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Meiosis and Its Deviations in Polyploid
Meiosis and Its Deviations in Polyploid
Meiosis and Its Deviations in Polyploid
Department of Molecular Biology, and b Computational Life Sciences Cluster (CLiC), Ume University,
Ume, Sweden
Key Words
Gynogenesis Hybridogenesis Kleptogenesis
Parthenogenesis
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
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
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
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]).
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.
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-
189
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
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.,
Meiosis in Polyploid Animals
191
secondary oocyte
primary oocyte
ootid
secondary oocyte
cleavage nuclei
ootid
ootid
ootid
cleavage nuclei
diploid
Gamete duplication
ootid
cleavage nuclei
diploid
cleavage nuclei
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
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
secondary oocyte
ootid
secondary oocyte
ootid
ootid
ootid
diploid
Terminal fusion
ootid
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
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
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
Cytogenet Genome Res 2013;140:185203
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
194
secondary oocyte
secondary oocyte
polar body
diploid
diploid
ootid
ootid
ootid
ootid
secondary oocyte
secondary oocyte
primary oocyte
primary oocyte
Stenberg /Saura
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].
Cytogenet Genome Res 2013;140:185203
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.
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].
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.
Meiosis 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].
197
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.
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
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].
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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