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Biological Journal of the Linnean Society, 2013, 109, 487–495. With 1 figures
Premeiotic endomitosis and the costs and benefits of
asexual reproduction
MICHAEL MOGIE*
Department of Biology and Biochemistry, University of Bath, Bath BA2 7AY, UK
Received 30 August 2012; revised 18 December 2012; accepted for publication 18 December 2012
Different patterns of development can influence the strength and direction of selection of a trait. Here, it is shown
how this may be the case for asexual reproduction in which eggs (animals) or spores (plants) inherit the maternal
chromosome number through a precursor cell undergoing an endoduplication of its chromosomes prior to meiotic
reduction. Asexuality involving premeiotic endoduplication (APE) has a wide but uneven distribution among
animals and plants. It is argued that different patterns of egg and spore production and differences in when
endoduplication occurs, together with differences in breeding structure (dioecious vs. hermaphroditic) and reproductive strategy (e.g. spawning vs. vivipary), can result in APE being associated with fecundity costs that can
result in an overall cost of sex or in an overall cost of asex or in APE being selectively neutral relative to sex. There
is a lack of a close correlation between the taxonomic distribution of APE and its potential costs and benefits
however, possible causes of which are explored. © 2013 The Linnean Society of London, Biological Journal of the
Linnean Society, 2013, 109, 487–495.
ADDITIONAL KEYWORDS: asexual reproduction – apogamy – cost of asex – cost of sex – endoduplication
– endomitosis – parthenogenesis.
INTRODUCTION
Asexual reproduction will replace sexual reproduction
if asexual females or hermaphrodites are reproduced
at a rate greater than that of sexual females or
hermaphrodites (all else being equal). Sexual females
reproduce sons as well as daughters (Maynard Smith,
1978), and asexual hermaphrodites can fertilize the
eggs of sexuals, siring progeny that are asexual
(Charlesworth, 1980). Hence replacement of sex by
asex can occur even if the fecundity of asexuals is
much less than that of sexuals. For example, all else
being equal, asex will replace sex in a dioecious population with a 1 : 1 sex ratio if the fecundity of asexuals
is greater than half that of sexuals.
Clearly, reductions in fecundity resulting from the
acquisition of asex must be large if they are to
prevent asex replacing sex. Here, a potential cause of
such large reductions is explored with respect to
asexuality involving premeiotic endoduplication
*E-mail: [email protected]; [email protected]
(APE). In organisms reproducing by APE, an egg
(animals) or spore (plants) with the maternal chromosome number is produced through a precursor cell
undergoing an endoduplication of its chromosomes
followed by meiotic reduction. Offspring inherit only
maternal chromosomes, either through parthenogenesis, gynogenesis, or apogamy (i.e. in ferns, the development of embryos from somatic cells of the
gametophyte that has developed mitotically from the
spore). APE is reported in turbellarians, earthworms,
insects, mites, fishes, amphibians, and reptiles
(Stenberg & Saura, 2009) and may be characteristic
of reproduction in most persistently unisexual vertebrates (Neaves & Baumann, 2011). It occurs in almost
all asexual ferns (Walker, 1966) but has been recorded
in only one genus (Allium) of flowering plants (Kojima
& Nagato, 1992).
The cause of the reductions in fecundity that will be
described appears to be exclusive to APE. It is argued
that the reductions can be sufficient to confer an
overall cost of asex in some taxa but will be small or
absent in others. This variation reflects variation in
the process of egg or spore production, in reproductive
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
487
488
M. MOGIE
Sexual
Asexual with
premeiotic
doubling
2n
2n
mitosis
endomitosis
2n
2n
4n
reductional meiosis
generating a tetrad
n
n
2n
n
n
2n
n
n
2n
n
n
2n
fertilisation
parthenogenesis
or apogamy
fecundity
x2
fecundity
x1
Figure 1. A generalized outline of the potential fecundity
costs of APE. In a sexual individual a diploid (2n) egg or
spore precursor cell undergoes a premeiotic mitosis, generating two diploid daughter cells. Each enters meiosis.
The precursor cell therefore gives rise to two tetrads of
haploid (n) cells. In contrast, the diploid precursor cell in
the asexual individual undergoes a premeiotic endomitosis
to generate a single tetraploid (4n) product that enters
meiosis. The precursor cell therefore gives rise to a single
tetrad of diploid cells. Here, a switch from sex to APE
results in a 50% reduction in the number of cells entering
meiosis and therefore in a 50% reduction in the number of
meiotic products. Potentially, therefore, individuals reproducing by APE could experience only half the fecundity of
sexual relatives.
strategy, in breeding structure, and in the location of
the endoduplication event. The extent to which the
taxonomic distribution of APE is shaped by these
costs, by their avoidance, or by constraints on its
evolution is explored.
POTENTIAL FECUNDITY COSTS OF APE
The basic argument for associating APE with fecundity costs is as follows (Fig. 1). Consider a diploid cell
about to undertake premeiotic mitosis. In a sexual
individual, this mitosis results in two diploid daughter cells each of which enters meiosis. Assume that
each meiosis results in a single haploid egg (with the
other three members of the meiotic tetrad degenerating). Hence the initial diploid cell gives rise via its
two mitotically derived daughters to two meiotically
derived eggs. In contrast, in an individual reproducing by APE the premeiotic mitosis is an endomitosis.
This results in a single tetraploid daughter cell rather
than in two diploid daughter cells. The single tetraploid daughter cell enters meiosis to give a single
diploid egg. Hence the initial diploid cell gives rise via
its single endomitotically derived daughter to a single
meiotically derived egg. Thus the asexual individual
experiences a 50% reduction in egg production compared with the sexual individual. This will result in a
fecundity cost of APE if there is a positive correlation
between the number of eggs initiated and reproductive success.
The fecundity costs potentially associated with APE
may be large enough to greatly reduce or neutralize
the overall cost of sex or replace it with an overall cost
of asex. For example, reproductive success will be
halved if it is determined by the number of eggs
initiated. The cost implications of this halving differ
between dioecious and hermaphroditic organisms. For
a dioecious population with a 1 : 1 sex ratio, the
halving will result in sexual and asexual females
reproducing the same number of daughters, in which
case APE will be selectively neutral relative to sex.
For a population of hermaphrodites, because all offspring produce eggs, the halving will result in an
overall 50% cost of asex if the switch to APE also
results in male sterility. This cost will be reduced if
asexuals are able to sire progeny that are asexual in
crosses with sexuals, but it will remain substantial
unless asexuals are very effective male parents. This
will be unlikely as the male function in asexual hermaphrodites is often poor (Mogie, 2011).
The argument developed in the previous two paragraphs indicates how the fecundity costs associated
with APE can render asex neutral or costly compared
with sex. But the argument is expressed in very
general terms and does not take into account variation between major taxa in the pattern of egg or spore
production. Different patterns have different cost
implications. Therefore, the effects on fecundity of a
switch from sex to APE will be considered for each of
the major taxonomic groups in which its occurrence
has been reported: flowering plants, ferns, vertebrates, and invertebrates.
Mention also needs to be made about the uncertainty surrounding the location of the endoduplication
event, as different locations can have radically different cost implications. Endoduplication can involve the
premeiotic mitosis (e.g. Stenberg & Saura, 2009), but
documentation of when or how it occurs is poor. For
example, doubled chromosome complements consistent with endoduplication have been observed in parthenogenetic vertebrates but the event giving rise to
this doubling has not been observed (Neaves &
Baumann, 2011). In Allium, endoduplication does not
involve the premeiotic mitosis but occurs either
during the interphase preceding meiosis or during
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
PREMEIOTIC ENDOMITOSIS AND COSTS OF ASEX
prophase of the first meiotic division (Kojima &
Nagato, 1992). The latter is also its location in some
stick insects (Scali, 2009) and may be its location in
the grasshopper Warramaba virgo (White et al.,
1977). This is important, as meiotic endoduplication
does not influence the number of cells undergoing
meiosis and is not predicted to influence the number
of meiotic products. Hence, large fecundity costs may
be associated with premeiotic endomitosis but they
are not predicted to be associated with meiotic
endoduplication.
FLOWERING
PLANTS
These are heterosporic, producing two types of spore
from different meioses: megaspores which give rise to
eggs; and microspores which give rise to male
gametes. Egg production begins with a megaspore
mother cell (MMC) developing within an ovule and
undergoing meiosis. In most taxa, one member of the
resulting tetrad survives to form a megaspore. This
initiates three rounds of mitosis, resulting in an
eight-nucleate embryosac (female gametophyte) one
cell of which differentiates as an egg. Variation in
megaspore production and embryosac development
does occur (Yadegari & Drews, 2004) but, typically, an
ovule gives rise to a single mature embryo [although
polyembryonic seeds occur as anomalies in many taxa
(Carman, 1997)]. On maturation, the ovule and
embryo comprise the seed.
The endoduplication associated with a switch to
APE has three possible locations: the mitosis that
produces the MMC, premeiotic interphase, and
prophase of the first meiotic division. None of these
locations will interfere with the development of a
megaspore, and hence with the development of a
fertile seed containing a single embryo. Thus fecundity effects resulting from endoduplication are not
expected to accompany a switch to APE, in which case
sex will be costly compared with APE.
FERNS
Most ferns are homosporous, with meiosis resulting
in a single type of spore. Following dispersal the spore
develops mitotically into a multicellular, cosexual
gametophyte that generates eggs and sperm by
mitosis. Eggs are retained by gametophytes and
embryos develop in situ.
Spore production in ferns begins when an archesporial cell (AC) within a sporangium initiates a
series of m mitoses (usually, m = 4). In sexuals, this
results in 2m spore mother cells (SMCs) that undergo
meiosis. Each member of a meiotic tetrad differentiates as a spore, thus an AC gives rise to 4(2m) spores.
A switch to APE in which endoduplication is achieved
489
through a premeiotic endomitosis will halve this
number, as it will result in an AC giving rise to only
2m-1 SMCs, and thus to 4(2m-1) spores. A 50% reduction in spore number per sporangium is characteristic
of APE (Walker, 1966; Beck, Windham & Pryer, 2011),
indicating that endoduplication is achieved through a
premeiotic endomitosis rather than during meiotic
prophase.
The implications of this reduction are discussed
elsewhere (Mogie, 1990, 1992). Briefly, all else being
equal, a 50% reduction in spores will result in an
equivalent reduction in the number of gametophytes
and hence in the number of embryos and sperm. The
capacity of asexuals to sire viable, fertile progeny in
crosses with sexuals will be further compromised by
sperm having the full parental complement of chromosomes, resulting in progeny with elevated ploidy
levels. After a few generations, the male function of
asexuals could drive ploidy levels to the maximum
level compatible with viability, after which it would
contribute only to inviable progeny. This will reduce
the reproductive success of sexuals, but there is no
reason to expect that the scale of this reduction will
be sufficient to compensate for the 50% reduction in
fecundity experienced by asexuals as a consequence of
APE. Moreover, further fecundity costs are associated
with APE in ferns as the premeiotic mitosis in some
sporangia is normal rather than endomitotic, but the
subsequent meioses in these sporangia are irregular
and result in abortive spores (Walker, 1966). Hence
an overall substantial cost of asex will be associated
with APE in ferns.
ANIMALS
Egg production begins when a germ line stem cell
(GSC) divides mitotically to produce a daughter GSC
and a non-GSC daughter. The former repeats this
process. The latter may differentiate directly into an
oocyte and enter meiosis. This is the case in some
insects with panoistic ovaries [although it is not clear
whether a single premeiotic mitosis is characteristic of
panoistic ovaries in this group (Büning, 1994)]. Alternatively, the non-GSC daughter may initiate a series
of mitoses, generating a cyst (cluster) of cells. All cells
in a cyst may become oocytes and enter meiosis (see
Supporting Information, Fig. S1). This is the case in
insects with neopanoistic ovaries and appears to be
the case in vertebrates (Matova & Cooley, 2001;
Lechowska et al., 2012). It is also expected to be the
case in any insects that have panoistic ovaries in
which the non-GSC daughter initiates a series of
mitoses. In animals with meroistic ovaries, however,
only one or a few cells in the cyst become oocytes
and enter meiosis, with the rest becoming supportive nurse cells (see Fig. S2). Meroistic ovaries are
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
490
M. MOGIE
characteristic of modern groups of insects. Panoistic
ovaries are characteristic of most arachnids, crustaceans, and pantopods, and of basal groups of insects.
Neopanoistic ovaries are found in Thysanoptera and
Plecoptera (Büning, 1994).
Here, the use of ‘meroistic’ will be extended to
describe egg production in any animal taxon in which
a GSC gives rise to nurse cells as well as to oocytes.
These include annelids (Świa˛tek et al., 2012), mites
(Cabrera, Donohue & Roe, 2009), and Coleoptera
(Büning, 1994), which include taxa that reproduce by
APE. For example APE has been reported in the
annelid Tubifex tubifex (Baldo & Ferraguti, 2005), the
mite Brevipalpus obovatus (Pijnacker et al., 1980),
and the beetle Ptinus clavipes f. mobilis (Smith,
1971).
The use of ‘panoistic’ will be extended to describe
egg production in any animal taxon in which the
non-GSC daughter either enters meiosis or produces
a cyst of descendant cells by mitosis, all members of
which differentiate as oocytes and enter meiosis.
These include vertebrates, Orthopetera (Büning,
1994), and turbellarians, which include taxa that
reproduce by APE. For example, APE has been
reported among vertebrates in the fish Poeciliopsis
(Cimino, 1972) and in lizards (Kearney, Fujita &
Ridenour, 2009), among Orthoptera in W. virgo
(White et al., 1977), and among turbellarians in
Schmidtea polychroa (D’Souza & Michiels, 2009).
[The ancestral condition of oocyte production in the
Turbellaria is archoophoran, whereby a female gonad
produces oocytes that manufacture their own yolk
and egg shell. In the more derived neoophoran condition (found in Schmidtea) the female gonad contains
alecithal oocytes and vitelline cells that produce both
the yolk and egg shell forming granules required for
oocyte maturation (Gremigni, 1997). The vitellaria
that produce the vitelline cells and the germaria that
produce the oocytes are produced by different cell
lines formed by the division of the female germ cell
lineage (Levron et al., 2010). Hence vitelline cells do
not appear to be analogous to the nurse cells of
meroistic ovaries (which are produced by the same
cell line as the oocyte). Consequently, with respect to
the potential costs of APE, the pattern of oocyte
production in both archoophoran and neoophoran
types appears to be sufficiently reminiscent of that
found in the panoistic ovaries of other invertebrate
groups to merit inclusion under the extended definition of panoistic used here.]
For both meroistic and panoistic ovaries, a switch
from sex to a form of APE in which endoduplication
occurs during meiotic prophase will not affect the
number of oocytes, and hence will not affect the
number of meioses or meiotic products. A switch of
this type therefore will not affect fecundity. Conse-
quently, sexuals co-occurring with individuals with
APE will experience an overall cost of sex. In contrast, a switch to a form of APE in which endoduplication is achieved through a premeiotic endomitosis
can reduce the number of oocytes, and therefore can
be associated with fecundity costs that can reduce the
overall cost of sex or replace it with an overall cost of
asex or with sterility. The effect depends on ovary
type and is explored below.
PANOISTIC
OVARIES WITH A SINGLE
PREMEIOTIC MITOSIS
Candidate insects for this ovary type include
the Archeognatha, the Zygentoma, the Odonata, the
Embioptera, the Phasmatodea, the Orthoptera, the
Grylloblattaria, and the Dictyoptera (Büning, 1994).
Here, the GSC divides mitotically to produce a daughter GSC and a non-GSC daughter that does not
undergo mitosis but enters meiosis. The evolution or
establishment of APE involving premeiotic endomitosis may be unlikely in these taxa. This is because the
endoduplication event will have to involve the GSC
mitosis, as this is the only premeiotic mitosis. This
will result in the GSC mitosis giving rise to a single
cell, rather than to a daughter GSC and an oocyte.
This cell could remain a GSC or differentiate as an
oocyte. It can be speculated that the former is likely,
as the different fates of the two daughter cells of
normal GSC mitosis are a consequence of them experiencing different environments. Thus a GSC develops as a GSC because it is located within a GSC niche
(Spradling et al., 2011). Following a normal mitosis,
one daughter cell is retained within the niche and
therefore develops as a GSC. The plane of division
moves the other daughter outside of the niche into an
environment compatible with it differentiating as an
oocyte. Presumably, an endomitosis would result in
the single-cell product remaining within the GSC
niche and developing as a GSC.
If this speculation is incorrect and the GSC does
leave its niche after endomitosis, it will differentiate
into an oocyte. But this will be associated with a rapid
depletion of GSCs. A failure to fully replace these will
result in a reduction in oocyte production and thus,
potentially, in a reduction in fecundity. It is unclear
whether this reduction in fecundity will be sufficient
to confer an overall cost of asex.
If the speculation is correct, however, and the GSC
remains in the GSC niche after endomitosis, one of
two fates is likely. Either it enters further endocycles,
or it reverts to a normal mitosis. The first fate will
result in the GSC experiencing increasing ploidy
levels but will never result in an oocyte. Here,
endoduplication will be associated with sterility, not
with asexual reproduction. The second will result in
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
PREMEIOTIC ENDOMITOSIS AND COSTS OF ASEX
the GSC reinitiating oocyte production. Here, endoduplication will be associated with the loss of a single
egg for each active GSC, a reduction that may not
have a great effect on fecundity. This latter fate may
be unlikely, however, because studies of endocycles in
insects that occur as a normal part of differentiation
and development show that cells that undergo such
divisions rarely, if ever, return to normal mitosis (Fox,
Gall & Spradling, 2010).
In conclusion, the evolution of a viable form of APE
may be unlikely in animals with this type of ovary
when endoduplication is achieved through a premeiotic endomitosis.
491
oocytes in annelids (Świa˛tek et al., 2012). This will be
accompanied by the loss (through endomitosis) of one
nurse cell for each oocyte produced in individuals
reproducing by APE. And in the sexual dermapteran
Anisolabis maritima, a sequence of three mitoses
generates four two-celled clusters each of which comprises an oocyte and nurse cell (Büning, 1994). If a
switch to APE involving a premeiotic endomitosis was
to occur, two two-celled clusters could be produced
resulting in a 50% reduction in oocytes, or four
oocytes could be produced whose viability would be
threatened by the absence of supporting nurse cells.
DISCUSSION
PANOISTIC
OVARIES WITH
>1
PREMEIOTIC MITOSIS
The fecundity implications of a switch from sex to
APE are the same as those already described for ferns
and are illustrated in Figure 1. m generations of
mitosis separate the GSC from the oocytes entering
meiosis (m > 1). Hence a GSC in a sexual individual
gives rise to 2m oocytes that enter meiosis, but a GSC
in an individual reproducing by APE gives rise to only
2m-1 oocytes, as the final mitosis is an endomitosis.
Thus a transition from sex to APE is associated with
a 50% reduction in the number of oocytes entering
meiosis, and thus with a reduction in fecundity if
there is a positive correlation between the number of
oocytes and fecundity. As noted at the beginning of
this section, a 50% reduction in fecundity will result
in APE being selectively neutral relative to sex in a
dioecious population with a 1 : 1 sex ratio, and will
result in APE being associated with an overall cost of
asex in hermaphrodites.
MEROISTIC
OVARIES
The fecundity implications of a switch from sex to
APE are illustrated in Figure S2. A GSC initiates m
mitotic generations to form a cell cluster. Depending
on taxon, one or several cells in the cluster differentiate as oocytes and enter meiosis, with the rest
differentiating as nurse cells (Büning, 1994). With
APE, the production of an oocyte will require one cell
within a cluster to undergo an endomitosis rather
than a mitosis. This will not affect the number of
clusters. But one nurse cell will be lost within a
cluster for each oocyte produced endomitotically. The
loss of a single nurse cell may not affect oocyte viability if the cluster is large and only one cell differentiates as an oocyte. This is unclear. But if viability is
maintained APE will not be associated with fecundity
costs. Hence it will be associated with an overall cost
of sex. Fecundity costs are likely with some patterns
of cluster differentiation, however. For example,
several cells within a cluster can differentiate as
Debate about the source and extent of costs of sex
continues (Lehtonen, Jennions & Kokko, 2012;
Meirmans, Meirmans & Kirkendall, 2012). Here, the
potential for an association between APE and fecundity costs is investigated. Measures of gamete or
offspring number do indicate that some asexuals
reproducing by APE experience fecundity costs compared with sexual relatives. Spore production per
sporangium in asexual ferns is 50% that in sexuals
(Walker, 1966; Beck et al., 2011). Within the
Ambystoma jeffersonianum complex of mole salamanders, the number of eggs produced by asexuals was,
on average, only approximately two-thirds that of
sexuals (Uzzell, 1964). Gynogenetic triploids of the
topminnow Poeciliopsis monacha-lucida have lower
size-corrected fecundity than the diploid sexual
parental species P. monacha (Lima & Bizerril, 2002).
It is unclear whether APE is associated with fecundity effects in other taxa. APE is not predicted to be
associated with reductions in egg production in flowering plants, but even if such a reduction was to occur
it may not result in a reduction in fecundity, as plants
typically initiate far more seeds than they mature
(Wiens, 1984). Evidence is limited on the fecundity of
parthenogenetic reptiles compared with their sexual
relatives (Eckstut et al., 2009). The evidence that is
available does not indicate that asexuals typically
suffer fecundity costs, with lower, equal and higher
fecundity being reported in asexuals compared with
their sexual relatives (Kearney et al., 2009). Differences between sexuals and asexuals in reproductive
characteristics are reported for the planarian
Schmidtea polychroa (e.g. Weinzierl, Schmidt &
Michiels, 1999). But asexual reproduction is by
apomixis in some lineages and by APE in others
(D’Souza & Michiels, 2009). As apomixis does not
involve endoduplication it is not associated with
the fecundity costs that can be associated with
APE. Hence individuals reproducing by apomixis
need to be compared with those reproducing by APE
before differences between sexuals and asexuals in
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
492
M. MOGIE
reproductive characteristics can be ascribed to APE
rather than to apomixis or to asexuality per se.
Caution should be exercised in ascribing endoduplication as the cause of any fecundity differences
between individuals reproducing by APE and sexual
relatives. The causal link between endoduplication
and a reduction in spore production is clear for ferns.
But the link between endoduplication and fecundity is
less clear for other taxa, not least because it may not
be known whether endoduplication is achieved via a
premeiotic endomitosis rather than through a doubling during meiotic prophase (which will not be
associated with reductions in the number of spores or
eggs initiated). Moreover, differences in fecundity
between sexuals and asexuals may have other causes.
For example, as noted for squamate reptiles by
Kearney & Shine (2005), reduced fecundity over a
breeding period in asexuals may be the result of
selection for long-term survival and reproductive
success. Similarly, whereas endoduplication may contribute to the lower fecundity of asexual Poeciliopsis
monacha-lucida compared with that of the sexual
parental species P. monacha, there is another potential cause that may contribute to these differences.
This is the presence in the asexual of the parental
P. lucida genome (Lima & Bizerril, 2002).
Another potential cause of reduced fecundity in
asexuals is defects during embryo development
(Uyenoyama, 1984; Lively & Johnson, 1994). These
may result from the destabilizing effects of polyploidization or hybridization, both of which are often
associated with APE. In flowering plants, they may
result from genetic imbalance between the embryo
and nutritive endosperm (Haig & Westoby, 1991;
Koltunow & Grossniklaus, 2003). They may also
result from the exposure of recessive deleterious
genes due to an increase in homozygosity (Archetti,
2010). The latter may not be a major cause of reductions in fecundity of individuals reproducing by APE,
however, because sister chromosome pairing during
meiosis may be common. This pairing pattern will
maintain heterozygosity and is associated with APE
in several taxa, including Allium (Kojima & Nagato,
1992), Aspidoscelis lizards (Lutes et al., 2010),
Ambystoma (Bell, 1982; Bi & Bogart, 2010), Warramaba virgo (White et al., 1977), and Schmidtea
polychroa (D’Souza & Michiels, 2009).
Although no clear message has yet emerged about
the extent to which APE is associated with fecundity
costs, a causal link between these and endoduplication is clear in some taxa (e.g. ferns) and predicted in
others. The taxonomic distribution of APE is not that
predicted from knowledge of these costs, however. For
example, approximately 10% of ferns are asexual, and
almost all of these reproduce by APE (Walker, 1966).
Yet the 50% reduction in spore production associated
with APE is predicted to result in a substantial cost of
asex. In contrast, APE is very rare in flowering
plants, where it is not expected to be associated with
fecundity costs (hence it is expected to be associated
with a cost of sex). A major reason for this pattern of
occurrence appears to involve constraints, the imposition of which can prevent APE’s evolution in flowering plants, and the lifting of which can favour its
establishment in ferns.
The evolution of APE may be unlikely in flowering
plants because it may be unlikely that eggs produced
by a process involving endoduplication followed by a
reductional meiosis will avoid fertilization. Hence a
mutation causing these changes would result in an
aberrant and inviable form of sex (with a lineage
achieving deleteriously high ploidy levels after a few
generations) rather than in a viable form of asex. This
argument emerges from a consideration of the
number of cell divisions involved in egg production,
which imposes a minimum time for egg maturation
(Mogie, 1992). In sexual flowering plants, the
minimum time required for an MMC to produce an
egg is that needed for a reductional meiosis followed
by the mitoses involved in embryosac development.
Flower opening and pollen release coincide with egg
maturation. As APE also involves a reductional
meiosis and the subsequent mitoses involved in
embryosac development, eggs would also mature
when conditions are conducive to fertilization. The
requirement to avoid fertilization may explain why
common forms of asex in flowering plants are apomictic. Apomixis is associated with meiotic restitution or
with the avoidance of meiosis, both of which can
result in eggs developing more rapidly than those
produced by reductional meiosis. Earlier maturation
provides eggs with the opportunity to divide parthenogenetically before pollination can occur and may be
a common requirement for the evolution of asex in
this group (Mogie, 1992).
A key insight into the success of APE in ferns is
that, with embryos reproduced apogamously, APE
does not involve eggs and hence sperm are not able to
disrupt it. [Indeed, asexual ferns appear to be unable
to produce eggs (Walker, 1966), so apogamy provides
them with an escape from female sterility.] This is
important because during sexual reproduction sperm
must swim through free water to gain access to eggs
which are retained by the gametophyte. Embryos are
not dispersed. Because of this, ferns reproducing
sexually are restricted to sites that have free water
during the reproductive season. In contrast, because
of the absence of a requirement for sperm the reproductive success of apogamous ferns is not dependent
on free water. They can therefore achieve ecological
isolation from sexuals by establishing in sites that are
too dry for sexual reproduction (Mogie, 1990, 1992).
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495
PREMEIOTIC ENDOMITOSIS AND COSTS OF ASEX
Such isolation may be essential to the success of APE
in this group given the fecundity costs with which it
is associated. Isolation may be aided by hybridization,
with which the evolution of asexuality is associated
(Walker, 1966).
The 50% reduction in spore production in ferns
reproducing by APE is associated with a cost of asex
because they are hermaphroditic. Among dioecious
vertebrates, females reproducing by APE are predicted to experience a 50% reduction in oocyte production. This will result in APE being selectively
neutral relative to sex if the reduction in oocyte
production causes the same reduction in fecundity
and if the sex ratio is 1 : 1. Or it will result in small
costs or benefits of APE if the sex ratio deviates
slightly from 1 : 1 or if the reduction in fecundity is
close to but not identical to the reduction in oocyte
production. As small benefits of APE will be neutralized by small advantages of sex, the establishment
and maintenance of APE in this group is problematic.
A resolution of this problem is suggested by recognizing that a large reduction in oocyte initiation need not
result in an equivalent reduction in fecundity. Hence
an overall substantial cost of sex can characterize
interactions between sexuals and asexuals reproducing by APE.
APE in vertebrates appears to be concentrated
in taxa in which females invest heavily in a few
individually expensive offspring. For example, Poeciliopsis is viviparous (Panhuis et al., 2011). Parthenogenetic lizards are oviparous or viviparous and belong to
genera in which females produce small clutch sizes
(usually of fewer than five eggs per clutch) [Kearney
et al. (2009) provide a list of parthenogenetic lizards,
and appendix 2 of Meiri, Brown & Sibly (2012) provides information on clutch size]. The loach Misgurnus anguillicaudatus is a serial spawner with
relatively low fecundity (Growns, 2004). Ambystoma
jeffersonianum also lays eggs in several small
clutches, with a sexual female producing approximately 200 eggs during a breeding season (Uzzell,
1964; Brodman, 2002).
The bias in the distribution of APE away from taxa
in which females reproduce large numbers of individually cheap offspring (e.g. broadcast spawners)
towards those in which females reproduce small
numbers of individually expensive offspring may
reflect different fecundity costs associated with the
different reproductive strategies. Thus the correlation
between egg initiation and fecundity is likely to be
positive and strong in broadcast spawners, with a
large proportion of the many eggs initiated surviving
to develop into gametes (Rothchild, 2003). Here, the
potentially large fecundity costs of APE that may
result from the 50% reduction in oocyte production
are likely to be realized. In contrast, although cleidoic
493
or viviparous individuals can also produce many
oogonia and oocytes, most of these will degenerate, for
example through oocyte apoptosis and follicular
atresia (Rothchild, 2003; Krysko et al., 2008). Here,
the correlation between egg initiation and fecundity is
likely to be weak or non-existent with the result that
fecundity costs of APE will be small or absent.
In conclusion, new insights are provided about the
relationship between the maintenance of sex and patterns of egg and spore production, breeding system,
and reproductive strategy. It is argued that costs of
sex resulting from the production of males in dioecious taxa or from the siring of progeny by asexuals in
hermaphroditic taxa may be ameliorated or completely overcome by fecundity costs associated with
APE. Fecundity costs of APE are not predicted for all
taxonomic groups or for all reproductive strategies,
however. They are predicted for ferns but not for
flowering plants. They are predicted for invertebrates
with meroistic ovaries if cell clusters are small or if
many cells in a cluster differentiate as oocytes, but
they are not predicted if cell clusters are large and
most cells function as nurse cells. They are predicted
for vertebrates and for invertebrates with panoistic or
neopanoistic ovaries if there is a strong and positive
correlation between the number of oocytes initiated
and reproductive success, but they are not predicted if
this correlation is weak or absent because of high
frequencies of apoptosis and follicular atresia.
ACKNOWLEDGEMENTS
I thank two anonymous reviewers for their helpful
comments.
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SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Figure S1. An illustration of the fecundity costs of APE compared with sexual reproduction in vertebrates and
in invertebrates with neopanoistic ovaries or with panoistic ovaries in which there is more than one mitosis. The
figure depicts a diploid (2n) germ line stem cell (GSC) dividing mitotically to form a daughter GSC and a
non-daughter cell. The daughter GSC continues this process (indicated by dotted arrows). The non-daughter cell
initiates a series of m mitotic divisions to produce a cyst (cluster) of cells. m = 3 generations of mitosis are
illustrated. The mitoses are normal in the sexual pathway and result in a cyst of 2m = 8 diploid cells that enter
meiosis to produce eight haploid eggs that are fertilized to produce eight offspring. The first two mitoses in the
asexual APE pathway are also normal but the third is an endomitosis, resulting in a cyst of 2m – 1 = 4 tetraploid
cells that enter meiosis to produce four diploid eggs that divide parthenogenetically to produce four offspring.
Figure S2. An illustration of the fecundity implications of APE compared with sexual reproduction in animals
with meroistic ovaries. The figure depicts a diploid (2n) germ line stem cell (GSC) dividing mitotically to form a
daughter GSC and a non-daughter cell. The daughter GSC continues this process (indicted by dotted arrows). The
non-daughter cell initiates a series of m mitotic divisions to produce a cyst (cluster) of cells. m = 3 generations of
mitosis are illustrated. All mitoses are normal in the sexual pathway and result in a cyst of 2m = 8 diploid cells.
One of these becomes an oocyte and enters meiosis to produce a haploid egg that is fertilized. The remaining cyst
cells become nurse cells. In the asexual pathway one of the mitoses in the third mitotic generation is an
endomitosis; the others are normal mitoses. Hence the cyst in the asexual comprises six diploid nurse cells and
one tetraploid oocyte that enters meiosis to produce a diploid egg that develops parthenogenetically.
© 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 487–495