertilization by the fusion of gametes, generating a descendant with a mixed genome. Moreover, meiosis is frequently accompanied by recombination between homologous chromosomes (homologues), facilitating the shuffling of alleles and thereby providing additional gene combinations for selection.

Besides sexual reproduction, asexual reproduction also evolved. This review will only discuss parthenogenesis in female animals (meaning “virgin birth” in Greek), whereby a gamete is produced through the germline but develops without outcrossing. Hence, we will particularly address these systems where lack of mixing between the parental genomes is compensated by modifying the female meiosis to maintain ploidy in progenies. We will not discuss reproduction by bud-

ding, fission, or fragmentation involving the soma. We will also not discuss hybridogenesis, where sperm/oocyte fusion takes place (Lavanchy & Schwander, 2019), nor androgenesis (Schwander & Oldroyd, 2016), in which the sperm nuclear DNA is only transmitted to the descendants. Haplodiploid systems are also not included here because although haploid males evolve from the maternal genome only (i.e., from haploid unfertilized oocytes), female meiosis follows the canonical two-step divisions (Kennedy, 2021).

It is now well established that asexuality is a derived character and that sexuality is the ancestral state in eukaryotes (Bell, 1982). Asexuals are found in many taxa but remain rare, although the exact proportion of asexuals has not been systematically quantified. Yet, asexuality is estimated to affect less than 0.1% of vertebrates (Vrijenhoek, 1998; White, 1973), while in insects, asexuality can reach 1.5% (Kooi et al., 2017; Liegeois et al., 2021). The widespread occurrence of sexual reproduction is, however, a paradox in evolutionary biology when considering its inherent costs. The key argument for this paradox is that all else being equal, an asexual should benefit from a twofold advantage over sexual parents due to the lack of investment in males (Maynard Smith, 1968, 1971,

<footnote n="1">¹Department of Ecology and Evolution, University of Lausanne, Biophore, Lausanne, Switzerland</footnote>

<footnote n="2">²Laboratory of Biology and Modeling of the Cell, Ecole Normale Supérieure de Lyon, CNRS UMR 5239, Inserm U1293, University Claude Bernard Lyon 1, Lyon, France</footnote>

<footnote n="3">³Department of Biology, University of Namur, URBE, Laboratory of Evolutionary Genetics and Ecology, Namur, Belgium</footnote>
1978, 1986). Nevertheless, very few species have renounced sex completely, suggesting substantial evolutionary benefits that affect its maintenance in the long term. In this review, we will not discuss this specific paradox of sexual reproduction, which has been detailed elsewhere (Barraclough et al., 2003; Birky Jr, 1996; Crow & Kimura, 1965; Engelstädter, 2017; Hartfield & Keightley, 2012; Kondrashov, 1993; Lenormand et al., 2016; Maynard Smith, 1968; Otto, 2009). Here, we explore another paradox imposed by meiotic divisions (and recombination) during the transition from sexual to asexual species. Indeed, any meiotic modifications that circumvent ploidy reduction should theoretically lead to a loss of heterozygosity (LOH), resulting in effective inbreeding. This can only be prevented if recombination is abandoned or specific mechanisms actively reduce LOH, but the absence of recombination can result in other disadvantages. Recent re-examinations of iconic asexual species, along with research on emerging species, have revealed that many asexuals—convergently—retain recombination and heterozygosity through distinct mechanisms. We will briefly discuss this convergence (the why) to gain insights into the trade-offs that shape the evolution of alternative reproductive strategies across taxa, but the bulk of the review will use these examples to highlight the importance of integrating detailed cytological analyses with state-of-the-art genomics to uncover the precise meiotic mechanisms behind asexual species (the how).

Such a transdisciplinary approach will benefit significantly from standardizing the nomenclature, which has been problematic in the field, to ensure a shared language between both cytology and genomics. Finally, through this review, we emphasize that many conclusions on asexuals have been based on weak cytological evidence or misunderstandings of cytology. The most significant is the widely accepted notion that asexuals have lost meiosis, which has led to many misinterpretations. To this end, we also propose in this review a simplification and a clarification of certain concepts.

Overall, the outline of this review is: (1) describe the differences between meiosis and mitosis and why asexual reproduction through the germ cells is never ameiotic, (2) describe the known mechanisms of ploidy maintenance and propose a more straightforward way to classify them and (3) underscore the meiotic modifications notably demonstrated in iconic asexual species, along with the mechanisms to reduce LOH despite recombination that have been uncovered thus far. We also discuss the cases of asexual species experiencing high LOH or loss of recombination and (4) conclude with a discussion of the new burning questions raised by these recent discoveries.

## Mitosis and meiosis are two very different types of cell divisions

As we will see, asexual species undergo a modified meiosis, which allows the maintenance of ploidy from mother to daughter. In some cases, these modifications are genetically identical to mitosis. Some famous asexuals have, therefore, been categorized as ameiotic or mitotic-like parthenogens (Normark et al., 2003; Schön et al., 2009). By extension, asexuality is often referred to as loss of meiosis. Here, we will demonstrate that although meiosis is modified to various extents in asexuals, these species still make gametes through a division process containing meiotic-like chromosomes, with hallmarks of meiosis being observed. Switching from meio-

sis to a mitotic program during gamete production is very unlikely. Indeed, meiosis is a sophisticated multi-step program with unique cellular features and involves other molecular actors than those during mitosis (Figure 1).

Mitosis is the somatic cell division that ensures the proliferation of somatic cells. During mitosis, the ploidy of the cells does not change. The chromosomes replicate at the start of mitosis during interphase (2n, 4C) and get equally distributed into two daughter cells (2n, 2C). Sister chromatids (SCs) are attached to the microtubules of the mitotic spindle and bi-oriented towards each of the two poles for segregation (Figure 1A and B). Daughter nuclei inherit one chromatid per homolog, i.e., an assortment of non-sister chromatids (NSCs).

Meiosis occurs only in germline cells and generates gametes. A canonical meiosis involves two successive divisions without replication in between (Figures 1A, B, and 2). In meiosis I, the homologues pairs form during meiotic prophase and later segregate apart. The ploidy has evolved from 2n, 4C to 1n, 2C (Figure 2). During meiosis II, the SCs separate from each other, and the ploidy evolves to 1n, 1C, producing reduced haploid gametes. The orientation of the attachment of the SCs to the spindle microtubules varies depending on the stage of meiosis: in meiosis I, within a given pair of homologues, the SCs are co-oriented to the same pole, whereas in meiosis II, SCs are bi-orientated to both poles. In most species, canonical meiosis involves the recombination of homologues, generating four chromatids per chromosome, each with slightly different genetic content (Figure 1). Each meiotic division in females, therefore, produces a haploid female pronucleus with a random genetic composition (containing 1 SC per homolog), while mitosis generates two diploid daughter cells that are genetically identical to the mother cell (containing 2 NSC).

A hallmark of canonical meiosis is the pairing (Figure 1C), whereby homologues recognize each other, enabling the formation of another hallmark, the bivalents (Figure 1B and C). Without pairing in meiosis I, the first meiotic division generally leads to aneuploidy (Lui & Colaiácovo, 2013; MacIennan et al., 2015). Indeed, because the SCs are co-oriented, each chromosome (pair of chromatids) can move in either direction instead of segregating away from its homolog (Figure 1A and C). In many species, pairing is achieved by forming another meiosis-specific element, the synaptonemal complex (Figure 1A and D: reviewed in Rubin et al., 2020). The synaptonemal complex is a ladder-like tripartite structure that physically connects the homologues (Figure 1C.i). The lateral parts of the synaptonemal complex are attached, inter alia, via specific cohesins (Sakuno & Hiraoka, 2022; Woglar et al., 2020). In many organisms, the pairing of homologues goes along with recombination. Recombination is the reciprocal exchange of part(s) of two SCs between homologues upon Double Strand Breaks induced by the meiotic-specific and highly conserved topoisomerase-like protein SPO11. This exchange creates a cohesive structure, the crossing-over, that stabilizes the association between homologues. The cytological manifestation of the crossing-over is the chiasmata, another hallmark of most meiosis. In the absence of crossovers (COs), homologues commonly fail to maintain cohesion (Figure 1B and E). Depending on the species, the establishment of the synaptonemal complex is dependent on Double Strand Breaks (yeast, humans, jellyfish, etc.) or independent (Caenorhabditis elegans, Drosophila melanogaster) (Blokhina et al., 2019; Boateng et al., 2013; Giroux C. 1989;
<figure><img src="image_2.png" /><figcaption>**Figure 1.** Canonical features of female Meiosis and Mitosis and their emblematic Cellular features. (A) Schematic representation of division in meiosis and mitosis cellular manifestations. i. Schema of mitosis anaphase. Mitosis is a symmetrical division that forms two identical daughter cells. In mitosis, centrosomes (stars) orchestrate the divisions. ii. IF of the mitosis anaphase the sexual sea urchin. MT is yellow, and DNA is blue. Adapted from Von Dassow (http://www.celldynamics.org/celldynamics/research/cytokinesis/index.html). iii. IF of the mitosis anaphase, the sexual nematode *Caenorhabditis elegans*. MT is green, and DNA is blue. Adapted from the Dumont website. Most meiosis divisions are acentriolar and asymmetric. iv. Schema of meiosis anaphases with Polar bodies Pbs extrusion. Each meiotic division extrudes one Pb. v. IF of the meiosis I anaphase the sexual nematode *C. elegans*. MT is green, and DNA is pink. Adapted from (Dumont https://www.ijm.fr/nos-equipes/dumont-lab-vf/). vi. IF of the meiosis I</figcaption></figure>
<figure><img src="image_3.png" /><figcaption>**Figure 1.** Continued</figcaption></figure>

anaphase the sexual mouse *Mus musculus*. Adapted from Dumont (2007). vii. DIC image of the mature oocyte of the sexual Human. Two pronucleus are present (male and female), and two polar bodies Adapted from Beuchat (2008). viii. DIC image of the mature oocyte of the asexual nematode *Diploscapter pachys*. Only one Pb is extruded, and only one pronuclei (female) is present. Adapted from Eweis (2022). ix. Schema of meiosis anaphases without Pb extrusion. No Pb is extruded, and all sets of chromatids undergo the two meiotic divisions. One pronuclei and three meiotic products are found at the end of the meiosis. x. IF of the meiosis I anaphase the asexual honeybee *Apis mellifera capensis*. Two sets of chromatids (c) are present. Adapted from Cole-Clark (2017). xi. IF of the meiosis II anaphase, the sexual fly *Drosophila melanogaster*. The two sets of homologous chromosomes that undergo meiosis II are aligned. MT is green, and DNA is red. Adapted from Loppin (2015). xii. IF of the mature oocyte of the sexual fly *D. melanogaster*. Three meiotic products and two pronuclei (male and female) are present. MT are green, and DNA is red. Adapted from Loppin (2015). (B) Schematic representation of chromatids segregation in mitosis and meiosis. In the metaphase of mitosis, sister chromatids (SCs) are bi-oriented toward different poles to separate them in the unique anaphase. No Pb is formed. In meiosis, during prophase I, Homologous chromosomes pair into bivalents (C) and recombine (E). Depending on the species, pairing (C) and recombination (E) occur in different orders. The structural stability of bivalents is ensured by the synaptonemal complex (D) and chiasmata(s) (E). SCs structure forms a univalent. In meiosis I, SCs are co-oriented toward the same pole. In anaphase I (meiosis I), Homologous chromosomes are separated, and one set of chromosomes forms the first Pb (A). In anaphase II (meiosis II), SCs are bi-oriented toward different poles. One set of SCs forms the second Pb (A). C) Pairing is a feature of meiosis. i. IF of chromosomes pairing in the sexual butterfly *Bombyx mori*. *B. mori* has 2n = 60 chromosomes, and 30 bivalents are present. DNA is in blue; the homologous chromosomes pair in prophase I. Adapted from Xiang (2024). The sketch represents a bivalent. ii. FISH of chromosomes pairing in the asexual bdelloid rotifera *Adineta vaga*. *A. vaga* has 2n = 12 chromosomes, and six bivalents are present. FISH probes are loaded on different locations of chromosomes 2 and 5. When paired, the red and green FISH staining overlaps. DNA is blue. Adapted from Terwagne (2022). iii. Karyotype of chromosomes pairing in the asexual and sexual crustacean *Daphnia pulex*. *D. pulex* has 2n = 24 chromosomes, and 12 bivalents are present. Adapted from Hiruta (2010). (D) The Synaptonemal complex. i. Transmission Electron Microscopy (TEM) of the three layers of the synaptonemal complex. Adapted from Ortiz (2016). ii. TEM of the synaptonemal complex of the sexual butterfly *Ephestia kuehniella*. Adapted from Marec and Traut (1993). iii. TEM of the synaptonemal complex of the asexual mite *Archegozetes longisetosus*. Adapted from Bergmann (2018). (E) Recombination and Chiasmata. i. IF of the chiasmata of the asexual nematode *Mesorhabditis belari*. Recombined chromatids are stained with EdU in pink and DNA in blue. Adapted from Blanc (2023). ii. IF of the chiasmata of the sexual lizard *Aspidoscelis tigris*. Multiple loops of chiasmata are observable in grey. Adapted from Lutes (2010). The sketch represents a pair of Homologous chromosomes where green circles highlight chiasmatas. In all the sketches, MT are green, chromatids are blue, homologous chromosomes are represented in different blue shades, the centrisome is the star, and the centromere is round. Microtubules (MT), SCs, Polar body (Pb), Immunofluorescence staining (IF), Differential Interference Contrast (DIC), Fluorescence In Situ Hybridization (FISH), TEM.
<figure><img src="image_4.png" /><figcaption>**Figure 2.** The three main categories of meiotic modifications in parthenogenetic systems, with nine sub-categories and their theoretical consequences at the genomic level. Each row includes each sub-category of meiosis with or without recombination. The first line refers to canonical meiosis. For simplicity, only meiosis with the production of polar bodies is shown in this category, whereas meiosis without cytokinesis also exists. Modification in this later case leads to fusion of meiotic products as shown in B. The two columns on the right show the genomic expectations in the long term with and without recombination. Haploid chromosomes are indicated by "n" and diploid by "2n"; "C" represents the number of chromatids. The sister chromatids are dark and light blue, corresponding to homologous chromosomes. LOH, Loss of Heterozygosity.</figcaption></figure>
<figure><img src="image_5.png" /><figcaption>**Figure 3.** Oocytes from asexual *Aspidoscelis tesselata* lizards contain twice the amount of chromosomal DNA compared to sexual *Aspidoscelis gularis* lizards. i. DAPI-staining of recombining chromosomes of asexual and sexual *Aspidoscelis*. ii. Quantification of the chromosome volumes for both species. Figure adapted from Lutes (2010).</figcaption></figure>

Ishiguro et al., 2014; Scherthan et al., 2014). The number of recombination events per chromosome is also highly variable (Chakraborty et al., 2017; Stapley et al., 2017). Some sexual species nevertheless show achiasmatic bivalents, i.e., chromosomes that are able to pair but do not undergo crossing-over. Hence, although pairing seems essential for properly segregating homologues during meiosis I, COs are dispensable (Lenormand & Dutheil, 2005; Rubin, 2024).

Another important landmark of female animal meiosis is asymmetry, which leads to a single very large oocyte after divisions, full of maternally contributed material (such as proteins, RNAs, and yolk, Figure 1B). When cell cleavages follow meiotic divisions, there is little size reduction because the meiotic spindle is small and positioned asymmetrically. Consequently, because cytokinesis bisects the spindle, tiny polar bodies are extruded, and the oocyte remains very large (Figure 1B.iv-viii). Of note, after meiosis I, the first polar body may or may not divide during meiosis II, depending on the species. Hence, some species show two tiny polar bodies on the side of the large oocyte, whereas others have three. In other species, for instance, in insects, the segregation of chromatids during the meiotic divisions is not accompanied by cell cleavages, leaving the large oocyte intact. The four products of meiosis align, and only one of those will become the oocyte pronucleus (Figure 1B.ix-xii) (Bourouh et al., 2016; Loppin et al., 2015; Riparbelli & Callaini, 2005). In both cases, this asymmetry is achieved thanks to the particular architecture of the meiotic spindle, which remains off-centre (Fabritius et al., 2011) and small because it does not scale with cell size (Crowder et al., 2015) (Figure 1B). It has been proposed that this asymmetric positioning is favoured by the absence of centrioles (Severson et al., 2016), which are degraded during oogenesis and reintroduced paternally at fertilization in many species (Delattre & Gönczy, 2004; Kalbfuss & Gönczy, 2023; Manandhar et al., 2005). Centrioles nucleate astral microtubules, which are necessary to position the spindle in the centre of the cell, thanks to the dynamic instability of microtubules. Acentriolar/anastral spindles can, therefore, remain off-centre. In mouse oocytes, for instance, this is achieved by pushing forces exerted by the actin cytoskeleton on the spindle (Almonacid et al., 2014). Nevertheless, the elimination of maternal centrioles is not a prerequisite for the proper positioning of the meiotic spindle. Indeed, centrioles and astral microtubules are maintained during female meiotic divisions in some echinoderms, molluscs, annelids, and nemertea

(Engelstädter, 2017; Kalbfuss & Gönczy, 2023; Manandhar et al., 2005). In starfish oocytes, these astral microtubules themselves participate in the asymmetric positioning of the spindle as they transport and anchor the centrioles at the plasma membrane (Borrego-Pinto et al., 2016).

Overall, although mitosis and meiosis both involve cell division, they transmit genetic material in very different ways, including distinct cellular and molecular features. We claim that, unless proven otherwise, all asexual animals described so far that reproduce through the germline undergo meiosis. As we will see in the next section, the difference between meiosis and mitosis is not only a semantic point but an important distinction when deciphering the mechanistic changes at the origin of asexuality (Sato et al., 2021).

## A cytological classification, clarification, and simplification of meiosis in parthenogens

In asexual animals, meiosis is adjusted and ensures that ploidy is maintained in the gametes produced despite the lack of paternal genome contribution. Many modifications to female meiosis leading to ploidy maintenance have been described in asexual species, particularly in exquisite detail by Suomalainen (Suomalainen, 1950, 1987). Here, we propose to group all these modifications into three broad categories only (Figure 2): endoreplication (before or after meiosis, Figure 2A), fusion of meiotic products (Figure 2B) or abortion of one meiotic division (Figure 2C) as outlined in the next section. Our classification is based on cytology. The following sections then highlight the genetic consequences of these meiotic modifications for each category.

## Two-step meiotic divisions with chromosome endoreplication

In this first category, ploidy is maintained by doubling chromosomes before or after the regular two-step meiotic divisions. DNA replication occurring before divisions is called pre-meiotic endoreplication and the cell has a ploidy of 4n, 8C in interphase (Figure 2A.i) (Dedukh et al., 2020; Dedukh, Altmanová, et al., 2022, 2024; Itono et al., 2006; Lutes et al., 2010; Newton et al., 2016; Spangenberg et al., 2024). Each chromosome is in two copies; the end product of meiosis is a gamete with two chromatids (2n, 2C). Depending on how the four chromosomes have formed the two pairs, the gamete will inherit two SCs or one chromatid per homolog (i.e., NSCs).
<figure><img src="image_6.png" /><figcaption>**Figure 4.** DAPI-staining of asexual ant species *Ooceraea biroi* that undergoes fusion of non-sister chromatids products during meiosis. Homologous chromosomes are paired in prophase I (28 bivalents). The two divisions occur to produce four meiotic products containing 14 chromatids. However, after anaphase II, the two central meiotic products fuse, restoring diploidy by assorting non-sister chromatids. The arrow indicates the fused products. Adapted from Oxley (2014). In the sketches, homologous chromosomes are represented in different blue shades.</figcaption></figure>

Some examples here include several parthenogenetic lizards of *Aspidoscelis* and *Darevskia* genera (Figure 3) or within the teleostean genera Loach, *Misgurnus*, and Cobiti (Dedukh, Altmanová, et al., 2024; Itono et al., 2006; Lutes et al., 2010). Of note, if recombination occurs between identical chromosomes, it is genetically identical to an absence of recombination (Figure 2A.i) (Lutes et al., 2010) (see below).

In other cases, the extra replication step occurs after the divisions, in a process called post-meiotic endoreplication (or “gamete duplication”) (Zhang et al., 2015) (Figure 2A.ii). This modification results in the presence of two identical chromatids in the gamete. Well-known examples include the hybrid teleostean genera *Carassius* and *Clarias* (Dedukh, Lisachov, et al., 2024; Zhang et al., 2015), the nematode species *Heterodera betulae* (Triantaphyllou, 1963).

## Two-step meiotic divisions followed by fusion of the meiotic products

In the second category, the two-step meiotic divisions are preserved, but ploidy is restored after fusion of two of the meiotic products. Fusion may arise when meiotic products are not extruded from the oocyte, as found in many insects for instance, the four initial products are arranged linearly, with NSCs in the two central products and SCs in the two external products. The product of fusion will be designated as the future zygote nucleus (2n, 2C) (Figures 2B and 4). Fusion of two external meiotic products leads to the assortment of SCs in the egg and has often been called “automixis terminal fusion” (Figure 2B.i). This is found, for instance, in the parthenogenetic sawfly *Pristiphora pallipes* (Comrie, 1938), the mayfly *Ephoron shigae* (Sekiné & Tojo, 2009), and *Drosophila mangabeirai* (Murdy & Carson, 1959). Conversely, the fusion of the two central products leads to the assortment of NSCs, often called “automixis central fusion” (Figure 2B.ii). The term was first used by Carson in 1961,

who found this mechanism during facultative parthenogenesis in *D. parthenogenetica*, *D. robusta*, and *D. mangabeirai* (Carson, 1961; Murdy & Carson, 1959; Stalker, 1954). The honeybee *Apis mellifera capensis*, the raider ant *Ooceraea biroi*, and the wasp *Venturia scanescens* are other examples of insects undergoing this fusion of the central products of meiosis (Figure 4) (Beukeboom & Pijnacker, 2000; Cole-Clark et al., 2017; Oxley et al., 2014).

The mechanism underlying these fusion events is still unknown. Interestingly, genetic mapping in Cape Honey Bee (*A. mellifera capensis*), where fusion of the two internal products (i.e., NSCs) occurs (see below), identified a single locus as the major determining factor for parthenogenesis (Oldroyd et al., 2021). This locus shows similarity with SMC proteins, which are essential for chromatid cohesion, suggesting that specific SMC proteins could prevent the complete separation of the first meiotic products, thereby promoting their fusion.

## Abortion of one meiotic division

### Abortive meiosis I

In some asexual species, the first meiotic division is initiated but aborted or skipped altogether. Consequently, there is no segregation of the homologues, and only SCs segregate during a single successful division (which corresponds to meiosis II). This leads to the assortment of NSCs with only one polar body formed (Figures 2C.i, ii, iii, and 5). For instance, although chromosomes were paired and started to segregate properly, meiosis I aborts during anaphase in the nematode species *Mesorhabditis belari* (Blanc et al., 2023) (Figure 5) and *Rhabditophanes diutinus* (Perrier et al., 2024), in the crayfish *Procambarus fallax f. virginalis*, in the bdelloid rotifer *Adineta* vaga (Terwagne et al., 2022) (Figure 5) and the parthenogenetic crustacean *Artemia* (Xu et al., 2023). The underlying mechanisms of abortion are unknown. Genetically, abortive meiosis I is identical to fusion of NSCs, although it is very
<figure><img src="image_7.png" /><figcaption>**Figure 5.** Abortive meiosis I in the asexual nematode *Mesorhabditis belari* (i) and the bdelloid rotifer *Adineta vaga* (ii). There are 10 bivalents (2n = 20) in *M. belari* and six bivalents (2n = 12) in *A. vaga*. For i. and ii. In prophase of meiosis I, homologous chromosomes are paired. In anaphase I, univalent segregation begins but is not completed. All univalent chromosomes then perform meiosis II. Anaphase II separates sister chromatids, and half of the sister chromatids are extruded into the unique polar body. Figure adapted from Blanc et al. (2023) and Terwagne et al. (2022). In the sketches, homologous chromosomes are represented in different blue shades.</figcaption></figure>

different cytologically, as it leads to a single complete meiotic division instead of two successive ones. As we will see below, misinterpretation of cellular traits has been problematic for some emblematic asexuals, and this is why the reconstruction of all the meiotic steps is essential.

In other species, meiosis I aborts because the homologues have failed to pair during meiotic prophase (Figures 1C and 2C.i). This would generally lead to aneuploidy during meiosis I (because of the co-orientation of SCs) unless this step is skipped, allowing SCs to segregate normally during meiosis II. The nematode species *Diploscapter pachys* (Fradin et al., 2017) and *Meloidogyne incognita* (Triantaphyllou, 1963, 1981), the teleostean Amazon molly *Poecilia for-mosa* (Dedukh, Cruz, et al., 2022) and *Carassius auratus* (Yamashita et al., 1993), or the annelid *Lumbricus linea-tus* (Christensen, 1960) are species for which the absence of chromosome pairing is unambiguously evident at the cyto-logical level. Because a lack of pairing prevents recombina-tion, this type of modified meiosis leads to an assortment of NSCs that are identical to those of the mother cell. Therefore, the outcome is genetically equal to mitosis (Figure 1B). In the past, these species for which a single division associated with an absence of recombination was suspected have often been called “mitotic-like” parthenogens and, by extension, “ameiotic,” which has led to the widespread but incorrect idea that asexuals do not undergo meiosis. They are also

often referred to as “apomictic” (meaning literally “absence of mixing”), but we will see below why this terminology has also led to confusion in the field. Abortive meiosis I, without homolog pairing and recombination, is only an extreme case of modified meiosis, whereby the first steps of meiosis are skipped.

The mechanisms of meiotic abortion are generally unknown. Yet, some interesting information has been obtained for a few species. When homologues fail to pair, this can be due to a defect in loading the synaptonemal complex, like in Amazon molly (Dedukh, Cruz, et al., 2022). In *Daphnia pulex* (where meiosis I is abortive, see below), precise genetic mapping com-paring cyclical with obligate parthenogens has highlighted the REC-8 locus as playing a significant role in meiotic changes. Although the mechanisms are still unclear, this finding sug-gests that mutations in this meiotic cohesin may be directly involved in the switch from regular to abortive meiosis I in asexual *D. pulex* (Eads et al., 2012; Molinier et al., 2021).

## Abortive meiosis II

Theoretically, ploidy could be restored by abortion of the second meiotic division. Genetically, this corresponds to an assortment of SCs (Figure 2C.iv and v). Most analyses pointing out this mechanism are based on genetics, show-ing a genome-wide homozygosity within a single generation without cytological confirmation. This mechanism has been
<figure><img src="image_8.png" /><figcaption>**Figure 6.** Artificial generation of one heteromorphic chromosome shows inverted meiosis in the asexual mealybug, *Planococcus citri*. X-irradiation on *P. citri* generates a unique heteromorphic chromosome where a single pair of sister chromatids (SCs) is partitioned into small and big sections. DAPI-staining of the first prophase presents five bivalents (2n = 10), and the arrow indicates the heteromorphic chromosome. During the first cycle of meiotic division, the small sections (i.e., SCs) of heteromorphic chromosomes separate into two sets of chromosomes, demonstrating that SCs separate first. Arrows point to the small sections of the heteromorphic chromatids, adapted from Bongiorni (2004). In the sketches, homologous chromosomes are represented in different blue shades.</figcaption></figure>

proposed in facultative parthenogenetic species such as elas-
mobranch sharks and rays (Chapman et al., 2008; Feldheim
et al., 2010, 2017; Harmon et al., 2016; Portnoy et al., 2014;
Robinson et al., 2011), the snake species *Boa constrictor*
*imperators*, *Epicrates cenchria cenchria*, and *Python regius*
(Booth et al., 2011; Ianni et al., 2023; Kinney et al., 2013), as
well as in the nematodes *Meloidogyne hapla* and *M. javanica*
(Liu et al., 2007; Van der Beek et al., 1998). However, we
found no compelling cytological evidence of abortive meio-
sis II in either natural or facultative parthenogenetic species.
Without such evidence, current genetic tools are unable to
differentiate between abortive meiosis II, fusion of SCs, or
post-meiotic endoreplication. As a result, there is no definitive
proof supporting the existence of abortive meiosis II.

The specific case of inverted meiosis

Inverted meiosis is an atypical meiosis where SCs segregate
first, while NSCs remain physically linked until the second
meiotic division (Figure 2C.iii and v). To date, inverted meiosis
has only been described in species with holocentric chromo-
somes, i.e., centromeres all along the chromosomes. It likely
evolved secondarily after the emergence of holocentricity, as
the chiasmata structure in holocentric chromosomes allows
for this inversion in chromatid separation (Bogdanov, 2016;
Mandrioli & Manicardi, 2020; Wrensch et al., 1994). Within
these groups of species (so far described in plants and some
insects), asexuals have emerged. Here, ploidy is maintained
by the abortion of one of the two meiotic divisions. Contrary
to canonical meiosis, abortion of the first event of meiotic
division, i.e., meiosis II, assorts SCs in the gamete (Figure
2C.v). While abortion of the second division, i.e., meiosis I,
assorts NSCs together (Figures 2C.iii and 6). Demonstrating

the existence of inverted meiosis is a complicated task, and
it has been proven so far only when two homologues of dis-
tinct morphological appearance existed (i.e., heteromorphic
chromosomes or using a method distinguishing homologues
(Wrensch et al., 1994). Inverted meiosis with abortive meiosis
I have been demonstrated in asexual mealybugs (Figure 6)
(Bongiorni et al., 2004). In the spider mite *Tetranychus urti-
cae*, a mechanism of inverted meiosis has been pointed out
using X-irradiation, generating heterologs (Feiertag-Koppen,
1976, 1980). It has also been proposed for oribatid mites
(Archetti, 2022), although this is not based on cytological evi-
dence, as discussed below.

Of the importance of nomenclature

In 1973, (Tremblay & Caltagirone, 1973), in “Fate of polar
bodies in insects” described two classes of modified meiosis:
“*In apomictic (or ameiotic) parthenogenesis, the eggs usually
undergo only one mitotic or parameiotic division, which is
equational, with expulsion of only one diploid polar body. In
meiotic (or automictic) parthenogenesis, maturation is reduc-
tional, and a haploid pronuclei and one or two polar bodies
are formed; the somatic number of chromosomes is restored
by fusion of two of the haploid nuclei resulting from matura-
tion or by fusion of two cleavage nuclei.*”

These terms and definitions have been widely used to clas-
sify parthenogenetic animals. We argue that they have gen-
erated a lot of confusion and misunderstanding in the field
because the number of polar bodies, the presence or absence
of fusion events, etc., are not good criteria to define the class
of modified meiosis and, hence, the genetic consequences of
the modifications (as described later). This is more than just a
semantic problem.
<table><caption>**Table 1.** Genomic consequences of recombination and chromatids assortment. The assortment of sister chromatids consistently results in the loss of heterozygosity, as does the assortment of non-sister chromatids with recombination.</caption><thead><tr><th rowspan="2"></th><th rowspan="2"></th><th>Assortment of NSCs</th><th>Assortment of SCs</th></tr><tr><th>Abortive meiosis I<br>Absence of pairing<br>Inverted meiosios with abortive meiosis I<br>Fusion of NSCs<br>Pre-meiotic endoreplication</th><th>Abortive meiosis II<br>Inverted meiosis with abortive meiosis II<br>Fusion of SCs<br>Post-meiotic endoduplication</th></tr></thead><tbody><tr><td rowspan="2">Recombination</td><td>✓</td><td>LOH</td><td>LOH</td></tr><tr><td>◎</td><td>no LOH</td><td>LOH</td></tr><tr><td colspan="4">Theoretical Long-term Expectations</td></tr></tbody></table>

The term “fusion” is extensively used in current literature on asexual reproduction, often conflating cytological phenomena with genetic content. “Terminal fusion” refers to the assortment of SCs, whereas “central fusion” denotes the assortment of NSCs. These terms are based on initial descriptions within a few specific taxa, namely fungi and insects, where fusion is effectively observed (Doty & Menez, 1960; Stalker, 1954). Asexual species restoring ploidy through a fusion event, mixing their own meiotic products, were also termed automictic. By contrast, asexual animals lacking homologous recombination and pairing, displaying an assortment of NSCs after a single division (hence, no fusion), as found in mitosis, have been called apomictic (which literally means an absence of fusion). For an obscure reason, apomixis has come to describe “mitotic-like parthenogenesis” only, which has rapidly drifted to the idea that apomixis reflects an absence of recombination and meiosis overall. Many species have next been classified as apomictic and ameiotic because no fusion events were cytologically observed, or the number of polar bodies produced were identical to those found in species where homologous pairing (and hence meiosis I) was absent. As discussed earlier, multiple ways exist to restore ploidy without any fusion event, while maintaining recombination and most steps of the meiotic process. This misclassification has occurred in rotifers, *Daphnia* and *Artemia*, for instance (see below). For these reasons, we propose throughout this review to avoid the terms “apomixis” and “automixis” because of the general confusion they have generated and use “fusion” only when it is cytologically shown. Instead, we recommend a simplified cytological classification (as described above), considering the genetic outcomes: SC or NSC assortment, with or without recombination (Table 1).

## LOH and recombination in asexuals: exploration of a paradox

We have seen above that depending on the cellular changes that allow ploidy restoration, the chromatids that are associated in the future zygote can be two SCs (endoreplication, abortion of meiosis II, fusion of SCs or post-meiotic endoreplication) or two NSCs (abortion of meiosis I or fusion of NSCs). These mechanisms of ploidy restoration in the absence of outcrossing have significant genetic consequences. In most cases, local or even a global LOH is expected on all chromosomes after one meiotic division or through time (Figure 2;

Table 1). Post-meiotic endoreplication will indeed generate an immediate LOH genome-wide (Figure 2A.ii). Assortment of SCs will also lead to rapid LOH, except for the portions distal to a CO site if recombination happens (Figure 2B.i, C.iv, and C.v). On the contrary, an assortment of NSCs will maintain heterozygosity but generate homozygous portions of chromosomes distal to the COs due to the random assortment of recombinant and non-recombinant chromatids (Figure 2B.i, C.ii, and C.iii). In the absence of outcrossing, these homozygous stretches will remain homozygous—except when random mutations arise—and progressively, the proportion of homozygous regions will increase over generations. Overall, asexuals are expected to have highly homozygous genomes unless recombination is abolished (Table 1). Surprisingly, the majority of asexual species studied so far display a relatively high level of heterozygosity (Jaron et al., 2021). How and why is this the case? Many asexual species originate as hybrids, inheriting a high heterozygosity (as discussed below) (Jaron et al., 2021). Moreover, for a long time, the prevailing view in the literature suggested that asexual species are ameiotic and lack recombination, which seemed consistent with these genetic observations. However, recent studies reveal that while asexual species generate gametes via meiosis, few have entirely abandoned recombination. This creates a persistent genetic paradox: despite recombination, many asexual species seem to maintain a genome-wide heterozygosity. The underlying mechanisms remain elusive, mainly due to a lack of studies integrating cytological evidence—essential for unambiguously identifying the meiotic alterations—with genome-wide analyses quantifying LOH. The few investigations combining these approaches have begun to shed light on this paradox, as explored below.

Until now, cytological evidence was often insufficient because many studies rely on older microscopy techniques or drawings, and more advanced methods are either challenging to implement or have yet to be applied. The rarity of samples compounds this challenge, the physical accessibility to the tissue of interest, or the difficulty in capturing brief meiotic events. Additionally, many genetic studies were performed before the advent of next-generation sequencing. They were based on a few marker loci with a potential bias towards poorly or highly recombining regions. Other studies used circular reasoning, such as “because the species is highly heterozygous, it must have lost recombination,” without cytological data to support these claims. This lack of rigorous
confrontation between cytological and genomic empirical data has led to many misinterpretations.

Below, we present data from asexual animal systems where the reevaluations of their reproductive mode were made possible mostly by combining cytology and state-of-the-art genomic.

## Some emblematic asexuals do undergo meiotic recombination—and cannot be called ameiotic anymore

The emblematic crustacean *Daphnia pulex* offers an insightful example; it is a cyclical parthenogenetic species. For a long time, meiosis during its asexual phase was described as “apomictic” or ameiotic (i.e., non-recombining) based on early cytological studies (Kühn, 1908; Ojima, 1954; Zaffagnini & Sabelli, 1972) but which is in contradiction with the large LOH stretches observed (Omilian et al., 2006). Revisiting the cytology solved this paradox. The initial studies inferred a mitotic-like division by focussing solely on the number of polar bodies (Tremblay & Caltagirone, 1973). Observing only a single polar body at the end of meiosis led the authors to conclude that meiosis I was absent and a process similar to mitosis, implying no recombination, occurred. Subsequent careful reinvestigations revealed that during the asexual phase, homologues pair at the onset of meiosis I, initiating segregation but aborting it, while meiosis II proceeds canonically. This produces an unreduced gamete with an assortment of NSCs and one polar body (Hiruta & Tochinai, 2012; Hiruta et al., 2010). Genomic analyses further confirmed that chromosomes in *D. pulex* recombine (Omilian et al., 2006; Xu et al., 2011). To conclude, this recombining asexual species exhibits LOH as expected, but it can be offset by occasional outcrossing during sexual events.

Another iconic asexual system was recently resolved, the bdelloid rotifer *Adineta vaga* (Judson & Normark, 1996). Bdelloid rotifers are a notorious ancient asexual metazoan clade that diversified into more than 460 asexual morphospecies without any description of males or male organs (Segers, 2007). The old cytology on the oogenesis of two bdelloid rotifer species revealed no pairing of homologues nor reduction in chromosome numbers (Hsu, 1956a, 1956b). Hence, they have been considered ancient asexual scandals because they evolved as strict mitotic parthenogens (“apomixis”) for millions of years (Tang et al., 2014) without recombination or outcrossing (Hsu, 1956a, 1956b). Terwagne et al. (2022) revisited the oogenesis of *A. vaga* using cytological methods, while its genome has been sequenced and recently assembled at the chromosome scale (Simion et al., 2021). The cytology revealed an abortive meiosis I in *A. vaga*, in which homologues form pairs but do not segregate (Figure 5ii), while a unique meiotic division segregates SCs with the formation of a single polar body (Terwagne et al., 2022). The genomic data identified six pairs of homologues with a mean heterozygosity of around 1.7%, but with large-scale LOH detected, representing signatures of recombination between homologues (Simion et al., 2021). Therefore, cytology agrees with the genomic observations: abortive meiosis I with heterozygosity being maintained except in recombining regions (Figure 2C ii). However, in the wild, *A. vaga* maintains a heterozygous genome along its chromosomes and a higher heterozygosity than laboratory strains (pers. comm.). At present, it remains unclear how bdelloid rotifer *A. vaga* prevents being highly homozygous in the wild while reproducing through a

non-reductional meiosis I with recombination. Hypotheses put forward include rare horizontal genetic exchanges and strong purifying selection, which may effectively eliminate individuals with deleterious alleles in a homozygous state. This selective pressure is particularly potent in large populations.

The brine shrimp *Artemia* represents another case of notorious asexual scandal (Judson & Normark, 1996). *A. parthenogenetica* is not a unique species but rather a group of lineages where parthenogenesis evolved several times (Sainz-Escudero et al., 2022) and whose origins date back between 10,000 and 1 million years, depending on the author (Muñoz et al., 2010; Perez et al., 1994; Rode et al., 2022). During the 20th century, the process of meiosis in *A. parthenogenetica* has been a subject of debate due to unclear definitions and incorrectly established terminology. Of the various parthenogenetic lineages, most are polyploids, which are not undergoing homologous recombination and fail meiosis I, and were considered “apomictic,” dividing mitotically. However, particular attention has been given to the asexual diploid Ap2n. Recent research on genomic and cytological aspects of Ap2n directly contradicts the “apomictic” conclusion and converges on the failure of meiosis I (Nougué et al., 2015; Xu et al., 2023). In the Ap2n lineage, recombination is still present with LOH signatures detected at a few marker loci, but the recombination rate appears lower than in sexual lineages (Haag et al., 2017). Ap2n *A. parthenogenetica* is, therefore, one more example of a recombining asexual experiencing low LOH. Possible explanations for the maintenance of heterozygosity are the decrease in recombination rate, the purging of the homozygote’s deleterious alleles, and- or rare sexual events in the wild (Boyer et al., 2021). Indeed, Ap2n females can occasionally produce rare males, which can cross with related sexuals and initiate the origin of new asexual lineages (contagious asexuality) (Boyer et al., 2021, 2023). Therefore, the persistence of recombination in Ap2n may be constrained by positive selection for rare sexual reproduction or contagious asexuality, which depends on residual male production and a minimal level of recombination.

## LOH could be limited despite recombination through overdominance selection

*Apis mellifera capensis*, the Cape Honey Bee, is a facultative parthenogenetic species. When the queen of a colony is lost, workers spontaneously produce queens and workers via parthenogenesis. From this population, a specific clone composed of workers reproducing asexually has emerged, referred to as the “Clone” (Oldroyd et al., 2011).

Joined cytology and genomics revealed that in *A. mellifera capensis* “Clone,” diploidy is maintained by randomly assorting NSCs (through a true fusion of meiotic products) with recombination being present. Despite a significant LOH compared to the sexual Capensis population, the Clone still maintains an unexpectedly high genome-wide heterozygosity level (Baudry et al., 2004; Cole-Clark et al., 2017; Goudie et al., 2012; Oldroyd et al., 2011). Heterozygosity appears to be maintained through selection against homozygous recombinants at specific genes under heterozygous advantage (overdominant loci), acting in linkage disequilibrium with neutral loci. In particular, progenies arising from recombination are eliminated from the population, ensuring the maintenance of heterozygosity. It has been demonstrated explicitly in *A. mellifera capensis* “Clone” for the complementary sex determining (*csd*) locus, which, at the homozygous state,
generates unviable diploid males. All loci linked to *csd* are never found at the homozygous state due to this over-dominance (Goudie et al., 2012). Goudie et al. (2014) also identified other loci on distinct chromosomes in *A. mellifera capensis* where heterozygosity is preserved, suggesting a potential heterozygote advantage. However, no direct fitness association was observed, and the specific overdominant loci remain unidentified. Finally, with a potentially high recombination and mortality rate in *A. mellifera capensis*, this asexual Clone can absorb the genetic load imposed by LOH at overdominant loci since a few fit descendants are sufficient to start a new population. Other examples of overdominance selection may exist but have not yet been identified.

## LOH can be avoided despite recombination through co-inheritance of the crossing-over products

In the nematode *Mesorhabditis belari*, asexual females are produced upon abortive meiosis I (Blanc et al., 2023). Here, chromosomes (which are holocentric) are paired. Evidence for recombination was confirmed using the incorporation of EdU (an analogue of thymidine) during germ cell proliferation, which allowed the labelling of one chromatid out of the two of a given chromosome. If two chromatids of different colours recombine (which statistically happens in 50% of the combinations), a bicolour chromatid should be visible. This approach revealed that all chromosomes recombine, and CO is not restricted to the tip of chromosomes but can occur all along the chromosomes. The analysis of linkage disequilibrium between loci also confirmed recombination. *M. belari* females are, therefore, recombinating asexuals with an assortment of NSCs, as observed in *D. pulex* and *A. vaga* (Hiruta et al., 2010; Terwagne et al., 2022). In such a scenario, LOH distally to the crossing-over is theoretically expected. However, the genome of *M. belari* is heterozygous genome-wide with no signs of LOH, even locally. There are two possible scenarios for reconciling these observations. The combination that assembles two chromatids of a given chromosome with similar portions, i.e., portions with LOH, may lead to dead animals, as shown above for the Apis Clone or suspected of the rotifer *A. vaga* of *Apis mellifera capensis*. Given that the species has ten pairs of chromosomes, elimination of progenies that have inherited two identical portions of a chromosome would generate a high lethality in the population, which is not observed. Alternatively, such combinations of chromatids are not evenly produced because the products of a crossover are co-inherited. In other words, if both CO products or none of the CO products go into the egg, heterozygosity is maintained for a given chromosome. This was confirmed by observing the co-inheritance of bicolour EdU chromatids, i.e., recombinant chromatids, in embryos at the end of meiosis I (Blanc et al., 2023).

Interestingly, the same type of non-Mendelian chromatid segregation has also been observed in the clonal raider ant *Ooceraea biroi* (Blanc & Delattre, 2024; Lacy et al., 2024). Unlike most ants, which have reproductive queens and mostly non-reproductive workers, all individuals in the colonies of *O. biroi* reproduce via parthenogenesis. Like in the nematode *M. belari*, *O. biroi* chromosomes repeatedly recombine with no evidence of LOH accumulation over generations. Recombination was demonstrated by sequencing rare haploid males and phased haplotypes from females. The data revealed an average of 0.4 COs per chromosome and meiosis event. Of the 144 recombination events identified, only one

led to partial LOH. Again, the lethality observed in the colony cannot explain the absence of animals with LOH. *O. biroi* is, therefore, another case of recombinating asexual, which maintains heterozygosity genome-wide by the selective sorting of recombinant chromatids during meiosis. Interestingly, *O. biroi* has monocentric chromosomes, suggesting that this mechanism is not restricted to holocentricity, as found in *M. belari*. Here, in contrast to *M. belari*, the meiotic divisions are complete, and ploidy is restored after fusion of the two products of meiosis I, i.e., NSCs. Although the first division seems complete here, we cannot exclude that the failure of completing meiosis I in both the nematode and the ant (because of fusion or because of an interruption during anaphase I, respectively) is the consequence of a persisting physical connection between the recombinant chromatids. Alternatively, chromatids could be physically separated but co-oriented during meiosis II because of some “tagging” or “memory” of the crossing-over (Blanc & Delattre, 2024; Lacy et al., 2024). More work will be needed to determine the mechanistic basis of co-inheritance and whether it is shared between these distantly related species. Interestingly, the co-inheritance mechanism might also be present in other species for which LOH is absent, and heterozygosity is uniform and high despite recombination. The following species display this pattern and would be potential candidates for a co-inheritance mechanisms: the Hymenoptera *Diglyphus wani* (Du et al., 2023), the nematode *Rhabditophanes diutinus* (Perrier et al., 2024), and this is also compatible with the patterns found in or Ap2n lineage of the brine shrimp *A. parthenogenetica* (Boyer et al., 2021; Nougué et al., 2015; Xu et al., 2023), etc.

Likewise, a mechanism based on asymmetric segregation of chromatids has been previously proposed for the other “asexual scandal” clade, the oribatid mites (Archetti, 2022). Cytological observations have revealed that the species *Platynothrus peltifer*, for instance, has holocentric chromosomes, which form bivalents at the onset of meiosis, strongly suggesting the chromosomes do recombine. From fixed samples, Taberly reconstituted the different steps of meiosis and concluded that the second meiotic division was abortive (Taberly, 1958, 1960). Oribatid mites would, therefore, belong to the category of recombinating asexuals, where SCs are assorted. A largely homozygous genome is expected in this case, except distally to the CO. However, oribatid mites of the *Oppiella* genus show only a small difference in heterozygosity between sexual and parthenogenetic strains (Brandt et al., 2021). To reconcile these results, it has been proposed that oribatid mites may undergo inverted meiosis (that would be simplified by the holocentricity of the chromosomes) combined with biased segregation of chromatids (called “Z segregation”), whereby the recombinant chromatids co-segregate (Archetti, 2022). Other scenarios have also been proposed whereby CO would be restricted to the chromosome ends upon non-inverted meiosis (Öztoprak et al., 2025). However, there is no cytological evidence of an inverted meiosis, nor terminal CO in oribatid mites at this stage. As mentioned above, heteromorphic chromosomes are needed to reconstruct the order of divisions formally. Besides, the description by Taberly is limited to a single drawing, which is difficult to interpret (Taberly, 1958). Therefore, it is also possible that oribatid mites are recombinating asexuals, fail meiosis I and avoid LOH through some of the mechanisms described above. The case of oribatid mites illustrates how important revisiting the old cytology is. However, as pointed out by Taberly himself
back in the 60s, exploring meiosis in these tiny mites is a real
challenge.

Non-recombining asexuals (avoiding LOH) are
often of hybrid origin

We have seen above how asexual species appear to maintain heterozygosity despite recombination. Here, we discuss the case of species that have lost recombination and, as expected, experience very low LOH accumulation (Engelstädter, 2017). The Amazon molly, *Poecilia formosa*, was described as the first parthenogenetic vertebrate (Hubbs & Hubbs, 1932). An in-depth cytogenetic analysis using markers of synaptone- mal complex proteins revealed that the chromosomes of *P. formosa* primary oocytes remain as univalents during mei- otic prophase, never proceeding to bivalent formation and homologous recombination (Dedukh, Cruz, et al., 2022). This impossibility to recombine in the absence of homologous pair- ing is consistent with genetic analyses showing that the het- erozygosity level of *P. formosa* is 10-fold higher than that of closely related sexual species. However, this elevated hetero- zygosity is most likely due to a hybridization event between two sexual species (Warren et al., 2018). Such heterozygosity may confer a fitness advantage in the short term (“the hybrid vigor”) by providing a resource for natural selection and increased fitness. Indeed, favourable heterozygosity may get “frozen” by asexual reproduction because recombination is absent (Konczal et al., 2021). Additionally, genetic diversity among clones may provide a short-term advantage to these asexual species in dealing with environmental changes. This may also be true for the non-recombining parasitic root-knot nematodes of the genus *Meloidogyne*. In the parthenogenetic species of this genus (*M. incognita* and *M. arenaria*), homo- logues are unable to pair, and only one division is observed, producing a single polar body (Marais, 1991; Triantaphyllou, 1963, 1981). Recent genomic studies on *M. incognita* con- firmed there is no evidence for recombination in this species (Koutsovoulos et al., 2020), with high heterozygosity levels observed, suggesting a hybrid origin (Blanc-Mathieu et al., 2017; Jaron et al., 2021). The parthenogenetic lizards of the genus *Aspidoscelis* are also of hybrid origin and show high heterozygosity. Although recombination is not abolished, it occurs between identical chromosomes after pre-meiotic post-meiotic endoreplication, which is another way to main- tain heterozygosity from mothers to offspring (Lutes et al., 2010).

More generally, a study by Jaron (2021) revealed that the majority of asexuals with high genome-wide heterozygosity levels are of hybrid origin. Hence, high heterozygosity may not be a direct consequence of the loss of recombination but may be maintained over time by the absence of recombination. One possible evolutionary scenario is that hybridization, which results in significant chromosomal divergence or polyploidy, impedes homologous pairing during meiosis I. Only those hybrids that bypass abortive meiosis I and proceed to meiosis II remain fertile and initiate an asexual lineage. While high heterozygosity and avoidance of extended LOH may offer short-term advantages, in the longer term, such species should theoretically increase their mutation load (Kondrashov, 1993; Muller, 1964). Asexual reproduction without recombination could, however, enable the species to persist if these hybridization events occur frequently, with new clones originating. Nevertheless, there are non-recombining asexuals for which the origin remains unknown, such as

the nematode *Diploscapter pachys* (Fradin et al., 2017) and *D. coronatus* (Hiraki et al., 2017). More work is needed to confirm whether recombination loss is systematically a threat to the long-term persistence of these species. At least, as discussed earlier, the iconic examples of ancient asexual “scandals”- historically categorized as non-recombining “mitotic” asexuals—have recently been revisited and show evidence of homologous recombination. The question is, therefore, still open.

Asexuals experiencing high LOH seem to cheat
with some sexual events

We have seen above that many strategies found in asexuals convergently prevent LOH. Here, we want to discuss the case of asexual species that do experience high LOH. Several asexual species restore ploidy through post-meiotic endoreplication, which immediately leads to genome-wide LOH. Species restoring ploidy through the assortment of SCs, whether by aborting meiosis II or fusing products of meiosis II, are also expected to experience substantial LOH, especially if crossing-over occurs near telomeres. Despite their highly homogeneous genomes, the persistence of these species remains an intriguing puzzle. However, species within this group appear to be facultative parthenogens, meaning they retain the ability to undergo sexual reproduction but switch to asexual reproduction (parthenogenesis) under specific conditions. Examples are found in the nematode species *M. hapla* (Liu et al., 2007; Triantaphyllou, 1966) or in sharks (Chapman et al., 2008; Feldheim et al., 2010, 2017; Harmon et al., 2016; Portnoy et al., 2014) and within some reptile species (Booth et al., 2011, 2023; Ianni et al., 2023; Kinney et al., 2013).

Many isolates of the plant-parasitic nematode *M. hapla* reproduce through facultative meiotic parthenogenesis (Liu et al., 2007; Triantaphyllou, 1966). In the absence of males, the diploid state is restored by fusion of products of meiosis II (i.e., SCs), resulting in a high homozygosity. Occasional sex events, however, occur, which produces males under stress conditions that can be crossed with females to produce heterozygous descendants (Liu et al., 2007).

Some *Timema* species are also homozygous asexuals, likely undergoing post-meiotic endreplication for over a million years. However, recent evidence of cryptic sex has been detected (Freitas et al., 2023), suggesting that immediate LOH can be compensated by occasional sexual events. These rare sexual occurrences may generate enough transient heterozygosity for homozygous individuals to arise and undergo selection, indicating that meiotic modifications may not pose a significant threat.

The retention of sexual capacities in a predominantly asexual population may provide an evolutionary advantage linked to high LOH, though the extent of this interconnection remains to be assessed. Further, studies on asexual and sexual *Saccharomyces* yeast suggest that high LOH can be adaptive in specific contexts, potentially accelerating adaptation (Heil, 2023). Nevertheless, further research is needed to identify whether species with high LOH can persist in the long term without outcrossing.

Conclusion

For a long time, it was widely believed that asexuality in animals was associated with the absence of meiosis and, hence, recombination. This perspective reconciled with the
observations that most asexuals possess highly heterozygous genomes. As the present review illustrates, recent revisits and exploration of more species show that many asexual animal species have retained meiotic recombination. Hence, a paradox emerged because, upon homologous recombination, heterozygosity should be rapidly lost.

Through precise examples given above, we have shown that asexuals have evolved various convergent strategies to maintain heterozygosity despite recombination. These include non-Mendelian meiotic segregation, overdominance selection against homozygous loci, strong purifying selection, and periodic genetic resetting through occasional sexual reproduction. In some asexual systems, recombination can also result in the production of rare males that can produce new asexual clones from sexual populations (contagious asexuality) or contribute to sporadic sexual reproduction.

The recurrent emergence of such mechanisms now calls into question the selective advantage of preventing LOH and maintaining recombination in asexual lineages. Upon transition to asexuality through a modified meiosis that induces LOH, recessive deleterious mutations may become exposed, resulting in a form of inbreeding depression and an immediate decline in fitness within the asexual lineage (Maynard Smith, 1978). However, this effect can be mitigated if the population size is sufficiently large or the recombination rate is relatively low. Nevertheless, it may be that those meiotic modifications that avoid immediate LOH are more often selected during the transition to asexuality.

In the long term, however, the selective advantages of LOH avoidance are less clear. LOH might also be beneficial because it unmasks beneficial recessive alleles, conferring significant fitness advantages, as observed in asexual yeast populations (Heil, 2023) and, at the same time, can reduce the mutation load more effectively by eliminating deleterious alleles through strong purifying selection.

On the other hand, having completely independent haplotypes, when LOH is avoided, may also be beneficial by allowing balancing selection (different haplotypes are favoured under different conditions) and greater diversity within a population. Such independent haplotype evolution, with relaxed selection on one and conservation of the other copy, has been recently revealed for the oribatid mite *P. peltifer* (Öztoprak et al., 2025).

What about the selective advantage of retaining recombination? There could be selection to maintain recombination because the complete absence of recombination presents a threat, as it prevents the purging of deleterious mutations (McDonald et al., 2016). Without any recombination, degeneration is frequently observed, as demonstrated by the evolution of sex chromosomes (Bachtrog, 2006). However, in the long term, recombination is expected to be ineffective in animals that do not undergo any outcrossing, as there are few alleles to reshuffle (Glémin et al., 2019). In the short term, if recombination is maintained, there is an accumulation of LOH at varying rates depending on the mechanism of ploidy maintenance, which is not necessarily advantageous either. Ultimately, recombination may be preserved in most asexuals not because it confers a selective advantage but only because mechanistically, it is not simple to abandon meiotic recombination from a sexual ancestor in which the entire machinery was present and efficient. Unless the first meiotic division is entirely bypassed and chromatid orientations are fully restructured in a single division, the lack of recombina-

tion will likely disrupt meiosis I, generating aneuploidy, as chiasmata are essential for proper chromosome segregation.

Overall, the reasons why LOH is generally avoided despite recombination remain unclear. Further exploration of asexual systems is needed to uncover the other constraints at play, which are difficult to envision today, given the limited number of well-characterized species. We hope our review will inspire more research groups to systematically sequence and investigate the meiotic processes of an increasing number of asexual organisms.

Many interesting asexual species clearly deserve more exploration, either because cytological and/or genomic studies have not yet been conducted, have not been compared, or require re-evaluation. For instance, weevils, a diverse group rich in parthenogenetic species, have long been considered non-recombining asexuals. However, recent cytological exploration of five species reveals that they undergo meiotic recombination and assort NSCs following the failure of meiosis I (Rożek et al., 2009). While the cytology is now well understood, genomic data are still lacking. On the other hand, the genome of three *Darwinulid* ostracod species has now been released (Van et al., 2021), but cytological data are still missing despite these non-marine ostracods being emblematic ancient asexuals. In the parthenogenetic wasp *Venturia canescens*, meiosis is modified and fuses the meiotic products containing NSCs (Figure 2B.ii) (Beukeboom & Pijnacker, 2000). However, the cytological outcome has not yet been confronted with the genomic data despite the recent release of the genome (Mao et al., 2023). Another intriguing group is tardigrades, known for their extreme resistance to desiccation and ionizing radiation. This clade includes sexual, parthenogenetic, and hermaphroditic species, which can coexist. Cytological studies have been performed on distinct species without conclusive results. Ammermann (1967) suggested that diploidy is restored during meiotic parthenogenesis by dividing univalents (i.e., SCs unit) before the second meiotic division, resulting in homozygosity across the genome. Studies by Bertolani (Bertolani, 1971, 1979, 1982, 2001; Bertolani & Buonagurelli, 1975) on sexual and parthenogenetic tardigrade species highlighted the absence of males and the presence of polyploid female populations without inferring the exact parthenogenetic reproductive mode. Finally, Altiero (2015) observed bivalents in an asexual tardigrade species without any details on the oogenesis process. Additional studies combining cytology and genomics are, therefore, timely in tardigrades. While aphid asexuality has been extensively studied, the cellular mechanisms underlying the meiotic modifications remain largely unexplored. The same applies to termites. In these eusocial insects, reproduction is typically restricted to a few individuals, namely the queens (similar to many hymenopteran species). Queens produce workers sexually, but new queens often arise through parthenogenesis. In their review, Hellemans and Roisin (2020) describe the parthenogenetic mode of reproduction known as asexual queen succession. Based on genetic studies, they conclude that ploidy restoration is either through the fusion of meiotic products (Figure 2B) or post-meiotic endoreplication (Figure 2A.ii), depending on the transition rate to homozygosity. However, no cytological data exist to confirm these processes of ploidy restoration. Other taxa rich in asexual species but poorly studied include earthworms and planarians.

Ultimately, the rarity of asexuals may not be solely due to long-term consequences but also because their emergence
requires highly specific modifications (Engelstädter, 2008; Levitis et al., 2017). Despite this, asexuals provide a great diversity of systems to explore, having originated repeatedly and independently across distinct clades throughout evolution, showing distinct meiotic modifications. This intriguing flexibility offers a valuable opportunity for more in-depth studies, comparing different species within the same genus or even different sub-populations of a single species that use various strategies to maintain ploidy without sexual reproduction. To conclude, asexual species are an invaluable resource for uncovering the flexible mechanisms of meiosis that remain hidden when studying canonical sexual species.

## Data availability

No new data were generated for this review. All data presented herein were produced in previously published studies and are appropriately cited in the references.

## Author contributions

Caroline S. Blanc (Conceptualization, Investigation, Resources, Writing—original draft, Writing—review & editing [equal]), Marie Delattre (Conceptualization, Investigation, Resources, Writing—original draft, Writing—review & editing [equal]), and Karine Van Doninck (Conceptualization, Investigation, Resources, Writing—original draft, Writing—review & editing [equal])

## Funding

This review is funded by the European Research Council (ERC, No Sex No Conflict project 864672, granted to Tanja Schwander) to C.S.B., the Agence Nationale de la Recherche (ANR-19-CE02-0012-01) for M. D. and a ERC grant (RHEA, 725998) for K. V. D.

## Acknowledgments

We would like to express our gratitude to Matthieu Terwagne for assisting us in gathering information on the meiosis of various species.

## Conflicts of interest

None declared.

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