Review
Unisexual reproduction among
vertebrates
William B. Neaves1,3 and Peter Baumann1,2,4
1
Stowers Institute for Medical Research, Kansas City, MO 64110, USA
2
Howard Hughes Medical Institute, Kansas City, MO 64110, USA
3
School of Medicine, University of Missouri Kansas City, MO 64108, USA
4
Department of Molecular and Integrative Physiology, University of Kansas Medical Center, Kansas City, KS 66160, USA
The past decade has seen a remarkable revision of
perspectives on unisexual reproduction in vertebrates.
One can no longer view it as a rare curiosity far outside
the mainstream of evolution. More than 80 taxa of fish,
amphibians, and reptiles are now known to reproduce by
parthenogenesis (Greek for ‘virgin birth’) or its variants,
and they persist in nature as all-female lineages. Other
lower vertebrates that ordinarily rely on sexual repro-
duction can resort to facultative parthenogenesis under
extenuating circumstances that isolate females from
males. Molecular tools have now been applied to the
study of unisexual organisms, and fascinating insights
have emerged regarding the molecular mechanisms that
preserve heterozygosity and increase genetic diversity in
all-female populations. A deeper understanding of the
underlying genetics increasingly calls into question the
assumption that unisexuality in vertebrates is an evolu-
tionary dead-end.
Unisexual vertebrates
Approximately 80 taxa of unisexual vertebrates have been
described [1–3], but additional species are being discov-
ered, as exemplified by the recent description of the par-
thenogenetic lizard Leiolepis ngovantrii [4]. Among
vertebrates, reproduction in the complete absence of males
is restricted to reptiles and is referred to as true partheno-
genesis. Gynogenesis and hybridogenesis are related re-
productive modes found in fish and amphibians. Here,
sperm from males of related sexually-reproducing species
is required, but male DNA is generally not retained in the
germline [5] (Box 1).
True parthenogenesis avoids the two-fold cost of sexual
reproduction by making no investment in males and en-
abling each individual in an all-female species to produce
offspring independently. In consequence, every member of
the population is theoretically capable of unilaterally estab-
lishing the species in a new habitat. Why sexual reproduc-
tion is nevertheless so prevalent in nature remains a
fundamental mystery in evolutionary biology [6–9]. Study-
ing the exceptions – those species composed solely of females
– carries the promise of furthering our understanding of why
sexual reproduction is so widespread.
Parthenogenetic species are often referred to as ‘dead-
ends’ because the ability to recombine and generate new
Corresponding author: Baumann, P. (peb@stowers.org).
0168-9525/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tig.2010.12.002 Trends in Genetics, March 2011, Vol. 27, No. 3
combinations of traits is absent in clonally reproducing
lineages [10]. As a consequence, asexual species are
thought to succumb rapidly to parasites, diseases, and
predation because of their negligible ability to adapt in a
changing environment [11]. However, the recognition that
several asexual taxa have thrived for long periods of time
[12] raises questions about the generality of this assump-
tion [9]. By applying the tools of molecular biology and
genomics, researchers have started to uncover the under-
lying molecular mechanisms of parthenogenesis [13] and
have revealed how a surprising complexity of genetic
diversity is generated in unisexual populations of sala-
manders [14]. Although many recent insights into asexual
reproduction have emerged from studies in invertebrates
and plants, consideration of parthenogenesis in these taxa
is beyond the scope of this review, and we instead focus on
asexual reproduction in vertebrates.
Here we discuss recent findings on the origin of parthe-
nogenetic vertebrates, the ovarian mechanism that pro-
duces fertile eggs with a full chromosome complement, the
surprising ability to create diversity by adding and delet-
ing whole genomes, and the foray of sexually reproducing
species into occasional episodes of parthenogenesis.
Hybrid origin of unisexual species
In all known instances in teleost fish, unisexuality has
arisen through interspecific hybridization [15]. Similarly,
in salamanders and frogs unisexual lineages invariably
arose from hybridizing sexual species [16,17] and, with
one possible exception [18], hybridization between sexual
species has given rise to all parthenogenetic species of
lizards [3].
Because of their hybrid origin, each unisexual verte-
brate species combines at its inception much of the genetic
diversity of two different sexual species. At many loci,
individuals of a parental sexual species are homozygous
for a species-specific allele. In those instances where the
two parental sexual species have distinct alleles, both
alleles are detected in individuals of the derived partheno-
genetic species. When mixing alleles from the parental
species endows the resulting parthenogenetic lineage with
hybrid vigor, it could establish a new species with the
fitness required to compete successfully with its progeni-
tors or the ability to occupy a niche not used by the parental
species. The high level of heterozygosity in most partheno-
genetic vertebrate species is viewed as a significant factor
81
Review
Box 1. Modes of unisexual reproduction in vertebrates
In true parthenogenesis, reproduction occurs in the absence of any
male contribution. Females produce unreduced eggs that carry the
somatic chromosome complement of the mother and sponta-
neously develop into viable offspring that are clones of the mother
(Figure I). It should be emphasized that unisexual reproduction in
vertebrates has nothing to do with hermaphroditism, the production
of sperm and eggs by male and female gonads within a single
individual. Unisexual vertebrates are females whose ovaries
produce eggs that maintain the lineage, and male reproductive
organs are absent. Among vertebrates, obligate parthenogenesis
occurs exclusively in all-female species of squamate reptiles.
In gynogenesis, females produce unreduced eggs carrying the
somatic chromosome complement of the mother, but the eggs must
be stimulated by interaction with sperm to initiate embryogenesis.
Sperm is provided by males belonging to related sexually-reprodu-
cing species but contribute no genetic material to the offspring.
Gynogenesis occurs in some all-female species of fish and
salamanders.
In hybridogenesis, females produce reduced eggs carrying the
maternal haploid chromosome complement, and the eggs must be
fertilized by sperm from a male of another species to produce
offspring. Hybridogenic offspring express both the maternal and
paternal haploid genomes in their somatic cells, but the paternal
chromosomes are excluded early in oogenesis such that haploid
eggs carrying only the maternal chromosome complement are
produced. This hemiclonal mode of reproduction occurs in uni-
[()TD$FIG]
sexual frogs, salamanders and some fish.
Parthenogenesis Gynogenesis Hybridogenesis
AB AB
AB
B’B*
B’B*
B In the case of a parthenogenetic Australian gecko, Het-
B’
B’
AB AB A events with sexual cytotypes carrying unique chromosomal
AB AB’
B’
AB
AB
AB’
TRENDS in Genetics
Figure I. Modes of unisexual reproduction in vertebrates. In parthenogenesis
and gynogenesis the two haploid genomes A and B inherited from the two
parental species are transmitted via a diploid oocyte to the next generation.
Unlike parthenogenesis, gynogenesis requires sperm (B’) to stimulate
development; however, male DNA does not contribute genetic information.
In hybridogenesis only one ancestral genome (A) is transmitted into the oocyte
and the other (B) is discarded. Diploidy is restored with a new genome (B’)
from a related sexual male. The somatic cells of the new generation contain the
ancestral A genome and the new B’ genome, but only the A genome will again
be transmitted to the next generation. The mode of inheritance in
hybridogenesis is hemiclonal in that only the maternal genome is clonally
transmitted from generation to generation.
in their ability to persist in nature over thousands of
generations.
Given the dominant role of hybridization in the origin of
unisexual vertebrates [19], what can be said about the
frequency at which parthenogenetically competent hybrids
are generated? The answer varies widely among taxa. For
example, compelling evidence for the origin of a unisexual
species of poeciliid fish from multiple hybridization events
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Trends in Genetics March 2011, Vol. 27, No. 3
between the same two sexual species has emerged from
study of mitochondrial DNA in Poeciliopsis monacha–
lucida [20]. The high level of mtDNA diversity in P. mon-
acha–lucida indicates the presence of many distinct clonal
lineages arising from numerous separate hybridizations
between females of P. monacha and males of P. lucida.
Contrasting evidence comes from unisexual salaman-
ders of the genus Ambystoma. Present-day diploid unisex-
uals carry haploid nuclear genomes from two different
sexual species, either A. laterale and A. jeffersonianum,
or A. laterale and A. texanum [21]. However, none of these
three sexual species served as the maternal partner in the
initial hybridization event that first gave rise to the uni-
sexual lineages. Instead, mitochondrial DNA analysis
revealed that the original hybridization involved a female
related to A. barbouri, a sexual species whose maternal
nuclear genome is not found in any contemporary unisex-
uals [12,14,22]. Unisexual Ambystoma reproduce by com-
bining features of gynogenesis and hybridogenesis, and the
original nuclear genome of A. barbouri was subsequently
replaced by a haploid genome from a recent sperm donor
(A. laterale, A. jeffersonianum, or A. texanum). The persis-
tence of the mitochondrial heritage from A. barbouri in all
contemporary diploid unisexuals indicates that the line-
age-originating hybridization event occurred long ago and
has not been repeated recently [12,21]. A new term, klep-
togenesis, has been applied to this remarkable mechanism
that generates diversity by replacing whole genomes and
sometimes elevating ploidy to produce a diverse array of
genotypes within local populations of salamanders [14].
eronotia binoei, three chromosomally-distinct triploid
clones reflect multiple origins through hybridization
inversions [23]. Subsequent study of 18 allozyme loci
revealed a minimum of 52 distinct genotypes among 143
individuals [24] and indicated that much of the genetic
diversity in H. binoei derives from multiple hybridizations
rather than from new mutations arising after hybrid for-
mation. By contrast, study of the gene encoding cytochrome
b in Caucasian rock lizards suggested that a single hybrid-
ization event, involving a female Darevskia (formerly
Lacerta) valentini and a male Darevskia raddei, gave rise
to two different unisexual species, D. sapphirina and D.
bendimahiensis [25]. Subsequent divergence of clonal off-
spring from the original hybrid female eventually led to the
recognition and description of two phenotypically-distinct
species.
In parthenogenetic Aspidoscelis lizards, established
species show little evidence of originating from multiple
hybridization events. For example, A. neomexicana
(Figure 1) arose as a hybrid between sexual A. inornata
and A. tigris [26], and the histocompatibility (i.e. ability to
exchange skin grafts without rejection) of individuals from
populations many miles apart suggests that this parthe-
nogenetic species is monoclonal [27]. Even a widely dis-
tributed species such as diploid A. tesselata, which occurs
from southwestern Texas completely across New Mexico
and into southern Colorado, seems to have originated from
a single hybridization event [28]. The evidence of very
minimal genetic differences among some populations
()TD$FIG][ Review
TRENDS in Genetics
Figure 1. The parthenogenetic species Aspidoscelis neomexicana (center) arose
from a hybridization event involving a male A. inornata (bottom) and a female A.
tigris (top). (Photograph by William B. Neaves).
within A. tesselata are attributed to mutations occurring
after the species originated. For example, two phenotypi-
cally-distinct lineages of A. tesselata occur together at a site
in New Mexico, but critical examination of histocompati-
bility among these lizards confirmed their origin from a
single hybrid progenitor [29].
The sole exception to hybrid origins among parthenoge-
netic lizards has emerged from a study of 14 microsatellite
loci in an all-female population of tropical night lizards. No
heterozygozity was found in Lepidophyma flavimaculatum
and greatly reduced heterozygosity was observed in anoth-
er all-female species (Lepidophyma reticulatum) compared
to related sexual species [18]. Clearly, the genetic variation
present in unisexual Lepidophyma does not conform to the
results expected if two separate genomes inherited from
different parental species combined in a hybrid. Although
parthenogenesis could indeed have arisen without hybrid-
ization in Lepidophyma, the greatly reduced or completely
absent heterozygosity in the two unisexual species could
have an alternative explanation. For example, a meiotic
mechanism involving bypass of the second meiotic division,
or fusion of the second polar body with the egg nucleus,
would cause homozygosity at most loci in subsequent
generations even if a lineage arose through hybridization
[()TD$FIG]
Premeiotic endoreplication
Sister chromosome
pairing
Oogonial fusion
Figure 2. Parthenogenetic animals generate oocytes with unreduced chromosome content by undergoing meiotic divisions with twice the number of chromosomes compared
to sexual species. Doubling of chromosomes occurs either by two rounds of replication without intervening mitosis, or by fusion of two oogonia. Homologous pairing occurs
between sister chromosomes instead of between homologs, and this is a key divergence from normal meiosis that permits the maintenance of heterozygosity over many
generations. At each meiotic division half the DNA is extruded to form a polar body. At the second meiotic division the first polar body also divides.
Trends in Genetics March 2011, Vol. 27, No. 3
and was initially endowed with high levels of heterozygos-
ity. Such mechanisms of ploidy restoration have been
described in cases of facultative parthenogenesis [30]
(see below).
In general, where distinct sexual species have hybridized
to form parthenogenetic or gynogenetic lineages, many
hybrids were produced but relatively few gave rise to new
species. Does this mean the ovaries of most interspecific
hybrids fail to undergo the modifications required for clonal
reproduction? Or does it mean that very few clonally-repro-
ducing lineages among those generated by hybridization are
capable of establishing themselves in nature?
The creation of hybridogenetic Poeciliopsis lineages in
the laboratory enabled examination of the fate of unisexual
populations arising from repeated hybridization events
between sexual progenitor species, and has provided an
explanation for the relatively low clonal diversity within
some all-female vertebrate species [31]. Most of 33 labora-
tory-generated unisexual hybrid strains had a higher inci-
dence of birth defects and lower survival rates than either
of the sexual progenitor species or of two unisexual strains
found in nature. However, a few of the synthetic unisexual
strains exhibited fitness characteristics comparable to
their sexual ancestors and to natural unisexual strains,
leading to the suggestion that successful unisexual
lineages result from selection of the most fit clones from
a broad spectrum of genotypes that arise from hybridiza-
tion events.
Ovarian mechanism of parthenogenesis
The oocytes of a diploid sexual species enter meiosis with
four copies of each chromosome, and after two meiotic
divisions the mature egg contains one copy of each. Most,
if not all, persistently unisexual vertebrates appear to rely
on doubling of chromosomes in egg-producing cells prior to
meiosis [13,32–36]. Doubling the number of chromosomes in
the cells that will become eggs, such that eight copies are
present instead of four, enables the production of eggs with
the complete somatic chromosome complement of the moth-
er without abandoning the meiotic program (Figure 2).
Meiosis I Meiosis II
TRENDS in Genetics
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Review
A diploid parthenogenetic species can acquire eight
instead of four sets of chromosomes in its premeiotic
oocytes by one of two pathways. One is chromosome du-
plication without cytokinesis, a process known as endomi-
tosis or endoreplication [37]. Alternatively, 8N oogonia
can arise by fusion of two diploid germ cells. For decades
researchers have assumed that endomitosis causes the
doubling of chromosomes in premeiotic oogonia of parthe-
nogenetic vertebrates, but the actual process has not been
documented. Discerning the mechanism of chromosome
doubling in parthenogenetic ovaries will be crucial to
determining the regulatory process that governs parthe-
nogenesis.
It should be clear that successful establishment of a
parthenogenetic species requires more than ovulation of
eggs carrying the somatic chromosome complement.
Chance, ecological opportunity, and competition with sym-
patric species all influence the prospects of an interspecific
hybrid, even when it is endowed with parthenogenetic
reproductive competency. The preservation of heterozygos-
ity is widely viewed as a key prerequisite for the ecologic
success of all-female species.
Maintaining a high degree of heterozygosity depends
strictly on how premeiotic bivalents form. If homologous
chromosomes associate to form bivalents, crossing-over
and independent assortment during meiotic divisions will
result in gradual loss of unique alleles in the discarded
polar bodies. Over time, the original hybrid genome will
trend toward homozygosity. Premeiotic doubling of chro-
mosomes in parthenogenetic species provides the opportu-
nity to form bivalents between sister chromosomes such
that heterozygosity is preserved from generation to gener-
ation. This mechanism was suggested several decades ago
[34,35,38], but the technology to distinguish unequivocally
between sisters and homologs has only recently been de-
veloped and employed [13,36]. It is now clear that pairing
and exchange does indeed occur between genetically-iden-
tical sister chromosomes, but how cells faithfully distin-
guish identical from highly similar chromosomes remains
unclear.
By preventing the loss of alleles in discarded polar
bodies, this mechanism of unisexual reproduction exposes
the species to the accumulation of deleterious mutations, a
phenomenon known as Muller’s ratchet that has been
viewed as a significant barrier to the long-term survival
of asexuals [39]. However, even when meiosis has been
modified such that no alleles are lost in polar bodies,
asexual species can still eliminate deleterious mutations
through the demise of those individuals or lineages bur-
dened with them. If an allele is sufficiently deleterious, it
will be eliminated by the failure of its carrier to survive or
reproduce. If not immediately detrimental to survival or
reproduction, a deleterious allele nevertheless cannot be
shared with individuals in the population other than the
clonally produced offspring of the individual in which it
originated. In the case of a beneficial mutant allele, it can
become widespread in the species through the superior
fitness it bestows on its carriers. Within an asexual species,
those clonal lineages that have accumulated beneficial
mutations could be expected to dominate and even enable
the species to evolve.
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Other requirements for successful parthenogenesis
If oogenesis is modified such that eggs carrying the unre-
duced somatic chromosome complement are ovulated and
loss of heterozygosity is avoided, what more is required to
induce such an egg to undergo embryogenesis? Vertebrate
oocytes arrest maturation at metaphase of meiosis II, a
state known as cytostatic factor (CSF) arrest, which nor-
mally persists until fertilization [40]. Fertilization of an
egg by a sperm causes a transient elevation of intracellular
calcium that releases meiosis II from CSF arrest [41]. All
unisexual teleost fish depend on sperm from a donor male
to activate embryo development [15]. Indeed, no unisexual
anamniote can initiate embryogenesis unless a sperm from
a sympatric sexual species penetrates the egg, even if the
sperm DNA makes no genetic contributions to the devel-
oping embryo such as the case in gynogenetic species.
At the very least, the contribution of sperm to the
initiation of embryogenesis in gynogenetic vertebrates
involves releasing arrest of meiosis II. Gynogenic lineages
could also rely on donor sperm to provide centrioles for the
formation of the centrosomes that support orderly mitosis
in proliferating cells of the developing embryo. In most
animals, maternal centrosomes do not survive meiosis; a
fertilizing sperm must bring to the egg not only a haploid
chromosome complement but also a pair of centrioles in its
basal body to generate the centrosomes needed for cell
division. Whether the need for centrioles explains the
sperm-dependence in anamniotes remains unclear. The
existence of true parthenogenesis in reptiles clearly con-
firms that such requirements can be overcome in verte-
brates. In parthenogenetic insects, the cytoplasm of
mature eggs has the potential to form functional centro-
somes without pre-existing centrioles [42,43]. Spontaneous
assembly of centrosomes in mature eggs of sexually repro-
ducing Drosophila is blocked by an undefined control
mechanism, but this block is released in parthenogenetic
strains [44]. How the seemingly strict requirement for
sperm among fish and amphibians has been overcome in
parthenogenetic lizards remains one of the biggest mys-
teries in the field.
Elevation of ploidy and genetic diversity
Ploidy elevation is considered to be an important evolu-
tionary mechanism to compensate for the disadvantages of
unisexual reproduction, particularly when ploidy is elevat-
ed through hybridization that adds a genome from another
species [45]. Such a saltatory increase in heterozygosity
provides the lineage with a new genetic repertoire that
could permit adaptation to a changing environment and
the exploitation of new ecological niches.
Adding haploid genomes through hybridization with
sexual males has elevated the ploidy of most parthenoge-
netic Aspidoscelis species [2]. Indeed, the presumed diploid
parthenogenetic precursors of several triploid species no
longer exist in nature, a circumstance indicative of a
selective advantage imparted by the additional genome.
Based on field observations and laboratory studies, hybrid-
ization events that superimpose a haploid sperm on a
parthenogenetic egg frequently produce viable offspring,
but establishment of a new clonal lineage with elevated
ploidy appears to be exceedingly rare in this genus.
Review
It therefore appears that most Aspidoscelis sperm carry a
dominant inhibitor of parthenogenetic reproduction that
causes infertility in the hybrids. By contrast, ploidy eleva-
tion does not cause sterility in many gynogenetic and
hybridogenetic species.
The role of ploidy elevation in the persistence of unisex-
ual species is particularly apparent in ambystomid sala-
manders, a notably ancient lineage. In habitats
surrounding the Great Lakes, unisexual ambystomid sal-
amanders employ a reproductive mode once thought to be
gynogenesis but now viewed as much more complex [14].
All unisexuals in this genus depend on sperm from a
sympatric sexual species to trigger embryo development
in their eggs. Some lineages, particularly triploids harbor-
ing three haploid nuclear genomes from two or three sexual
species, can produce clonal offspring without any genetic
contribution from the sperm that activates development
[21,46]. In such instances, reproduction occurs by typical
gynogenesis. However, the nucleus of a sperm so used
sometimes fuses with the egg nucleus to produce offspring
with elevated ploidy. In many natural populations, incor-
poration of the haploid sperm genome with the unreduced
triploid genome of the egg produces tetraploid individuals.
Some of these can carry the process to the next level and
produce pentaploid offspring [47]. The variation in ploidy,
and the fact that genomes from different males are spo-
radically incorporated, generate a notable degree of genetic
diversity within kleptogenic salamander populations.
The chromosomes contributed by each parental species
in triploid ambystomatid salmanders can be distinguished
by genome in situ hybridization. Such analysis led to the
realization that recombination events between non-homol-
ogous chromosomes have occurred and persisted across
generations [48]. Recombination between similar sections
of different chromosomes is referred to as homeologous
recombination and its occurrence during meiosis over-
comes the clonal integrity of the lineage and introduces
an unexpected source of genetic diversity. However, fur-
ther examination of the incidence of intergenomic
exchanges failed to find any evidence of homeologous
bivalents in over 100 preparations of lampbrush chromo-
somes, leading to the conclusion that homeologous recom-
bination is a rare event [36]. In the animals studied,
chromosomes with inherited intergenomic exchanges
appeared to form bivalents only with their sister copies,
lending support to the historic assumption that duplicated
premeiotic chromosomes pair with themselves instead of
with homologs [34]. However, a small number of quadri-
valents formed from pairs of homologous bivalents were
detected [36]. This observation suggests that recombina-
tion between homologous chromosomes can routinely occur
at low frequency and, if so, would also contribute to genetic
variation among the offspring of unisexual salamanders.
DNA fingerprinting technology provides greater sensi-
tivity for detecting genetic variation than allozyme analy-
sis. Applying this technique to parthenogenetic rock
lizards revealed a surprising degree of genetic diversity
within parthenogenetic populations [49,50]. Whether di-
versity arises from multiple hybrid origins, post-formation
mutations, or low levels of genetic recombination remains
to be determined. The rapid expansion of gene sequencing
Trends in Genetics March 2011, Vol. 27, No. 3
Box 2. Reproductive plasticity in vertebrate evolution
Unisexual reproduction might not be merely a short-term adaptive
strategy. Examples are now known that have persisted for millions
of years, as in the ambystomid salamanders [12,68,69]. Close study
of such instances has revealed surprising mechanisms for adding,
replacing, and recombining genomes from different sexual species
to increase and renew genetic diversity in unisexual lineages [46].
As more becomes known about the genetic mechanisms that enable
them to persist over many generations, sex retains a pivotal role in
their heritage and provides the means for further speciation through
subsequent hybridization between sexual males and clonally
reproducing females.
In turn, unisexual reproduction could influence the long-term
evolution of a genus if genomes of unisexuals eventually find their
way back into sexually reproducing species as reported in a
complex of cyprinid minnows [1]. Theoretical considerations lend
credibility to this possibility and suggest that occasional episodes of
sexual reproduction in an otherwise parthenogenic species could
offer all the advantages of sexuality without its costs [70]. Evidence
from several unisexual vertebrate taxa supports the interaction of
asexual and sexual reproductive modes. These instances include
the role of unisexual lineages in the introgression of genes from one
sexual species to another [71], and transitioning through symme-
trical polyploids from asexual to sexual reproduction [72].
technology and its application to unisexual species and
their sexual progenitors should soon provide estimates of
recombination between homeologous and homologous
chromosomes, respectively, as well as enable determina-
tion of the rates of point mutation, insertions and deletions,
and quantification of the activity of transposable elements
[51]. As more evidence of genetic diversity within unisexu-
al taxa emerges, the idea that parthenogenesis is an
evolutionary dead-end will require further examination
(Box 2).
Facultative parthenogenesis
For many decades, biologists have recognized obligatory
parthenogenesis as the persistent reproductive mode of
several vertebrate species. But even in sexually reprodu-
cing species, unfertilized eggs can sometimes undergo
spontaneous embryo development and give rise to viable
individuals. The capacity for such facultative parthenoge-
netic reproduction, even though rarely expressed, could be
advantageous if unmated females encounter situations in
which males are absent.
Recognition of the occurrence of facultative partheno-
genesis depends on reliable records of isolated females in
captivity that produce offspring without male contact and
on genetic marker technology to document the identity of
mother and offspring [52]. Facultative parthenogenesis
has been documented in taxa that otherwise accommodate
few or no persistently parthenogenetic species. Recent
examples documented with DNA fingerprinting or micro-
satellite genotyping of mother and offspring include sharks
[53,54], several species of snakes [55–58], and varanid
lizards [30,59].
In all but one case [60] the meiotic mechanism of facul-
tative parthenogenesis differs from that found in persis-
tently parthenogenetic species. The diploid chromosome
complement in the egg is restored either by failure of the
second meiotic division, or by fusion of the second polar
body with the egg nucleus, both mechanisms that can
result in homozygosity. Indeed, offspring produced by
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facultative parthenogenesis have only maternal alleles
and, in all but one case where genetic analysis was con-
ducted, they were homozygous at all loci.
For example, parthenogenetic reproduction in a hammer-
head shark heterozygous at three of four genotyped micro-
satellite loci resulted in a pup that was homozygous for
maternal alleles at all four loci [54]. An unmated requiem
shark found to be heterozygous at three of five genotyped
microsatellite loci produced an embryo that was homozy-
gous at all five loci [53]. Similar results came from parthe-
nogenetic offspring of a virgin bamboo shark; the mother
was heterozygous at four of ten microsatellite loci whereas
the two offspring were homozygous at all ten loci [61].
The unusual case that implicated a different meiotic
mechanism was a Burmese python at the Artis Zoo in
Amsterdam that produced seven embryos after at least
five years without contact with a male [60]. DNA polymor-
phism analysis showed identical fingerprints in all the
embryos, and all markers found in the embryos were
present in the mother, supporting the suspicion that the
embryos were produced parthenogenetically. However, the
seven Burmese python embryos were all females. In other
instances of facultative parthenogenesis in snakes, the
offspring were males, a result consistent with the ZW
chromosomal sex determination system operative in all
snakes [62,63] and the view that WW embryos are gener-
ally unviable. This instance of facultative parthenogenesis
could have involved a meiotic mechanism capable of clonal
reproduction. However, a recent report of facultative par-
thenogenesis in a female Boa constrictor of the closely
related Boidae family suggests that alternative explana-
tions must still be considered [64]. The study examined 22
fatherless offspring, and all were highly unusual WW (or
WO) females (not WZ as is typical). By being homozygous
or hemizygous for one or the other of two maternal alleles
at a number of loci for which the mother was heterozygous,
the offspring revealed their lack of genetic identity with the
mother and with each other.
So far, no instances of facultative parthenogenesis have
been detected in captive mammals. However, unfertilized
eggs of confined domestic fowl do sometimes undergo par-
thenogenetic development, and viable offspring have been
produced [65,66]. The absence of spontaneously occurring
parthenogenesis in mammals could be explained by the
dependence of normal in utero mammalian development
on genomic imprinting that governs the differential expres-
sion of parental alleles during embryogenesis. By engineer-
ing appropriate expression of selected parental alleles in
mouse oocytes made by serial nuclear transfer from a non-
growing oocyte with a deletion affecting a paternally
imprinted locus and a fully grown oocyte that already has
the maternal imprint, the pattern of differential genomic
imprinting was mimicked. A female parthenote was pro-
duced that developed to adulthood, mated with a normal
male mouse, and delivered viable offspring [67].
The formidable intervention required to create parthe-
nogenetic mice emphasized the improbability of unisexual
reproduction occurring naturally in mammals. By con-
trast, it seems likely that facultative parthenogenesis
might occur in nature among lower vertebrates. However,
this would have been virtually impossible to detect in
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Trends in Genetics March 2011, Vol. 27, No. 3
natural populations until the recent development of
DNA fingerprinting and microsatellite genotyping technol-
ogies. Even with these new technologies, applying them on
a scale sufficient to detect isolated cases of unisexual
reproduction would be a difficult task.
Concluding remarks
Interspecific hybridization has played an overwhelmingly
dominant role in the origin of parthenogenetic vertebrate
lineages, and additional rounds of hybridization have gen-
erated polyploid lineages with increased genetic diversity
by combining the haploid genomes of multiple sexual
species. Most persistently clonal vertebrate lineages ovu-
late unreduced eggs and sustain high levels of heterozy-
gosity inherent in their hybrid origin. Whether premeiotic
doubling of chromosomes occurs by endomitosis or by
fusion of oogonia has not been determined, and this must
be known before its regulation can be probed. This ranks
high among questions to be resolved by future research
(Box 3).
Large biological returns should come from research on
cellular regulatory changes that facilitate the mechanisms
of parthenogenetic oogenesis. Even in vertebrate taxa that
do not accommodate obligate parthenogenetic lineages,
rare and sporadic asexual reproduction can occur. The
existence of facultative parthenogenesis encourages the
search for regulatory switches that enable it.
Analysis of DNA polymorphisms and microsatellite
genotyping have already begun to clarify the origin and
genetic diversity of unisexual vertebrates, and these tech-
nologies will afford a wealth of insights during the decade
ahead. The field merits watching closely as the application
of genomic technology brings new understanding to a mode
of reproduction previously viewed as an insignificant curi-
osity. Whether unisexual reproduction represents a dead-
end or is an important element in vertebrate evolution
Box 3. Outstanding questions
 What is the mechanism of chromosome doubling in egg-
producing cells prior to meiosis in clonally reproducing verte-
brates? Most researchers in the field have assumed that
endoduplication of chromosomes occurs in oogonia or premeiotic
oocytes, but the same result could arise from fusion of ovarian
cells before entering meiosis. Chromosome doubling could be the
pivotal event that facilitates parthenogenetic reproduction, and
discerning how it is triggered in vertebrate ovaries makes the
determination of its mechanism a high priority for future research.
 Why are reptiles unique among unisexual vertebrates in produ-
cing eggs that do not require sperm to initiate embryo develop-
ment? Other unisexual vertebrates ovulate unreduced eggs
carrying the full somatic chromosome complement of the mother,
but they depend on sperm to stimulate embryogenesis.
 What triggers facultative parthenogenesis in sexually reproducing
species? In some sexual fish and reptiles, females denied contact
with conspecific males will eventually ovulate eggs that develop
spontaneously to produce offspring carrying only maternal
alleles. Nothing is yet known of the behavioral, hormonal, or
neurological induction of facultative parthenogenesis.
 Can genetic material from unisexual lineages find its way back
into sexually reproducing species? If so, unisexuals could serve as
conduits for introgression of genes from one sexual species to
another, and they could bring adaptive mutations accumulated
during episodes of asexual reproduction back into the sexual
mainstream.
Review
remains an unresolved question with important implica-
tions.
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