Meiosis and Its Deviations in Polyploid

Meiosis and Its Deviations in Polyploid
Cytogenet Genome Res 2013;140:185203

DOI: 10.1159/000351731
Published online: June 18, 2013
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
Key Words
Gynogenesis Hybridogenesis Kleptogenesis
Parthenogenesis
parthenogenesis, meiosis is replaced by what is effectively

mitotic cell division. The above modes have different evolutionary consequences, which are discussed. See also the sister article by Grandont et al. in this themed issue.
Copyright 2013 S. Karger AG, Basel
Abstract
We review the different modes of meiosis and its deviations
encountered in polyploid animals. Bisexual reproduction involving normal meiosis occurs in some allopolyploid frogs
with variable degrees of polyploidy. Aberrant modes of bisexual 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 haploid sperm in meiotic hybridogenesis, which elevates the
ploidy of hybrid offspring such that they produce diploid
gametes. Polyploids are then produced in the next generation. In kleptogenesis, females acquire full or partial genomes 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 maintaining the mothers ploidy level, including gamete duplication, terminal fusion, central fusion, fusion of the first polar
nucleus with the product of the first division, and premeiotic duplication followed by a normal meiosis. In apomictic
2013 S. Karger AG, Basel

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Polyploid plants are ecologically and economically important [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 generally match the sophistication and power seen in the analyses of factors both at the genetic and molecular level that
operate in polyploid plants [Grandont et al., 2013]. A significant fraction of the existing literature on the modes of
meiosis in polyploid animals is old and written in languages other than English. However, it is important to
acknowledge the importance of polyploidy in the evolution of animals: 2 rounds of historical polyploidization
Anssi Saura
Department of Molecular Biology
Ume University
SE901 87 Ume (Sweden)
E-Mail Anssi.Saura@molbiol.umu.se
(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 polyploidy 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 lineages. 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. Autopolyploidy 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 individual 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 formation 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 factors favor the formation of allopolyploids versus autopolyploids.
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 multiple copies of each chromosome will orient randomly
during the first meiotic division to give a random distribution 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 formation seem to be burdened with meiotic difficulties that
often cause decreased fertility. This is thought to be alleviated through a movement of chromosome ends (telomeres) 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 hybrid sterility in animals by examining the behavior of
chromosomes in crosses between different species of
186

DOI: 10.1159/000351731
moths. While the hybrid females exhibited more or less

complete pairing at meiosis, the males generally produced univalents during the first metaphase. The chromosomes 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 hybrid females and males of the parental species generated
triploid offspring [Federley, 1931] in which the 2 homologous sets of chromosomes formed bivalents during meiosis, with the third set of chromosomes remaining unpaired. Based on this finding, he predicted that if the sterility 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 polyploidy. 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 fusion 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 analogous to events that occur during animal parthenogenesis.
Thus, an unfertilized egg cell may give rise to a new individual 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 determination 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 family 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
Stenberg /Saura
Oocyte
A
Spermatocyte
Meiosis
Zygote
Hybridogenesis
Oocyte
Oocyte
Spermatocyte
Meiosis
C
Spermatocyte
Meiosis
Zygote
Zygote
Kleptogenesis
Pre-equalizing
Hybrid Meiosis
Oocyte
D
Spermatocyte
Meiosis
Zygote
Meiotic
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 Preequalizing 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 offspring is elevated through production of diploid gametes so that
triploidy is restored. See figures 26 for different modes of meiosis
in parthenogenetic animals.
et al. [1967] showed that in these frogs the telomeres aggregate 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 anuran families and 20 genera [Evans et al., 2012].
Figure 1 shows the different modes of meiosis deviating from the normal course of events found in polyploid
animals that reproduce through fertilization. True parthenogenesis 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 animals 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 [Beukeboom and Vrijenhoek, 1998].
In hybridogenesis (fig. 1A), half of the maternal genome of allodiploid hybrids is passed on to the next generation 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 species 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 androgenesis, 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
Meiosis in Polyploid Animals

DOI: 10.1159/000351731
Fig. 1. Deviations from the course of meiosis seen in polyploid

animals that reproduce through fertilization. A Hybridogenesis:
187
authors such as Gregory and Mable [2005], and the reader is encouraged to consult their work for an exhaustive
list of cases of polyploidy, ranging from anecdotal observations 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-Zorilla, 1966]. They did not, however, attribute this variation 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 subsequently confirmed by Bogart [1967]. Numerous diploid-polyploid 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 bivalents and multivalents during meiosis, and these observations have been extended to several species and degrees
of polyploidy [Bogart, 1980; Gregory and Mable, 2005].
Beak and Beak [1970] hybridized tetraploid O. americanus 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 between 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. chrysoscelis. Subsequent cytological observations clarified the
multiple origins of the polyploid taxon and its relationships with other species [Gregory and Mable, 2005; Holloway et al., 2006], while ethological and ecological studies have demonstrated that differences in their mating
calls maintain separation between the taxa [Bogart, 1980;
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DOI: 10.1159/000351731
Gregory and Mable, 2005; Mable et al., 2011]. Some crosses involving H. versicolor produced sterile triploid, tetraploid and pentaploid offspring [Gregory and Mable,
2005].
Other diploid-polyploid frog taxa that have been studied 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 homogametic (ZZ). Yoshimoto et al. [2010] confirmed female heterogamety (ZW) by characterizing an ovary-determining gene (DM-W) on the W chromosome. Polyploidy weakens the effect of the female-determining
factor, so that when both sex-determining factors are
present at equal levels, environmental cues appear to determine 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) represents 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 reproduce sexually. The males produce haploid gametes irrespective of their level of ploidy, and their meiosis is entirely normal. It thus appears that there is a pool of spermatogonia and that only the diploid cells enter meiosis in
males [Bickham et al., 1993]. While such phenomena appear only explicable by some kind of hybrid (alloploid)
origin, research examining the hybrid status is missing.
Hybridogenesis (fig.1A)
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-female biotypes that in turn gave rise to triploid spermdependent parthenogenetic (= gynogenetic) forms. Poeciliopsis 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-monacha [Schultz, 1980; Mable and Gregory, 2005; Lamatsch
and Stck, 2009; Mable et al., 2011]. The permanent hybrid genetic constitution of allodiploid P. monacha-lucida is maintained through hybridogenesis. During the onset 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
Stenberg /Saura
the P. lucida chromosomes are discarded. A single equational 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 Poeciliopsis are entirely gynogenetic [Schultz, 1967] (see below), making these fishes potentially interesting models
to study different forms of deviations from meiosis.
Polyploidy has been induced experimentally in amphibians, frogs and salamanders in particular [Fischberg,
1958; Astaurov, 1969; Mable et al., 2011]. Conditions favoring triploidy have been described by authors including 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 salamanders of the Ambystoma laterale-jeffersonianum complex [Bi and Bogart, this issue] were reported to reproduce through premeiotic doubling involving gynogenesis
[Cuellar, 1976]. Uzzell [1963, 1964] assigned these polyploids to A. platineum and A. tremblayi. However, Sessions [1982] later argued on the basis of cytological analysis 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. jeffersonianum-2 laterale. In addition, there is at least 1 triploid allfemale 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 salamanders. Triploid females must mate with males of the progenitor 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 larvae 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 produced 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 tetraploid individuals are produced regularly. Kelleys Island on Lake Erie is another natural laboratory for studying polyploidy in Ambystoma [Bogart et al., 1987]. In this
population, an A. laterale genome is always present regardless of the ploidy of the individual. Genome replacement is common [Bi et al., 2008] (see the section on kleptogamy 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 populations 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 pseudogamy with premeiotic doubling [Cuellar, 1976] may
prevail under cold conditions, but the mechanism proposed by Bogart and Licht [1986] predominates at higher
temperatures. Studies on mitochondrial DNA suggest
that Ambystoma are the oldest extant unisexual vertebrates [Bi and Bogart, 2010].
The central European water frogs Pelophylax esculentus (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 Bogart, this issue]. The molecular and cytological mechanisms responsible for hybridogenesis are poorly understood. 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 reproduce through hybridogenesis. The distributions of P.
esculentus and P. lessonae overlap widely. In mixed matings, 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-

DOI: 10.1159/000351731
189
somes and formation of 3 paired chromosomes, which

could permit recombination among non-sister chromosomes [Gnther, 1975; Bogart, 1980]. Christiansen and
Reyer [2009] have confirmed that diploid (LR) and triploid (LLR and LRR) P. esculentus have secondarily acquired a mode of sexual reproduction so that recombination takes place but only between genomes of 1 parental
species. The integrity of the parental genomes is suggested to be maintained intact based on a limited sample size
[Zalena et al., 2011], and further research would be desirable.
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. grandii grandii and B. atticus atticus, in which B. rossius is always the maternal parent and its genome is always passed
on to the offspring [Scali, 2009]. B. atticus exhibits automictic parthenogenesis (see below), whereas the triploid B. lynceorum is apomictic.
Kleptogenesis (fig.1B)
Bogart et al. [2007] proposed that unisexual salamanders of the genus Ambystoma exhibit a reproductive
mode that had not previously been observed in eukaryotes. Ambystoma from the Great Lake region have nuclear 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.1C)
Stck et al. [2002] reported that Bufo baturae toads
from the high mountains of northern Pakistan are triploid 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 novel 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+
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DOI: 10.1159/000351731
sperm. The ova are diploid with 1 NOR+ and 1 NOR genome, ensuring that the resulting offspring are also triploid (2 NOR+, NOR). Thus, in pre-equalizing hybrid
meiosis, both sexes are triploid and show Mendelian segregation 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 similar to gamete production according to meiotic hybridogenesis.
Meiotic Hybridogenesis (fig.1D)
The Squalius alburnoides complex, an Iberian cyprinid
complex [see also Collares-Perreira et al., this issue] previously known as Leuciscus, Rutilus or Tropidophoxinellus, arose by hybridization involving females of Squalius
pyrenaicus (P genome) and a species closely related to
Anaecypris hispanica, which is responsible for its A genome [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 female may be fertilized either by a haploid or diploid
sperm. Triploid females may reproduce through a mechanism that Alves et al. [2001] called meiotic hybridogenesis. Triploids can be either males or females. These females exclude the genome that is in minority. A subsequent reductional meiosis produces either haploid eggs
or a nonreductional meiosis produces diploid eggs. Fertile 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, several 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 triploid. Normal meiosis ensues following this exclusion [Lamatsch and Stck, 2009]. These authors speculate on a
hypothetical scenario involving gynogenesis paternal
leakage hybridogenesis meiotic hybridogenesis
meiotic allotetraploidy. This process might be accompanied by an increase in the number of males, causing initially all-female populations (such as those of Poecilia formosa; see the section on apomictic parthenogenesis) to
attain a more even sex balance, as observed for Squalius
Stenberg /Saura
[Lamatsch and Stck, 2009]. Choleva et al. [2012] crossed

14 pairs of bisexual Cobitis spined loaches. The male offspring 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 experiments, Choleva et al. [2012] argue that clonality and
gynogenesis may be triggered by interspecies hybridization. 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 individual without fertilization [Suomalainen et al., 1987].
Meiosis is the process that ensures genetic recombination
in eukaryotes. Diploidy, meiosis and fertilization are intertwined phenomena whose origins evidently date back
to an evolutionary period when an extra copy of the genome 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 vertebrates [Van de Peer and Meyer, 2005; Mable et al.,
2011], demonstrates that polyploidy can persist in an evolutionary lineage. In contrast, parthenogenesis has arisen
independently in many taxa. Almost without exception,
they are single species (although this may reflect the habits of animal taxonomists; plant taxonomists would treat
each apomictic lineage as a separate species) [Suomalainen 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 [Suomalainen 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 extinction if major changes occur and would represent evolutionary 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 recombination, 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 animals 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 chromosome number 2n in a diploid animal. In automictic parthenogenesis, 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 parthenogenesis can occur in the following ways:
Gamete Duplication
Here, the cleavage nuclei fuse or the halves of the divided chromosomes of the cleavage nuclei remain in the
same nucleus. Figure 2 shows the process of meiotic division 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.
DOI: 10.1159/000351731
191
secondary oocyte
primary oocyte
ootid
secondary oocyte
cleavage nuclei
ootid
ootid
ootid
cleavage nuclei
diploid
Gamete duplication
Without crossing over
ootid
cleavage nuclei
diploid
cleavage nuclei
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
With crossing over
Fig. 2. The genetic consequences of gamete duplication in a diploid. The mechanism enforces homozygosity irrespective of crossing over. Ootid = Polar body and oocyte; secondary oocyte = product of the first division.
192

DOI: 10.1159/000351731
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 chromosomes. There is no second polar body and the product of
the first division divides endomitotically, generating nuclei 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 produces 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 distributed among her offspring, and selection may operate on
these genotypes. Parthenogenetic Artemia exploit several
meiotic mechanisms, including apomictic parthenogenesis [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; Goldschmidt, 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. Selection 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 polar body is formed. The chromosomes of the product of
the first division arrange themselves on a second metaphase, but a functioning spindle is not formed and there
is no second anaphase. The daughter chromosomes are
Stenberg /Saura
secondary oocyte
ootid
secondary oocyte
ootid
ootid
ootid
diploid
Terminal fusion
ootid
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
With crossing over
diploid
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 locus and the centromere, an A1A2 heterozygote will produce 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 regarded 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 system of lepidopterans, triploid hybrids are generally intersex 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 parthenogenetic females was as follows: diploid parthenogens laid
fewest eggs, followed by diploid sexuals, while tetraploid
parthenogens laid more eggs than either. All of these differences were highly significant, although 1 diploid parthenogenetic population was rather productive. Evidently Wolbachia endosymbionts are not involved in this process [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
primary oocyte
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 chromosome number is restored in a fashion analogous to the
fusion between the second polar body and the female pronucleus.
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].
Fig. 3. The genetic consequences of terminal fusion. If there is no
crossing over, a heterozygous female will produce individuals homozygous for either allele. If there is crossing over between the
centromere and the locus, heterozygosity can be maintained. Ootid = Polar body and oocyte; secondary oocyte = product of the first
division.
Alps. The diploid parthenogenetic form has spread further over lower areas, while the tetraploid parthenogenetic race has spread over much of Europe. There are certain 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
DOI: 10.1159/000351731
193
secondary oocyte
ootid
secondary oocyte
secondary oocyte
primary oocyte
primary oocyte
secondary oocyte
polar body
diploid
diploid
ootid
ootid
ootid
Central fusion
Secondary oocyte fusion

With crossing over
194
secondary oocyte
secondary oocyte
Fig. 4. The genetic consequences of central fusion. A heterozygous

female will produce heterozygous offspring in the absence of crossing over. If there is crossing over, the heterozygote will produce 1/2
heterozygotes and 1/4 of each type of homozygotes in the first generation. Ootid = Polar body and oocyte; secondary oocyte = product of the first division.

DOI: 10.1159/000351731
polar body
diploid
diploid
ootid
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
primary oocyte
With crossing over
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 outcome. Ootid = Polar body and oocyte; secondary oocyte = product
of the first division.
Stenberg /Saura
there. Its population density fell during its expansion,

causing many females to remain unfertilized. They nevertheless attempted to lay eggs in some cases, occasionally 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, disturbances 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 transition from diploidy to tetraploidy in detail.
Several sperm nuclei may be incorporated into Dahlica eggs. Seiler and Puchta [1956], Seiler and Schffer
[1960] and Seiler [1963] studied the eventual contribution 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 involved in the establishment of parthenogenesis or tetraploidy 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 frequencies.
This mechanism has been observed in triploid parthenogenetic 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) lichenella also exhibits this type of meiosis [Narbel-Hofstetter, 1950]. Narbel-Hofstetter was uncertain of the species identity of her subject and tentatively identified it as
a parthenogenetic race of D. lichenella. Linnaeus had described 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]. According to Narbel-Hofstetter [1950], the chromosomes of
D. lichenella pair at the first meiotic division, and bivalents are formed at the first metaphase. The chromosomes 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 tetraploid number of chromosomes. Such a process is not expected to cause genetic erosion and, as shown by Chevasco 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. Consequently, the genetic constitution of the mother is passed
unchanged to her offspring. Asher and Nace [1971] studied 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 parthenogenetically 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 premeiotic doubling in Schmidtea, which also exhibits apomictic parthenogenesis. Some worms are diploid and reproduce sexually but others are triploid or tetraploid pseudogamous 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 polyploid 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].
DOI: 10.1159/000351731
195
secondary oocyte
ootid
ootid
ootid
ootid
secondary oocyte
primary oocyte
primary oocyte
germinal cell
Premeiotic doubling
Fig. 6. The genetic consequences of premeiotic doubling. The genome of the mother is passed unchanged to the offspring. Ootid =
Polar body and oocyte; secondary oocyte = product of the first division.
Premeiotic doubling is the prevalent mode of meiosis

in several large groups of polyploid parthenogenetic animals 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 hermaphroditic. The meiosis of polyploid lumbricids is entirely regular so that only bivalents are formed at the first
meiotic division [Omodeo, 1951a, b; Muldal, 1952]. Premeiotic doubling takes place in the testes of parthenogenetic polyploids, but normal sperm is evidently not produced [Christensen, 1980b].
Triploid Poeciliopsis (see the section on hybridogenesis) have originated through a series of hybridizations. A
196

DOI: 10.1159/000351731
fish with a genetic constitution comprising 1 genome of

P. monacha and 2 genomes of P. lucida called P. monacha-2 lucida has been observed. There are several kinds
of triploids involving different doses of haploid sets derived 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 cytologically reproduces through automictic parthenogenesis involving premeiotic doubling [Cuellar, 1971]. The whiptail 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 duplication 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 localized. Heteronotia has a very extensive distribution that
covers most of Australia [Fujita and Moritz, 2009]. The
triploid parthenogenetic Heteronotia binoei has originated through reciprocal crosses involving 2 diploid bisexual 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 mosaic, despite often being grouped with polyploids that reproduce sexually [Bickham et al., 1993].
A Mixed Case of Parthenogenesis
Christensen [1980b] describes the restoration of the
chromosome number in the polyploid and parthenogenetic enchytraeid Fridericia galba. Some chromosomes
form bivalents and undergo meiosis, while some others
apparently follow a mitotic pattern.
The enchytraeid Lumbricillus lineatus has parthenogenetic tri-, tetra- and pentaploid forms [Christensen, 1960,
1980a, b]. Its meiosis is asynaptic and the undivided univalents move in approximately equal numbers towards
Stenberg /Saura
the poles, where they are arrested at mid-anaphase. Division is initiated when the eggs are laid. The spindle elongates, the chromosomes move further apart and the spindle 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 resulting 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, contracting 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 mitotic cell division. A similar mechanism operates in the
major mode of parthenogenesis in plants. Apomictic parthenogenesis has originated independently in many polyploid animals. Two evolutionary scenarios can be invoked
to explain this. First, there may have been an intermediate
diploid parthenogenetic stage that became polyploid. Alternatively, 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 reported by Omodeo [1955] and Casellato and Rodighiero
[1972] to reproduce through apomixis. All other parthenogenetic and polyploid lumbricids exhibit automixis
with premeiotic doubling [Omodeo, 1951a, b; Christensen, 1980b].
In D. octaedra, the chromosome number is not doubled and the chromosome number is not reduced in the
oocytes, which undergo just 1 round of a single maturation 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 subsequent 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 experiments 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 reproduce via cyclical parthenogenesis, with parthenogenetic
females exhibiting apomictic parthenogenesis [Suomalainen 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 reproduce via obligate parthenogenesis [Beaton and Hebert, 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 parthenogenesis [Matthey, 1941].

DOI: 10.1159/000351731
197
Fig. 7. Gonomery or genome segregation in the apomictic oogen-
esis of tetraploid eggs of Otiorhynchus dubius. Upper left: a metaphase 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 Suomalainen [1940], with permission.
Coleoptera represent the largest order of animals. As

expected, they have several parthenogenetic and polyploid 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 apomictic 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 towards higher degrees of polyploidy. When there are several 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 wee198

DOI: 10.1159/000351731
vils (fig.7). An egg from a tetraploid female of e.g. Otiorhynchus dubius could have plates consisting of 33 and 11
chromosomes. Others might have 2 plates with 22 chromosomes, 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 gonomery and argued that the level of polyploidy had increased 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 parthenogenetic triploid that could have gone on to produce
a tetraploid in the same way, etc. The origin of parthenogenesis 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 prophase 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 nowseparate 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 Suomalainen [Saura et al., 1993].
Saura et al. [1993] argued that triploidy and parthenogenesis must have originated simultaneously, e.g. in a
species hybrid. Triploidy is, by far, the most common degree of ploidy in weevils. Given the rarity of parthenogenetic diploids, they are probably derived from triploids
via a shuffling of the haploid metaphase plates. New degrees of ploidy may be added via the same mechanism or
through chance fertilizations by diploid males. The geographical 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 sexual females. The genitalia of diploid sexual weevils and their
diploid or polyploid parthenogenetic counterparts are essentially similar [Szkessy, 1937]. Absence or relative rarity 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
Stenberg /Saura
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 apomictic parthenogenesis. Bromius (Adoxus) obscurus is triploid 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 European 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 allfemale populations. These fish live in disjunct populations in northeastern Mexico and adjacent areas of Texas
[Schultz, 1980]. They originated via hybridization involving 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 monophyletic origin [Lampert et al., 2005]. They produce viable female offspring through apomictic parthenogenesis
involving pseudogamy [Schultz, 1980]. Crosses of P. mexicana 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 meiotic division. When diploid oocytes from such laboratory
crosses were fertilized, however, they gave rise to viable
triploid offspring but did not generate diploid gynogenetic 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 pseudogamy in diploid Poecilia. One is temporary and autodiploid, 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 maternal set of chromosomes by suppressing the second meiotic 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. formosa, and this function may also be fulfilled by rare triploid males, though this has not been empirically demonstrated [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 chromosome 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. latipinna chromosomes and 2 from P. mexicana or vice-versa.
Following Schultz [1980], they should be called P. 2 mexicana-latipinna or P. mexicana-2 latipinna to indicate the
identity of their genomes. P. formosa may also rarely exhibit mosaicism so that somatic tissues of an individual
contain haploid, diploid and triploid cells [Lampert et al.,
2007b].

DOI: 10.1159/000351731
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 explain the geographical success of parthenogens better
than parthenogenesis itself. However, they are hard to
disentangle. Lundmark and Saura [2006] reviewed the literature on parthenogenesis, geographical distribution
and polyploidy in arthropods and concluded that polyploidy is the factor that is most likely to explain the success 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 parthenogenesis and perhaps even gynogenesis appear to be absent 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 [Casellato, 1987]. They lack sex chromosomes altogether; i.e.
the factors that are considered to represent the major obstacles to the formation of polyploidy in animals [Muller,
1925; Mable, 2004; Wertheim et al., this issue]. The polyploids are generally parthenogens, but there are poly199
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 diploid through octoploid. The only parthenogenetic form is
septaploid [Viktorov, 1997]. In this taxon, ploidy levels
correlate positively with geographic distribution, irrespective of the mode of reproduction [Grafodatsky et al.,
1982; Perel and Grafodatsky, 1983; Viktorov, 1997]. It
therefore seems that polyploidy rather than parthenogenesis 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 determined, but it should be always considered as a potentially occurring factor in surveys of animal distribution,
reproduction and evolution.
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Meiosis and Its Deviations in Polyploid

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Published online: June 18, 2013