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Meiosis and Its Deviations in Polyploid

Cytogenet Genome Res 2013;140:185203 DOI: 10.1159/000351731

Meiosis and Its Deviations in Polyploid Animals

P. Stenberg a, b A. Saura a

a Department of Molecular Biology, and b Computational Life Sciences Cluster (CLiC), Ume University, Ume , Sweden

parthenogenesis, meiosis is replaced by what is effectively mitotic cell division. The above modes have different evolu-tionary consequences, which are discussed. See also the sis-ter article by Grandont et al. in this themed issue.

Copyright 2013 S. Karger AG, Basel

Polyploid plants are ecologically and economically im-portant [see e.g. Tate et al., 2005]. While polyploidy is less common among animals, there is nevertheless a long and diverse list of recorded cases [Gregory and Mable, 2005]. Some polyploid animals are considered pests [Stenberg and Lundmark, 2004; Hendrix, 2006], while others have profound effects on ecology [Darwin, 1881; Hendrix, 2006]. Due to the limited importance and relative rarity of animal polyploidy, published studies of meiosis in polyploid animals have been limited in scope and have largely focused on a small number of animal groups. The analyses performed in these investigations do not gener-ally match the sophistication and power seen in the anal-yses of factors both at the genetic and molecular level that operate in polyploid plants [Grandont et al., 2013]. A sig-nificant fraction of the existing literature on the modes of meiosis in polyploid animals is old and written in lan-guages other than English. However, it is important to acknowledge the importance of polyploidy in the evolu-tion of animals: 2 rounds of historical polyploidization

Key Words Gynogenesis Hybridogenesis Kleptogenesis Parthenogenesis

Abstract We review the different modes of meiosis and its deviations encountered in polyploid animals. Bisexual reproduction in-volving normal meiosis occurs in some allopolyploid frogs with variable degrees of polyploidy. Aberrant modes of bi-sexual reproduction include gynogenesis, where a sperm stimulates the egg to develop. The sperm may enter the egg but there is no fertilization and syngamy. In hybridogenesis, a genome is eliminated to produce haploid or diploid eggs or sperm. Ploidy can be elevated by fertilization with a hap-loid sperm in meiotic hybridogenesis, which elevates the ploidy of hybrid offspring such that they produce diploid gametes. Polyploids are then produced in the next genera-tion. In kleptogenesis, females acquire full or partial ge-nomes from their partners. In pre-equalizing hybrid meiosis, one genome is transmitted in the Mendelian fashion, while the other is transmitted clonally. Parthenogenetic animals have a very wide range of mechanisms for restoring or main-taining the mothers ploidy level, including gamete duplica-tion, terminal fusion, central fusion, fusion of the first polar nucleus with the product of the first division, and premei-otic duplication followed by a normal meiosis. In apomictic

Published online: June 18, 2013

Anssi Saura Department of Molecular Biology Ume University SE901 87 Ume (Sweden) E-Mail Anssi.Saura @ molbiol.umu.se

2013 S. Karger AG, Basel14248581/13/14040185$38.00/0

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(paleopolyploidy) have evidently played key roles in the evolution of vertebrates [Van de Peer and Meyer, 2005; Mable et al., 2011]. Encouraging the future study of the mechanisms of meiosis and its deviations in recent poly-ploidy animals is an aim of our review.

As is the case in plants, many polyploid animals are allopolyploids, i.e. their polyploidy originates from the hybridization and subsequent genome duplication of 2 different species or at least different evolutionary lineag-es. Under such conditions, 2 (or more) identical sets of chromosomes are available to pair up in meiosis, given that the 2 lineages are not too closely related. Autopoly-ploidy can occur when chromosomes fail to separate during meiosis. The resulting gametes will be diploid. If such a gamete fuses with a haploid one, the resulting in-dividual will be an autotriploid; 2 diploid gametes will give rise to an autotetraploid. Autopolyploids are often sterile since the regular formation of bivalents at meiosis is unlikely [Mntzing, 1951]. However, multivalent for-mation by itself is not a reliable criterion for identifying cases of autopolyploidy [Chenuil et al., 1999]. Soltis et al. [2010] point out that we do not know what are the most frequent mechanisms of polyploidization and which fac-tors favor the formation of allopolyploids versus auto-polyploids.

It is self-evident that triploids and other polyploids with odd or aneuploid numbers of chromosomes cannot undergo normal meiosis. Unless there is some specific mechanism guiding the process of segregation, the mul-tiple copies of each chromosome will orient randomly during the first meiotic division to give a random distri-bution of bivalents and univalents in the resulting germ cells (or even some multivalents). The consequences of the various possible modes of chromosome pairing in polyploids were deduced by Haldane [1930] and Jackson and Casey [1980]. Allopolyploids with an even number of chromosomes may undergo conventional meiosis by the formation of bivalents of homologous chromosomes, but even in such cases, the initial stages of polyploid forma-tion seem to be burdened with meiotic difficulties that often cause decreased fertility. This is thought to be allevi-ated through a movement of chromosome ends (telo-meres) that attach to proteins on the nuclear envelope. Homologous chromosomes then form clusters called bouquets. Structures called pairing centers mediate the pairing of homologues. The process is still very much a mystery [Tsai and McKee, 2011].

Federley [1913] conducted pioneering studies on hy-brid sterility in animals by examining the behavior of chromosomes in crosses between different species of

moths. While the hybrid females exhibited more or less complete pairing at meiosis, the males generally pro-duced univalents during the first metaphase. The chro-mosomes of lepidopterans are small and difficult to study. Nevertheless, interspecies hybridization takes place in the wild and allows the exchange of mimicry adaptation between species [The Heliconius Genome Consortium, 2012]. Federley also found that backcrosses between hy-brid females and males of the parental species generated triploid offspring [Federley, 1931] in which the 2 homol-ogous sets of chromosomes formed bivalents during mei-osis, with the third set of chromosomes remaining un-paired. Based on this finding, he predicted that if the ste-rility of the triploids could be overcome, it would be possible to obtain fertile tetraploids. Building on these results, Astaurov [1969] used heat shock to induce poly-ploidy. He succeeded first in producing autopolyploid silkworm moths (Bombyx mori) which were sterile. He then applied heat shock to hybrids between B . mori and its wild relative, B . mandarina to generate allotetraploid silkworm moths, B. allopolyploidus , which were fertile. His approach resembles the induction of polyploid plants in principle [Mntzing, 1980].

An obvious way to circumvent the problems of hybrid sterility is to abandon sex altogether. The incidence of polyploidy correlates strongly with apomixis in plants and parthenogenesis in animals. Apomixis is a catch-all term that covers all kinds of vegetative reproduction in plants, including the formation of seeds without the fu-sion of gamete nuclei [Gustafsson, 1944]. In many cases, plant embryos originate from somatic tissue rather than the embryo sac. In plant parthenogenesis, an unfertilized egg cell gives rise to an embryo [for details, see Grandont et al., 2013], and some modes of this process are analo-gous to events that occur during animal parthenogenesis. Thus, an unfertilized egg cell may give rise to a new indi-vidual so that a deviating mode of meiosis accompanies this process.

Haldane [1922] and Muller [1925] argued that the comparative rarity of polyploidy in animals relative to plants was due to the prevalence of chromosomal sex de-termination in animals. According to this argument, polyploidy disrupts the balance of sex chromosomes [Wertheim et al., 2013]. Parthenogenesis and polyploidy were therefore considered to be related phenomena. The demonstration by Beak et al. [1967] that frogs of the fam-ily Ceratophrydidae were polyploid and reproduced in the normal bisexual fashion came as a major surprise. This observation has been amply confirmed [Bogart, 1980; Gregory and Mable, 2005; Mable et al., 2011]. Beak

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et al. [1967] showed that in these frogs the telomeres ag-gregate on the nuclear envelope to form a telomere cluster or bouquet during early meiotic prophase. This structure facilitates the sorting of homologous chromosomes into pairs. Since then, as many as 50 polyploid anuran taxa have been described, including 7 triploids, 30 tetraploids, 11 octoploids, and two dodecaploids, derived from 15 an-uran families and 20 genera [Evans et al., 2012].

Figure 1 shows the different modes of meiosis deviat-ing from the normal course of events found in polyploid animals that reproduce through fertilization. True par-thenogenesis or clonal reproduction involves females only so that the males are absent. About all imaginable deviations from normal meiosis are observed in polyploid parthenogenetic animals ( figs. 26 ).

Gynogenesis is a phenomenon that occurs in both an-imals and plants, in which female gametes cannot develop without stimulation from a male gamete but produce progeny with the maternal genotype. The process can be leaky, and so fertilization occurs in some cases [DSouza and Michiels, 2009] with entire genomes or subgenomic amounts of paternal DNA contributing to the offspring (overview in vertebrates: Lamatsch and Stck [2009]).

This process is mostly referred to as gynogenesis (female birth) or sperm-dependent parthenogenesis [Beuke-boom and Vrijenhoek, 1998].

In hybridogenesis ( fig. 1 A), half of the maternal ge-nome of allodiploid hybrids is passed on to the next gen-eration intact while the other half (generally the paternal one) is discarded. Hybridogenetic females are fertilized by males of related species (often one of the ancestral spe-cies of the hybridogenetic hybrid form) that contribute the missing genome, which is discarded again in the next round of meiosis. Hybridogenesis can also give rise to polyploid forms that may reproduce through other means. As will be seen later, many vertebrate polyploids have their origins in hybridogenesis. Finally, in andro-genesis, an unreduced sperm enters the egg cytoplasm, but the maternal genome is discarded. Sperm nuclei of various origins can trigger this response, which occurs in some stick insects [Scali, 2009] and molluscs (Corbicula) [Hedtkea et al., 2011].

This review focuses on the process of meiosis and its variants in polyploid animals. We describe the different modes of meiosis separately and give examples of each. The extent of polyploidy in animals has been reviewed by

Kleptogenesis MeioticHybridogenesis

Pre-equalizingHybrid Meiosis

Hybridogenesis

A B C DOocyteSpermatocyte

Oocyte

Spermatocyte

Oocyte

Spermatocyte

Oocyte

Spermatocyte

Zygote Zygote Zygote Zygote

Meiosis Meiosis Meiosis Meiosis

Fig. 1. Deviations from the course of meiosis seen in polyploid animals that reproduce through fertilization. A Hybridogenesis: clonal eggs are fertilized by sperm from a diploid or triploid male that belongs to a different, often ancestral species. B Kleptogenesis: females acquire full or partial genomes from their partners. C Pre-equalizing hybrid meiosis: both sexes are triploid; Mendelian seg-

regation takes place in the 2 genomes at the right, while the genome at the left is clonally transmitted by the mother. Modified from Stck et al. [2012]. D Meiotic hybridogenesis: the ploidy of the off-spring is elevated through production of diploid gametes so that triploidy is restored. See figures 26 for different modes of meiosis in parthenogenetic animals.

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authors such as Gregory and Mable [2005], and the read-er is encouraged to consult their work for an exhaustive list of cases of polyploidy, ranging from anecdotal obser-vations to the cytologically well-established.

Meiosis in Polyploid Animals with Bisexual Reproduction

Bisexual Reproduction in Tetraploid, Hexaploid and Octoploid Frogs Saez and Brum [1960] found that the South American

frog Odontophrynus americanus had 42 chromosomes and the related Ceratophrys ornata has as many as 108. In a subsequent study, they discovered an Odontophrynus species with only 22 chromosomes [Saez and Brum-Zo-rilla, 1966]. They did not, however, attribute this varia-tion to polyploidy. Beak et al. [1966, 1967] demonstrated that the frogs were autopolyploid and, as mentioned in the introduction, described the formation of multivalents during meiosis in males as well as the mechanisms by which it was suppressed. Their findings were subsequent-ly confirmed by Bogart [1967]. Numerous diploid-poly-ploid species pairs have been found since then, and the list keeps growing [Bogart, 1980; Gregory and Mable, 2005; Mable et al., 2011]. Beak et al. [1967] observed bi-valents and multivalents during meiosis, and these obser-vations have been extended to several species and degrees of polyploidy [Bogart, 1980; Gregory and Mable, 2005]. Beak and Beak [1970] hybridized tetraploid O . ameri-canus with diploid O . cultripes to obtain triploid offspring with equal numbers of males and females. They suggested that mating such triploids might produce higher ploidy levels via a process that would represent an intermediate between auto- and allopolyploidization [Gregory and Mable, 2005; Schmid et al., 2010; Evans et al., 2012]. Pereyra et al. [2009] have shown that natural hybrids be-tween diploid Odontophrynus species have a disturbed meiosis with incomplete pairing between homoeologous chromosomes.

The North American species pair Hyla versicolor and H . chrysoscelis has also been studied extensively. Bogart and Wasserman [1972] and Bogart [1980] assumed that H. versicolor was an autotetraploid derivative of H . chrys-oscelis . Subsequent cytological observations clarified the multiple origins of the polyploid taxon and its relation-ships with other species [Gregory and Mable, 2005; Hol-loway et al., 2006], while ethological and ecological stud-ies have demonstrated that differences in their mating calls maintain separation between the taxa [Bogart, 1980;

Gregory and Mable, 2005; Mable et al., 2011]. Some cross-es involving H . versicolor produced sterile triploid, tetra-ploid and pentaploid offspring [Gregory and Mable, 2005].

Other diploid-polyploid frog taxa that have been stud-ied intensively are the Australian Neobatrachus and the African Xenopus , as discussed by Gregory and Mable [2005]. Xenopus laevis is a standard laboratory animal, and its biology is well-known. The females of Xenopus are heterozygous for sex factors (ZW) while the males are ho-mogametic (ZZ). Yoshimoto et al. [2010] confirmed fe-male heterogamety (ZW) by characterizing an ovary-de-termining gene (DM-W) on the W chromosome. Poly-ploidy weakens the effect of the female-determining factor, so that when both sex-determining factors are present at equal levels, environmental cues appear to de-termine the sex of individuals [Kobel and Du Pasquier, 1986; Gregory and Mable, 2005; but see Evans, 2008], but the details are unknown.

The twist-necked turtle (Platemys platycephala) repre-sents a rather unique case in that its natural populations contain diploids and triploids as well as diploid-triploid and triploid-tetraploid mosaics. All of these seem to re-produce sexually. The males produce haploid gametes ir-respective of their level of ploidy, and their meiosis is en-tirely normal. It thus appears that there is a pool of sper-matogonia and that only the diploid cells enter meiosis in males [Bickham et al., 1993]. While such phenomena ap-pear only explicable by some kind of hybrid (alloploid) origin, research examining the hybrid status is missing.

Hybridogenesis ( fig.1 A) Polyploidy is observed in 2 genera of the Poeciliidae

family of livebearing fishes: Poecilia , which is described in more detail in the sections discussing terminal fusion and apomictic parthenogenesis (see below), and Poeciliopsis . In both genera, hybridization generated diploid all-fe-male biotypes that in turn gave rise to triploid sperm-dependent parthenogenetic (= gynogenetic) forms. Poe-ciliopsis is found in northwestern Mexico and lives in the headwaters of rivers. These environments allow 2 species from this genus, P . monacha and P . lucida , to meet. Their hybridization produces an all-female taxon, P . lucida - mo-nacha [Schultz, 1980; Mable and Gregory, 2005; Lamatsch and Stck, 2009; Mable et al., 2011]. The permanent hy-brid genetic constitution of allodiploid P . monacha - luci-da is maintained through hybridogenesis. During the on-set of meiosis, one set of chromosomes (the P . monacha genome) aligns on the metaphase plate and is transported into a reconstituted nucleus by a unipolar spindle, while


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the P . lucida chromosomes are discarded. A single equa-tional division follows, giving rise to haploid eggs with only the maternal set of chromosomes, as inferred by Cimino [1972a, b] [see Schultz, 1980]. These eggs are then fertilized by the sperm of P . lucida . Other related species can form similar hybridogenetic strains with P . monacha in other river systems [Schultz, 1980; Gregory and Mable, 2005; Lamatsch and Stck, 2009]. Triploid forms in Poe-ciliopsis are entirely gynogenetic [Schultz, 1967] (see be-low), making these fishes potentially interesting models to study different forms of deviations from meiosis.

Polyploidy has been induced experimentally in am-phibians, frogs and salamanders in particular [Fischberg, 1958; Astaurov, 1969; Mable et al., 2011]. Conditions fa-voring triploidy have been described by authors includ-ing Humphries [1966]. However, autotriploidy is rare in natural populations. Lowcock and Licht [1990] surveyed an extensive body of data covering 15 species of the genus Ambystoma and identified only 8 autotriploids from 1,700 studied individuals.

Triploid North American all-female mole salaman-ders of the Ambystoma laterale - jeffersonianum com-plex [Bi and Bogart, this issue] were reported to repro-duce through premeiotic doubling involving gynogenesis [Cuellar, 1976]. Uzzell [1963, 1964] assigned these poly-ploids to A . platineum and A . tremblayi . However, Ses-sions [1982] later argued on the basis of cytological anal-ysis that these forms must have originated from a single female produced by hybridization between an A . laterale male and an A . jeffersonianum female. One or 2 matings of this hybrid with A . jeffersonianum males gave rise to the triploid A . platineum = A . 2 jeffersonianum - laterale , while mating between the hybrid female and A . laterale males produced triploid A . tremblayi = A . jeffersonia-num -2 laterale . In addition, there is at least 1 triploid all-female strain that is recreated in each generation due to hybridization between A . texanum and A . laterale [Bogart et al., 1987; Gregory and Mable, 2005].

According to Gregory and Mable [2005], there are no convincing reports of parthenogenesis in these salaman-ders. Triploid females must mate with males of the pro-genitor species [Bogart, 1980]. Following Cuellar [1976], they may undergo a premeiotic doubling associated with pseudogamy. This would necessitate the involvement of sperm to stimulate development but not to fertilize the egg. There is, however, an alternative scenario. Bogart and Licht [1986] studied a population of salamander lar-vae from Pelee Island on Lake Erie in which the mothers were diploid, triploid or tetraploid. All required sperm to develop. Diploid females produced diploid and triploid

larvae, while both triploid and tetraploid females pro-duced triploid and tetraploid offspring. A male genome is incorporated into the eggs and may be either reduced or unreduced, thereby ensuring that both triploid and tet-raploid individuals are produced regularly. Kelleys Is-land on Lake Erie is another natural laboratory for study-ing polyploidy in Ambystoma [Bogart et al., 1987]. In this population, an A . laterale genome is always present re-gardless of the ploidy of the individual. Genome replace-ment is common [Bi et al., 2008] (see the section on klep-togamy below). Diploid females produce both haploid and diploid eggs in a single egg mass. When these eggs are fertilized, they give rise to diploids and triploids (e.g. A . laterale texanum texanum ), respectively. Tetraploids were also observed, indicating that reductional division must occur during hybrid meiosis in some cases [Bogart et al., 1987]. Lowcock et al. [1991] sampled A . laterale populations from central Ontario and found that all pop-ulations contained diploid males and females as well as triploid and tetraploid hybrid females. One population contained triploid males, pentaploid females and possibly also polyploid A . laterale . The situation was summarized by Gregory and Mable [2005], who suggested that pseu-dogamy with premeiotic doubling [Cuellar, 1976] may prevail under cold conditions, but the mechanism pro-posed by Bogart and Licht [1986] predominates at higher temperatures. Studies on mitochondrial DNA suggest that Ambystoma are the oldest extant unisexual verte-brates [Bi and Bogart, 2010].

The central European water frogs Pelophylax esculen-tus (Rana esculenta) are the hybridogenetic offspring of P . lessonae (R. lessonae) and P . ridibundus (R. ridibunda) [reviewed by Vorburger et al., 2009; see also Bi and Bo-gart, this issue] . The molecular and cytological mecha-nisms responsible for hybridogenesis are poorly under-stood. In addition to water frogs, fishes such as Squalius alburnoides and the stick insects Bacillus reproduce through hybridogenesis (see below). However, unlike these 2 taxa, P . esculentus is bisexual and both sexes re-produce through hybridogenesis. The distributions of P . esculentus and P . lessonae overlap widely. In mixed mat-ings, P . esculentus discards the P . lessonae genome into the first polar body and transmits only the genome of P . ridibundus [Gnther et al., 1979]. The hybrids backcross in every generation with P . lessonae , making them sexual parasites of the latter species. Matings between hybrids would also produce P . ridibundus offspring, but these are not viable.

Gnther [1970] found triploids among P . esculentus . Meiosis in these frogs involves contacts between chromo-

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somes and formation of 3 paired chromosomes, which could permit recombination among non-sister chromo-somes [Gnther, 1975; Bogart, 1980]. Christiansen and Reyer [2009] have confirmed that diploid (LR) and trip-loid (LLR and LRR) P . esculentus have secondarily ac-quired a mode of sexual reproduction so that recombina-tion takes place but only between genomes of 1 parental species. The integrity of the parental genomes is suggest-ed to be maintained intact based on a limited sample size [Zalena et al., 2011], and further research would be desir-able.

In addition to the vertebrate cases described above, some Mediterranean stick insects of the genus Bacillus reproduce through hybridogenesis [Scali, 2009], although it should be noted that these insects have many other modes of reproduction. The hybridogens are believed to have arisen via hybridization involving B . rossius, B . gran-dii grandii and B . atticus atticus , in which B . rossius is al-ways the maternal parent and its genome is always passed on to the offspring [Scali, 2009]. B. atticus exhibits au-tomictic parthenogenesis (see below), whereas the trip-loid B . lynceorum is apomictic.

Kleptogenesis ( fig.1 B) Bogart et al. [2007] proposed that unisexual salaman-

ders of the genus Ambystoma exhibit a reproductive mode that had not previously been observed in eukary-otes. Ambystoma from the Great Lake region have nucle-ar genomes derived from 24 different species, but all have the mtDNA of A . barbouri . No particular genome is consistently inherited in its populations [Bi et al., 2008]. In other words, females acquire full or partial genomes from their partners. These unisexuals diverged from A . barbouri some 2.43.9 million years ago. Bogart et al. [2007] coined the name kleptogenesis (birth by theft) to describe this reproductive mode, which is believed to be unique to unisexual Ambystoma .

Pre-Equalizing Hybrid Meiosis ( fig.1 C) Stck et al. [2002] reported that Bufo baturae toads

from the high mountains of northern Pakistan are trip-loid but reproduce bisexually. As mentioned above, this finding was entirely unexpected. Both triploid males and females are fertile, and produce triploid offspring. Stck et al. [2012] showed that these toads reproduce via a nov-el mode, called pre-equalizing hybrid meiosis.

The allotriploid Batura toads (Bufo baturae) have 2 copies of a genome with a nucleolar organizing region (NOR+) on chromosome 6 and a third copy without this region (NOR). Males only produce haploid NOR+

sperm. The ova are diploid with 1 NOR+ and 1 NOR ge-nome, ensuring that the resulting offspring are also trip-loid (2 NOR+, NOR). Thus, in pre-equalizing hybrid meiosis, both sexes are triploid and show Mendelian seg-regation and recombination in the NOR+ genome, but the NOR genome is transmitted clonally by the female [Stck et al., 2012]. The male gametogenesis is thus simi-lar to gamete production according to meiotic hybrido-genesis.

Meiotic Hybridogenesis ( fig.1 D) The Squalius alburnoides complex, an Iberian cyprinid

complex [see also Collares-Perreira et al., this issue] pre-viously known as Leuciscus, Rutilus or Tropidophoxinel-lus, arose by hybridization involving females of Squalius pyrenaicus (P genome) and a species closely related to Anaecypris hispanica , which is responsible for its A ge-nome [Pala et al., 2009]. In general, each S . alburnoides individual has at least 1 A and 1 P genome. The complex consists of individuals of various ploidy levels that cross among themselves through diverse reproductive modes, ranging from parthenogenetic forms through normal meiosis to 2 kinds of hybridogenesis [Alves et al., 2001]. Diploid females may reproduce through parthenogenesis or hybridogenesis. Diploid males may produce either haploid or diploid sperm. A haploid egg of a triploid fe-male may be fertilized either by a haploid or diploid sperm. Triploid females may reproduce through a mech-anism that Alves et al. [2001] called meiotic hybridogen-esis. Triploids can be either males or females. These fe-males exclude the genome that is in minority. A subse-quent reductional meiosis produces either haploid eggs or a nonreductional meiosis produces diploid eggs. Fer-tile tetraploid males and females may originate from the fusion of diploid eggs and diploid sperm [Alves et al., 2001; Gregory and Mable, 2005; Lamatsch and Stck, 2009; Collares-Perreira et al., this issue].

Evolutionary Pathways. In addition to Squalius , sev-eral other fish genera (Cobitis , Misgurnus and Phoxinus) have mechanisms that exclude an entire chromosome set. This set is the one that is present as a single copy in a trip-loid. Normal meiosis ensues following this exclusion [La-matsch and Stck, 2009]. These authors speculate on a hypothetical scenario involving gynogenesis paternal leakage hybridogenesis meiotic hybridogenesis meiotic allotetraploidy. This process might be accompa-nied by an increase in the number of males, causing ini-tially all-female populations (such as those of Poecilia for-mosa ; see the section on apomictic parthenogenesis) to attain a more even sex balance, as observed for Squalius


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[Lamatsch and Stck, 2009]. Choleva et al. [2012] crossed 14 pairs of bisexual Cobitis spined loaches. The male off-spring were sterile and the females produced unreduced eggs. They obtained synthetic triploids by fertilizing the eggs of synthetic triploid females by haploid sperm. Some female offspring were identical to their mother. They had originated through gynogenesis. On the basis of these ex-periments, Choleva et al. [2012] argue that clonality and gynogenesis may be triggered by interspecies hybridiza-tion. Polyploidy is then a consequence rather than a cause of clonality.

Meiosis in Parthenogenetic Polyploid Animals

In parthenogenesis an egg cell develops into a new in-dividual without fertilization [Suomalainen et al., 1987]. Meiosis is the process that ensures genetic recombination in eukaryotes. Diploidy, meiosis and fertilization are in-tertwined phenomena whose origins evidently date back to an evolutionary period when an extra copy of the ge-nome was needed to protect against strongly mutagenic conditions [Long and Michod, 1995]. As a result, sexual reproduction has become predominant in animals and obviously strong selective pressures maintain it in the world of today.

The existence of paleopolyploid animals, such as ver-tebrates [Van de Peer and Meyer, 2005; Mable et al., 2011], demonstrates that polyploidy can persist in an evo-lutionary lineage. In contrast, parthenogenesis has arisen independently in many taxa. Almost without exception, they are single species (although this may reflect the hab-its of animal taxonomists; plant taxonomists would treat each apomictic lineage as a separate species) [Suomalai-nen et al., 1987]. Cases of polyploidy in association with parthenogenesis tend to accumulate within a group of species or family [Gregory and Mable, 2005; Mable et al., 2011]. However, the cytological basis of parthenogenesis will not necessarily be similar in related species [Suoma-lainen et al., 1987].

Parthenogenesis or thelytoky restricts or abolishes the potential for genetic recombination, which is essential for adaptation. Animals that are incapable of adapting to changes in their environment are arguably doomed to ex-tinction if major changes occur and would represent evo-lutionary dead ends [Matthey, 1941; White, 1970, 1973]. Nevertheless, the ones studied by Matthey and White are currently doing well: some have persisted for hundreds of millions of years, prompting Maynard Smith to label bdelloid rotifers evolutionary scandals [Schn et al.,

2009; see also Schwander et al., 2011], or at least tens of thousands of years [Stck et al., 2010]. Many modes of parthenogenesis allow the retention of new mutations and genetic variation. However, this is a tainted blessing since it causes deleterious mutations to accumulate in parthenogenetic lineages via a process called Mullers ratchet [Muller, 1964]. Polyploidization multiplies the space available for absorbing this mutational load [Lokki, 1976]. On the other hand, in the absence of genetic re-combination, polyploidy dilutes the effect of beneficial mutations [White, 1973].

If an egg cell develops into a new individual without fertilization, the chromosome number of the mother must be restored by some process that differs from the normal course of meiosis. Parthenogenetic polyploid an-imals are known to make use of the following modes of restoring ploidy levels:

Automictic (Meiotic) Parthenogenesis

In this mode, the early stages of meiosis proceed in the same way as in animals that require fertilization. The chromosomes pair at the zygotene phase of meiosis, cross over, and form bivalents. The reduction in chromosome number during meiosis generates haploid nuclei (n) with half the maternal chromosome number (2n in a diploid). In sexual reproduction, the fusion of the female gamete with the male one then forms a zygote with the chromo-some number 2n in a diploid animal. In automictic par-thenogenesis, 2 haploid nuclei with the chromosome number n fuse, a restitution nucleus may be formed, or there may be an endomitotic event prior to meiosis. All of these replace the fusion of a male and female nucleus by a fusion of 2 nuclei derived from the process of meiosis in the female animal. The evolutionary consequences of automixis are variable and range from the enforcement of complete homozygosity to the retention of the mothers heterozygosity.

The restoration of the chromosome number in the eggs of polyploid animals with automictic parthenogen-esis can occur in the following ways:

Gamete Duplication Here, the cleavage nuclei fuse or the halves of the di-

vided chromosomes of the cleavage nuclei remain in the same nucleus. Figure 2 shows the process of meiotic divi-sion as it occurs in a diploid animal such as the phyllopod crustacean Artemia parthenogenetica . The genus Artemia comprises 8 species that are often collectively called A.

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salina in the literature and which have diploid (2n = 42), triploid, tetraploid, pentaploid, octoploid, and decaploid races [Gross, 1932; Browne et al., 1984; Zhang et al., 1991]. Artom [1931] showed that the first meiotic division in diploid females at a population in Ste, southern France, proceeds in the normal fashion, eliminating 21 chromo-somes. There is no second polar body and the product of the first division divides endomitotically, generating nu-clei with 2n = 42 chromosomes. The tetraploids probably arose automitotically [Zhang et al., 1991] via a process like this. As shown in figure 2 , this mode of meiosis pro-duces homozygous offspring from a heterozygous female in a single generation. Crossing over will not change the outcome. Any alleles present in the mother will be distrib-uted among her offspring, and selection may operate on these genotypes. Parthenogenetic Artemia exploit several meiotic mechanisms, including apomictic parthenogen-esis [Barigozzi, 1974; Suomalainen et al., 1987]. At least most polyploid Artemia have apomictic parthenogenesis, but the cases with an even level of ploidy deserve to be studied in detail [e.g. Haas and Goldschmidt, 1946; Gold-schmidt, 1952].

Terminal Fusion This is a type of meiosis in which the second polar

nucleus fuses with the egg nucleus. Figure 3 shows the consequences of this mode of meiosis with and without crossing over. If a female is heterozygous A1A2 and there is no crossing over between the locus and centromere, half of her offspring will be A1A1 homozygotes and the other half A2A2 homozygotes. There will be variety among her offspring but they will all be homozygotes. Se-lection can act on this variation. If there is crossing over between the centromere and the locus, the offspring will retain the heterozygosity of the mother. Any absence of crossing over will lead to homozygosity. In systems of this kind, heterozygosity can be maintained by selection. Crossing over can occur at localized chiasmata or at loci far from the centromere in long chromosomes [Asher, 1970].

Christensen [1961] showed that the chromosome number of the mother is restored through an abortive second meiotic division in the polyploid enchytraeids (Annelida) Cognettia glandulosa, Fridericia ratzeli and Mesenchytraeus glandulosus . The chromosome number is halved during the first meiotic division and the first po-lar body is formed. The chromosomes of the product of the first division arrange themselves on a second meta-phase, but a functioning spindle is not formed and there is no second anaphase. The daughter chromosomes are

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Fig. 2. The genetic consequences of gamete duplication in a dip-loid. The mechanism enforces homozygosity irrespective of cross-ing over. Ootid = Polar body and oocyte; secondary oocyte = prod-uct of the first division.


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kept together for a while but then separate and become included in a single interphase nucleus. Even though there is no complete second meiotic division, the chro-mosome number is restored in a fashion analogous to the fusion between the second polar body and the female pro-nucleus.

Among the vertebrates, the poeciliid fish P. formosa makes use of this mechanism in its temporary mode of parthenogenesis. These fishes otherwise reproduce via apomictic parthenogenesis [Schultz, 1980].

Central Fusion This mode involves the fusion of the 2 central polar

nuclei. Figure 4 shows the consequences of this type of meiosis in diploids. If the mother is heterozygous A1A2, her offspring will also be A1A2 heterozgyotes if there is no crossing over. If there is crossing over between the lo-cus and the centromere, an A1A2 heterozygote will pro-duce the following offspring: 1/4 A1A1, 1/2 A1A2 and 1/4 A2A2. Obligate inbreeding will lead to a similar erosion of heterozygosity. Selection can operate on the resulting genotypes and affect their frequencies.

The bagworm moth Dahlica triquetrella can be regard-ed as a model here. Like all lepidopterans, D. triquetrella females exhibit achiasmate meiosis with no crossing over. D. triquetrella has a diploid sexual form but also diploid and tetraploid parthenogenetic forms. Seiler and Puchta [1956] crossed both diploid and tetraploid parthenogens with conspecific males as well as males of several related species. All interspecies crosses failed to produce fertile offspring. Because of the ZZ/ZW sex determination sys-tem of lepidopterans, triploid hybrids are generally inter-sex individuals. Seiler [1959] described how the 2 polar nuclei fuse in parthenogenetic females and give rise to an embryo. Most unfertilized sexual females do not lay eggs, but there are exceptions. Seiler [1961] showed that the cytological mechanism of parthenogenesis functions quite imperfectly in the early stages. The fitness of diploid sexual, diploid parthenogenetic and tetraploid partheno-genetic females was as follows: diploid parthenogens laid fewest eggs, followed by diploid sexuals, while tetraploid parthenogens laid more eggs than either. All of these dif-ferences were highly significant, although 1 diploid par-thenogenetic population was rather productive. Evident-ly Wolbachia endosymbionts are not involved in this pro-cess [Kumpulainen et al., 2004], but further studies are certainly needed.

Based on sampling multiple populations, Seiler [1961] also described the distribution of the 3 forms (races) in Switzerland. The diploid sexuals are mainly found in the

Alps. The diploid parthenogenetic form has spread fur-ther over lower areas, while the tetraploid parthenoge-netic race has spread over much of Europe. There are cer-tain areas where all three coexist. Seiler argues that the diploid sexual overwintered in refugia (ice-free areas) in the Alps during the Ice Age and started spreading from

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Fig. 3. The genetic consequences of terminal fusion. If there is no crossing over, a heterozygous female will produce individuals ho-mozygous for either allele. If there is crossing over between the centromere and the locus, heterozygosity can be maintained. Oo-tid = Polar body and oocyte; secondary oocyte = product of the first division.

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Fig. 4. The genetic consequences of central fusion. A heterozygous female will produce heterozygous offspring in the absence of cross-ing over. If there is crossing over, the heterozygote will produce 1/2 heterozygotes and 1/4 of each type of homozygotes in the first gen-eration. Ootid = Polar body and oocyte; secondary oocyte = prod-uct of the first division.


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Fig. 5. The genetic consequences of automixis involving the fusion of the 2 products of the first meiotic division. There will be 1/6 of each type of homozygotes and 4/6 of heterozygotes in the offspring of a heterozygous mother. Crossing over will not affect the out-come. Ootid = Polar body and oocyte; secondary oocyte = product of the first division.


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there. Its population density fell during its expansion, causing many females to remain unfertilized. They nev-ertheless attempted to lay eggs in some cases, occasion-ally with success. In such cases, the fusion of central polar nuclei would take over and give rise to an embryo; again in some diploid parthenogenetic populations, distur-bances in the cortical egg plasm gave rise to tetraploids. This would explain the polyphyletic origins of tetraploid populations; a conclusion confirmed by Lokki et al. [1975; Elzinga, pers. commun.]. Seiler [1964] described the tran-sition from diploidy to tetraploidy in detail.

Several sperm nuclei may be incorporated into Dahli-ca eggs. Seiler and Puchta [1956], Seiler and Schffer [1960] and Seiler [1963] studied the eventual contribu-tion of these extra nuclei in the origin of parthenogenesis and polyploidy in crosses between species and modes of reproduction within D . triquetrella in detail. They showed that this process, called polyspermy, was evidently not in-volved in the establishment of parthenogenesis or tetra-ploidy in D . triquetrella .

The First Polar Nucleus Fuses with the Nucleus of the Secondary Oocyte This kind of meiosis produces an egg and a polar body

( fig. 5 ). A diploid heterozygous female with genotype A1A2 is expected to give rise to offspring that consists of 1/6 A1A1 homozygotes, 4/6 A1A2 heterozygotes and 1/6 A2A2 homozygotes. Linkage will not affect this situation, but selection may operate on the resulting genotype fre-quencies.

This mechanism has been observed in triploid parthe-nogenetic females of the phasmid Bacillus atticus whose populations are genotypically diverse [Marescalchi and Scali, 2003; Scali, 2009]. B. atticus is distributed over an extensive area around the Mediterranean.

The tetraploid bagworm moth Dahlica (Solenobia) li-chenella also exhibits this type of meiosis [Narbel-Hof-stetter, 1950]. Narbel-Hofstetter was uncertain of the spe-cies identity of her subject and tentatively identified it as a parthenogenetic race of D . lichenella . Linnaeus had de-scribed Tinea lichenella as a parthenogenetic species in 1761, but there still seems to be confusion concerning the species identity of this taxon [Chevasco et al., 2012]. Ac-cording to Narbel-Hofstetter [1950], the chromosomes of D . lichenella pair at the first meiotic division, and biva-lents are formed at the first metaphase. The chromo-somes segregate at the first anaphase, but the daughter nuclei formed in this way fuse with each other, so that the second metaphase is made up of univalents only. These undergo the second meiotic division to produce the egg

nucleus and a polar body, each with the original tetra-ploid number of chromosomes. Such a process is not ex-pected to cause genetic erosion and, as shown by Che-vasco et al. [2012], the populations of D . lichenella (or the closely related tetraploid D . fennicella ) are genetically quite variable.

A Premeiotic Doubling of the Chromosome Number Is Reduced through Meiosis Figure 6 shows how this process operates in a diploid

female. The daughter chromosomes resulting from the premeiotic doubling pair at the first prophase. Crossing over is restricted to sister chromosomes, i.e. 2 identical copies of a chromosome as shown by Lutes et al. [2010] in Aspidoscelis lizards. All bivalents are homozygous for all their genes and multivalents are never formed. Conse-quently, the genetic constitution of the mother is passed unchanged to her offspring. Asher and Nace [1971] stud-ied the effects of mutation, segregation and selection on genetic variation in triploid populations of animals that reproduce using this kind of meiosis and showed that even small amounts of segregation will cause substantial losses of heterozygosity.

The tricladid flatworm Schmidtea (Dugesia) polychroa is pseudogamous and hermaphroditic. A parthenogeneti-cally developing egg must be triggered to develop by a sperm, but the sperm nucleus does not fuse and the male does not contribute to the developing embryo. Benazzi [1957] and Benazzi Lentati [1970] have described the pre-meiotic doubling in Schmidtea , which also exhibits apo-mictic parthenogenesis. Some worms are diploid and re-produce sexually but others are triploid or tetraploid pseu-dogamous parthenogens. Beukeboom et al. [1996] showed that sperm can occasionally fertilize the eggs, generating tri-, tetra- or pentaploid individuals. Individuals with all of these ploidies have been observed in nature, although pentaploids and tetraploids are rare. This suggests that they arise continuously via fertilization by chance.

DSouza et al. [2004] have shown that in addition to the modes described above, there is also a mechanism that decreases the degree of ploidy in Schmidtea . A tetraploid may produce a reduced, diploid egg that fuses with a sperm and produces a triploid offspring. A maternal chromosome set can also be expelled from the egg and replaced with a paternal set; a process that comes close to hybridogenesis. The resulting offspring will be a poly-ploid F1 hybrid with an unchanged degree of polyploidy. Accordingly, there may be a cycle involving triploids and tetraploids or sex without any change in ploidy level [DSouza and Michiels, 2009].

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Premeiotic doubling is the prevalent mode of meiosis in several large groups of polyploid parthenogenetic ani-mals such as the oligochaete families Lumbricidae and Tubificidae [Christensen, 1980b] as well as in vertebrates [Suomalainen et al., 1987; Gregory and Mable, 2005; Mable et al., 2011]. The oligochaetes are in general her-maphroditic. The meiosis of polyploid lumbricids is en-tirely regular so that only bivalents are formed at the first meiotic division [Omodeo, 1951a, b; Muldal, 1952]. Pre-meiotic doubling takes place in the testes of parthenoge-netic polyploids, but normal sperm is evidently not pro-duced [Christensen, 1980b].

Triploid Poeciliopsis (see the section on hybridogene-sis) have originated through a series of hybridizations. A

fish with a genetic constitution comprising 1 genome of P . monacha and 2 genomes of P . lucida called P . mona-cha -2 lucida has been observed. There are several kinds of triploids involving different doses of haploid sets de-rived from related species. All of these reproduce through premeiotic doubling [Cimino, 1972b] in conjunction with pseudogamy [Schultz, 1967, 1980].

Instances of polyploidy in reptiles have been reviewed by various authors [Bogart, 1980; Gregory and Mable, 2005; Kearney et al., 2009]. One case (Aspidoscelis lizards, formerly Cnemidophorus) that has been studied cytologi-cally reproduces through automictic parthenogenesis in-volving premeiotic doubling [Cuellar, 1971]. The whip-tail lizards (Aspidoscelis) of the southwestern USA and northern Mexico and from northern South America are the best-known group of parthenogenetic lizards [Bogart, 1980; Suomalainen et al., 1987; Gregory and Mable, 2005; Kearney et al., 2009], and are all of hybrid origin, with at least 8 species being triploid hybrids. Lutes et al. [2010] have observed the meiosis that follows the premeiotic du-plication of these lizards. The sister chromosomes pair, and synaptonemal complexes and chiasmata are seen. The triploidy of Aspidoscelis has originated from at least 2 rounds of hybridization, as summarized by Gregory and Mable [2005]. Lutes et al. [2011] have fertilized triploid oocytes of A . exsanguis with haploid sperm of A . inornata . The resulting tetraploid females were fertile. Moritz [1991] showed that the major parthenogenetic lineages of the Australian gekkonid lizard Heteronotia binoei have arisen recently and that its places of origin can be local-ized. Heteronotia has a very extensive distribution that covers most of Australia [Fujita and Moritz, 2009]. The triploid parthenogenetic Heteronotia binoei has originat-ed through reciprocal crosses involving 2 diploid bisexu-al lineages, which has resulted in 4 possible cytotypes [Roberts et al., 2012]. The twist-necked turtle (Platemys polycephala) is apparently not a true polyploid but a mo-saic, despite often being grouped with polyploids that re-produce sexually [Bickham et al., 1993].

A Mixed Case of Parthenogenesis Christensen [1980b] describes the restoration of the

chromosome number in the polyploid and parthenoge-netic enchytraeid Fridericia galba . Some chromosomes form bivalents and undergo meiosis, while some others apparently follow a mitotic pattern.

The enchytraeid Lumbricillus lineatus has parthenoge-netic tri-, tetra- and pentaploid forms [Christensen, 1960, 1980a, b]. Its meiosis is asynaptic and the undivided uni-valents move in approximately equal numbers towards

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the poles, where they are arrested at mid-anaphase. Divi-sion is initiated when the eggs are laid. The spindle elon-gates, the chromosomes move further apart and the spin-dle becomes V-shaped, with the apex of the V oriented towards the egg membrane. Anaphase is then arrested again and the chromosomes of the 2 nuclei form 2 second metaphase plates. The chromosomes divide equationally and move along the continuous spindle in the second anaphase. Two complements from each of the daughter nuclei from the first division move towards the apex of the V, while the other 2 move towards its arms. The re-sulting 4 chromosome groups fuse two-by-two and form 2 nuclei, each of which has a full set of chromosomes. A polar body is then extruded. The process of reproduction in L . lineatus thus has characteristics of both automictic and apomictic parthenogenesis but does not quite fit in either category.

A population may reproduce via a mixture of terminal and central fusion [Asher, 1970]. In such cases, contract-ing effects eliminate the influence of linkage on the gain of homozygosity and equilibrium heterozygosity values. Any new mutants that arise readily become fixed in the parthenogenetic lineage [Suomalainen et al., 1987].

Apomictic (Ameiotic) Parthenogenesis

Here, meiosis is replaced with what is essentially a mi-totic cell division. A similar mechanism operates in the major mode of parthenogenesis in plants. Apomictic par-thenogenesis has originated independently in many poly-ploid animals. Two evolutionary scenarios can be invoked to explain this. First, there may have been an intermediate diploid parthenogenetic stage that became polyploid. Al-ternatively, polyploidy may have arisen first (as occurs in species hybrids). Hybrids of this kind are not expected to produce functional gametes through meiosis, but they may be rescued from sterility by parthenogenesis. The question is whether there is an initial automictic stage that is later replaced by (at least in principle) more derived apomictic parthenogenesis. White [1973] argued that apomictic parthenogenesis must originate in a single-step process (or macromutation) since thelytokous genetic mechanisms are too rigid and inflexible to be capable of the delicate evolutionary transformation from automixis to apomixis, which would necessarily involve a great many mutational steps if the new mechanism was to be efficient.

We shall here review the mechanism of oogenesis in cytologically verified cases of apomictic parthenogenesis in polyploid animals.

The earthworm Dendrobaena octaedra has been re-ported by Omodeo [1955] and Casellato and Rodighiero [1972] to reproduce through apomixis. All other parthe-nogenetic and polyploid lumbricids exhibit automixis with premeiotic doubling [Omodeo, 1951a, b; Christen-sen, 1980b].

In D . octaedra , the chromosome number is not dou-bled and the chromosome number is not reduced in the oocytes, which undergo just 1 round of a single matura-tion division. The parthenogenetic strains are generally hexaploid [Christensen, 1980b; Suomalainen et al., 1987; Hongell and Terhivuo, 1989]. D . octaedra is the most common earthworm in northern Europe. It lives in forest habitats and is important in the breakdown of litter. In other parts of the world, it is a harmful invasive species [Hendrix, 2006; Simonsen and Holmstrup, 2008], and so its study is not just of academic interest. Terhivuo and Saura [1990] found that the extent of genotypic variation in D . octaedra exceeded that seen in other polyploid and parthenogenetic earthworms. Hongell and Terhivuo [1989] showed that only univalents were observed during oogenesis, a finding that was incompatible with a subse-quent premeiotic doubling and confirmed earlier reports of apomictic parthenogenesis in this species [Omodeo, 1955; Casellato and Rodighiero, 1972]. Simonsen and Holmstrup [2008] proved through a set of rearing exper-iments that the offspring of individual worms exhibited genetic variation, which is consistent with the results of Terhivuo and Saura [1990]. The oogenesis of D . octaedra thus merits more extensive study.

Water fleas (Daphnia) have been reported to repro-duce via cyclical parthenogenesis, with parthenogenetic females exhibiting apomictic parthenogenesis [Suoma-lainen et al., 1987]. Hiruta et al. [2010] and Hiruta and Tochinai [2012] have, however, shown evidence of an abortive first meiotic division followed by formation of a polar body in Daphnia pulex so that additional studies are clearly needed. There are, in addition, polyploids that re-produce via obligate parthenogenesis [Beaton and He-bert, 1988; Decaestecker et al., 2009].

Grasshoppers have large chromosomes. Consequently they have contributed much to our understanding of the processes of meiosis and parthenogenesis [White, 1973]. Certain diploid tettigids reproduce occasionally through terminal fusion [e.g. Nabours, 1937], while the diploid grasshopper Warramaba virgo has premeiotic doubling [e.g. White, 1980]. The wingless grasshopper Saga pedo is tetraploid and reproduces through apomictic partheno-genesis [Matthey, 1941].

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Coleoptera represent the largest order of animals. As expected, they have several parthenogenetic and poly-ploid forms. Most of these are weevils (Curculionidae), the largest beetle family. A total of 75 parthenogenetic weevil taxa have been described to date [Saura et al., 1993]. All of these as far as examined exhibit apomic-tic parthenogenesis, and almost all are polyploid. There are 4 diploid, 43 triploid, 18 tetraploid, 6 pentaploid, 3 hexaploid and 1 decaploid taxa, commonly designated as races. They belong to 52 morphological species from 24 genera [Suomalainen et al., 1987]. Parthenogenesis has apparently originated independently within each of these biological species [Suomalainen et al., 1987; Stenberg et al., 2003]. In each species, the direction of evolution is to-wards higher degrees of polyploidy. When there are sev-eral polyploid races (for instance triploid and tetraploid), the tetraploids generally have a wider distribution than the triploids. Patterns of this kind have been described as geographical parthenogenesis by Stenberg et al. [2003] and are observed in other groups of parthenogenetic and polyploid animals [Seiler, 1961; Suomalainen et al., 1987].

Suomalainen [1940] repeatedly observed 2 or more metaphase plates with the haploid chromosome number during the oogenesis of polyploid parthenogenetic wee-

vils ( fig.7 ). An egg from a tetraploid female of e.g. Otio-rhynchus dubius could have plates consisting of 33 and 11 chromosomes. Others might have 2 plates with 22 chro-mosomes, while others still would have 22, 11 and 11 chromosomes. Finally, an egg may have 4 plates with 11 chromosomes each. He named this phenomenon go-nomery and argued that the level of polyploidy had in-creased via an additive process involving allopolyploidy. That is to say, a diploid parthenogenetic female would have been fertilized by a diploid male to produce a par-thenogenetic triploid that could have gone on to produce a tetraploid in the same way, etc. The origin of partheno-genesis may have involved a diploid automictic stage that would in turn have evolved into apomixis and polyploidy.

Seiler [1947] observed that in triploid Otiorhynchus sulcatus , the spindle can be multipolar during the pro-phase of oogenesis. The chromosomes do not pair during prophase; instead, once they have oriented themselves on the metaphase plate, they scatter across the entire spindle. This is followed by a rudimentary meiosis, but the now-separate chromosomes align themselves again pairwise to form a metaphase plate and undergo what is effectively a mitotic division. The vestiges of meiosis observed by Seiler [1947] were later interpreted to be a consequence of the gonomery (multiple plate) hypothesis of Suoma-lainen [Saura et al., 1993].

Saura et al. [1993] argued that triploidy and partheno-genesis must have originated simultaneously, e.g. in a species hybrid. Triploidy is, by far, the most common de-gree of ploidy in weevils. Given the rarity of parthenoge-netic diploids, they are probably derived from triploids via a shuffling of the haploid metaphase plates. New de-grees of ploidy may be added via the same mechanism or through chance fertilizations by diploid males. The geo-graphical distributions of different degrees of polyploidy in weevils support the view that triploid parthenogenesis was the first to arise, and that it originated separately in each species. It was then followed by higher degrees of polyploidy with rare transitions to diploidy. The diploid parthenogens have a wider distribution than triploids [Lokki et al., 1976], which may indicate that the diploids represent the derived form in this case.

One might suggest that diploid parthenogens could be common but not readily distinguished from diploid sexu-al females. The genitalia of diploid sexual weevils and their diploid or polyploid parthenogenetic counterparts are es-sentially similar [Szkessy, 1937]. Absence or relative rar-ity of males is therefore a useful first indicator of potential parthenogenesis in a population for an entomologist studying its extent. However, in cases where there is a

Fig. 7. Gonomery or genome segregation in the apomictic oogen-esis of tetraploid eggs of Otiorhynchus dubius . Upper left: a meta-phase plate with 44 chromosomes; upper right: a metaphase plate with a separate haploid and triploid plate; lower left: 2 diploid plates, the rest: 1 diploid plate and 2 haploid plates. From Suoma-lainen [1940], with permission.


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skewed sex ratio due to the presence of parthenogenetic females, they are usually triploid or have a higher degree of polyploidy. It thus seems that the frequency of diploid parthenogens has not been severely underestimated. Stenberg and Lundmark [2004] and Hirsch et al. [2012] showed that even though some of these weevils harbor Wolbachia endosymbionts, they are unlikely to explain the transition to parthenogenesis or to polyploidy.

In addition to curculionids, certain chrysomelids are polyploid parthenogens that reproduce through apomic-tic parthenogenesis. Bromius (Adoxus) obscurus is trip-loid in Europe [Suomalainen, 1965]. The diploid sexuals live in North America and feed on quite different plants, i.e. alder (Alnus) and grapevine (Vitis) while the Euro-pean triploids feed on fireweed (Chamaenerion) . For a review of parthenogenesis in beetles, see Suomalainen et al. [1987].

Poecilia formosa , the Amazon molly, does not live in the Amazon River, but its name refers to is almost all-female populations. These fish live in disjunct popula-tions in northeastern Mexico and adjacent areas of Texas [Schultz, 1980]. They originated via hybridization involv-ing female P . mexicana and male P . latipinna [Schultz, 1980; Sola et al., 1992], probably derived from single or very few individuals that lived some 120,000280,000 years ago [Avise et al., 1991; Schartl, 1995b; Stck et al., 2010]. Triploids were first observed in the laboratory, but they are fairly common in nature and possibly of mono-phyletic origin [Lampert et al., 2005]. They produce via-ble female offspring through apomictic parthenogenesis involving pseudogamy [Schultz, 1980]. Crosses of P . mex-icana limantouri with P. latipinna , i . e . the cross that gave rise to P. formosa, exhibits automictic oocyte production through a random fusion of products of the second mei-otic division. When diploid oocytes from such laboratory crosses were fertilized, however, they gave rise to viable triploid offspring but did not generate diploid gynoge-netic lineages [Lampert et al., 2007a; Stck et al., 2010].

According to a rather speculative review by Schultz [1980], 2 modes of meiosis are associated with pseudog-amy in diploid Poecilia . One is temporary and autodip-loid, which has never been empirically found, it seems, while the other is permanent and allodiploid. In the first case, a failure of synapsis causes a doubling of the mater-nal set of chromosomes by suppressing the second mei-otic division, allowing the second polar body to fuse with the egg cell (automixis involving terminal fusion). In the second case, the first division is suppressed [Schultz, 1980]. As stated in the relevant section above, the related genus Poeciliopsis exhibits premeiotic doubling.

Several related species act as sperm donors for P . for-mosa , and this function may also be fulfilled by rare trip-loid males, though this has not been empirically demon-strated [Lamatsch et al., 2010]. Such males would not contribute to the genetic constitution of the offspring [Gregory and Mable, 2005] but have been shown to arise through gynogenesis with leakage, i.e. the incorporation of subgenomic amounts of DNA plus complete chromo-some sets [Schartl et al., 1995a; Lamatsch et al., 2010], when a sperm encounters and fertilizes an egg that would normally only require contact with a sperm to commence development. P. formosa triploids have 1 set of P . latipin-na chromosomes and 2 from P . mexicana or vice-versa. Following Schultz [1980], they should be called P . 2 mex-icana - latipinna or P . mexicana -2 latipinna to indicate the identity of their genomes. P . formosa may also rarely ex-hibit mosaicism so that somatic tissues of an individual contain haploid, diploid and triploid cells [Lampert et al., 2007b].

Comparing Polyploidy in Sexually and Parthenogenetically Reproducing Animals

Lundmark [2006] pointed out that parthenogenetic animals can be polyploid, of hybrid origin or both, and that both of these phenomena are often proposed to ex-plain the geographical success of parthenogens better than parthenogenesis itself. However, they are hard to disentangle. Lundmark and Saura [2006] reviewed the lit-erature on parthenogenesis, geographical distribution and polyploidy in arthropods and concluded that poly-ploidy is the factor that is most likely to explain the suc-cess of asexual arthropods. Mable et al. [2011] reviewed the occurrence of polyploidy in amphibians and fish. These 2 groups both have numerous available modes of reproduction, as discussed above. Although true parthe-nogenesis and perhaps even gynogenesis appear to be ab-sent in amphibians, these authors were unable to identify conclusive evidence indicating that any specific factor was driving polyploidy.

Earthworms may be regarded as another test case. All of them are hermaphrodites, and the parthenogens retain male structures to a variable extent [Christensen, 1980b]. About 40% of Palearctic earthworms are polyploid [Ca-sellato, 1987]. They lack sex chromosomes altogether; i.e. the factors that are considered to represent the major ob-stacles to the formation of polyploidy in animals [Muller, 1925; Mable, 2004; Wertheim et al., this issue]. The poly-ploids are generally parthenogens, but there are poly-

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ploids with an even degree of polyploidy that undergo sexual reproduction as well. The sexual forms of Eisenia nordenskioldi have even ploidy levels ranging from dip-loid through octoploid. The only parthenogenetic form is septaploid [Viktorov, 1997]. In this taxon, ploidy levels correlate positively with geographic distribution, irre-spective of the mode of reproduction [Grafodatsky et al., 1982; Perel and Grafodatsky, 1983; Viktorov, 1997]. It

therefore seems that polyploidy rather than partheno-genesis is responsible for the variation in the success of these forms [Lundmark and Saura, 2006]. The role of polyploidy in the evolution of animals remains to be de-termined, but it should be always considered as a poten-tially occurring factor in surveys of animal distribution, reproduction and evolution.

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