Molecular Reproduction & Development 78:3–8 (2011)
Polar Bodies—More a Lack of Understanding Than a
Lack of Respect
SAMUEL SCHMERLER1AND GARY M. WESSEL2*
1Department of Ecology and Evolutionary Biology, Brown University, Providence,
2Department of Molecular and Cellular Biology, Brown University, Providence,
Polar bodies are as diverse as the organisms that produce them. Although in many
animals these cells often die following meiotic maturation of the oocyte, in other
highlight some of this diversity and summarize the evolutionary basis for their utility.
Mol. Reprod. Dev. 78: 3–8, 2011. ? 2010 Wiley-Liss, Inc.
Received 8 October 2010; Accepted 17 November 2010
* Corresponding author:
185 Meeting Street, Box G-SFH
Providence, RI 02912.
Grant sponsor: Supported by NIH,
number: RO1 HD28152.
A polar body is the byproduct of an oocyte meiotic
division. It is the small cell that normally apoptoses, and in
textbook figures, it usually just disappears. This portrayal,
though, does not do the cell justice.
Polar bodies typically form by asymmetric cytokinesis:
cytosol and organelles are shunted into the secondary
oocyte during meiosis I, and then into the egg in meiosis
II (Fig. 1A). This leaves the ovum’s sister and aunt (or
cousins, if the first polar body also undergoes meiosis II)
with relatively little cytoplasm, so in most organisms, these
polar bodies simply degenerate. The polar body of human
oocytes, for example, apoptoses in 17–24hr following its
formation, and the resulting fragments remain entrapped
within the zona pellucida (Longo, 1997). Polar bodies were
first reported in 1824 by Carus in gastropods, but their role
was not clarified until the work of Butschli in 1875, Giard in
1902). These structures were often confused with egg
fragments or expelled yolk masses, but were eventually
referred to as directional bodies (or Richtungskorper), a
The common names ‘‘polocytes’’ and ‘‘polar bodies’’ derive
from their polar position in the eggs (e.g. Fig. 1B).
Some may not consider the polar body to meet the
standards ofa cell, but indeedit does. Human polar bodies,
for example, have a nucleus, ribosomes, Golgi, mitochon-
dria and cortical granules (Zamboni, 1970), although the
Abbreviations: DNA, deoxyribonucleic acid; FISH, fluorescence in situ
hybridization; PGD, preimplantation genetic diagnoses.
products and their descendent
cell lineages pertains to some of
evolution’s most vexing
questions . . .
? 2010 WILEY-LISS, INC.
twins may even result when one spermatozoa fertilizes the
ovum and a second sperm fertilizes its sister polar body
of the second (haploid) polar body have been reported
(Machin, 2009), but clearly polar bodies have cellular and
Human polar bodies have become increasingly impor-
tant clinically for human disease assessment, and as me-
trics of embryonic potential. For example, the polar body is
currentlybeing used as a DNA source representative of the
oocyte for genetic testing (Fig. 1B) (Verlinsky et al., 1997,
1999). Removal of one or both polar bodies resulting from
meiotic divisions I and II enables testing of various genes
Figure 1. Diversity of polar body function and fate in various organisms. A: Diagrammatic representation of the meiotic process of the oocyte
(large line) and the sequential formation of the polar bodies with reductive DNA divisions. Shown in blue are the four sister chromatids of one
reveal genetic abnormalities inherent within the oocyte. RNA detected by qPCR may be used to reflect genetic and epigenetic activity to reveal
additional oocyte functionality. C: Many insects develop by parthenogenic activation. Amongst the great diversity of this developmental
mechanism are cases of polar body fusion with the egg. This creates a diploid cell and activation of development. D: In scale insects, the polar
bodies survive and form the bacteriome, an essential nutrient structure of the adult. To construct the bacteriome, the polar bodies first fuse with
of maternally derived bacteria that is needed by the adult to convert the sugary sap diet into amino acids and other essential nutrients. E: In the
and the supporting endosperm tissues. Shown is one example in which the polyploid endosperm forms bynuclear fusion of the meiotic products
i.e. equivalent to a polar body, with each other and with one of the sperm at fertilization.
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SCHMERLER AND WESSEL
and transcripts by qPCR or by fluorescence in situ hybrid-
ization (FISH). Such preimplantation genetic diagnoses
(PGD) enable predictive characters for Mendelian disor-
in which a blastomere is removed from the embryo for
as a predictor for the oocyte in tests for embryonic viability
(Klatsky et al., 2010).
But in many other organisms, polar bodies are not
dispensable. They are not simply waste bins for three-
and they do not disappear following meiosis.
Though we are most familiar with animals in which
sperm–egg fusion initiates development, diversity is the
way of life. Many animals begin development instead
is, without incorporation of a sperm genome (Fig. 1C).
Indeed, animals use multiple mechanisms of parthenogen-
form of developmental activation, a haploid pronucleus
forms in the egg along with one or two haploid polar body
nuclei. Following completion of meiosis, two nuclei fuse to
restore the somatic number of chromosomes, either the
diploidy was first observed in 1889 by Hertwig in parthe-
nogenic starfish eggs (see Korschelt and Heider, 1902). In
animals, polar bodies participate in four basic mechanisms
to restore the 2n chromosome content in parthenogenic
organisms. These are: (1) the second polar body (haploid)
fuses with the haploid oocyte pronucleus; (2) the second
polar body (haploid) fuses with a haploid daughter nucleus
from division of the first polar body (diploid); (3) a daughter
nucleus from division of the first polar body fuses with the
parthenogenic animals employ one of these mechanisms
for egg activation and restoration of chromosome number
(Strand and Grbic, 1997).
In other animals and some plants, polar bodies give rise
to vital tissues that protect and nourish the embryo. These
apparent ‘‘oddities’’ reveal the diverse mechanisms used
during reproductive development and may even allude to
the origins of meiotic strategies. In the least,they challenge
our understanding of sibling rivalry and cooperation by
collapsing these interactions within a single chimeric
entity—that is, an ‘‘organism’’ with nuclei, cells, or even
tissues of nonidentical genomes. After all, the essence of
meiosis is genetic recombination, so that each meiotic
division produces a distinct sibling. Embryos that retain
their polar bodies during development thus have two or
more different genomes; the degree of difference depend-
ing on the extent of cross-over between chromatids. Yet
despite their genetic disparities, discrete cell lineages
may coexist intimately. Diversity in the determination of
developmental fates in meiotic products’ illustrates the
complexity of these relationships.
POLAR BODY FORMATION OF A NUTRITIVE
The polar bodies of some scale insects (family: Diaspi-
didae, which includes many agricultural pests; see Fig. 2A)
actually live full and productive, if downright bizarre, lives
(Normark, 2004a; see Fig. 1D). Rather than degenerating
after meiosis, they fuse together into a single triploid cell.
thus pentaploid, containing three maternal DNA chromo-
chromosome set from the developing embryo, and one
chromosome set from the sperm DNA acquired at fertiliza-
tion. The pentaploid cells proliferate to form a structure
called the bacteriome, and the developing embryo sur-
rounds and incorporates this structure into the larvae. The
bacteriome then becomes an ‘‘organ’’ housing endosymbi-
otic bacteria necessary for the insect’s nutrition.
The mature scale insect is thus chimeric: a pentaploid
bacteriome within a normal haplo-diploid body (males lose
their paternal genome as they develop; Ross et al., 2010).
Figure 2. A: An adult female armored scale insect (Quadraspidiotus juglansregiae) with its protective scale removed; (B) an adult female
parasitoid wasp (Copidosoma floridanum) laying its egg into that of its host, the cabbage looper moth (Trichoplusia ni); (C) adult onions
(Allium cepa). Photo credits: (A) Benjamin B. Normark, (B) Michael R. Strand, (C) Ranier Haessner.
Mol Reprod Dev 78:3–8 (2011)
POLAR BODY DIVERSITY
No other adult animals live as obligate chimeras (Normark,
2004a,b). What’s going on here?
One explanation interprets this chimerism as a strategy
for gender crypsis, that is, preventing detection of the
maternal or paternal genome (Normark, 2004a,b). Scale
insects rely on their bacterial endosymbionts to manufac-
ture amino acids that are lacking in their own diet of sugary
ing bacteria in males are, evolutionarily, as good as dead.
So some bacterial lineages have evolved to suicidally kill
any male embryos they find themselves in, in order to free
up resources for the dead males’ sisters and their endo-
symbionts (Hurst, 1991; Majerus, 2003; Normark, 2004c).
Scale insects may use their pentaploid bacteriomes to
each bacteriome always contains two full copies of its
mother’s diploid genome and one full copy of its father’s
haploid genome, preventing the bacteria inside from deter-
mining the sex of their host.
POLAR BODY FORMATION OF A PROTECTIVE
Polar bodies play a similarly vital role in the life cycles of
Copidosoma floridanum (Fig. 2B) and some other parasit-
oid wasps (Strand and Grbic, 1997; see Fig. 1E). Develop-
ment in these insects begins when the adult deposits its
eggs into an egg of the cabbage looper moth, Trichoplusia
ni. It is within this other egg and its subsequent caterpillar
that the parasitic wasp embryos and larvae will develop,
eventually killing their host. The wasp egg has a distinct
polarity and is enclosed within a thin chorion. During early
development, the polar body nucleus separates from the
egg’s pronucleus, and migrates to the future anterior of the
embryo. This polar body remains viable and forms a polar
body cell. Within this cell, the polar body nucleus divides
without cytokinesis to form a syncytial compartment at the
anterior of the egg that eventually migrates as an extraem-
bryonic tissue surrounding the dividing blastomeres. The
embryo then ruptures out of its chorion and continues
development, now enveloped by the polar-body-derived
extraembryonic structure. This polar-body-derived tissue
system. Crucially, it also organizes embryo proliferation in
these wasps, subdividing the original embryo into multiple
embryos, each of which develops autonomously from the
others within its own polar-body-derived sheath. The polar
body tissue invades divisions between the embryos and
separates them from each other, leading even to differenti-
ation between larval castes (Strand and Grbic, 1997). And
this extraembryonic tissue may also play a role in kin
recognition, allowing the sterile, precocious soldier larvae,
which kill embryos from other wasp eggs, to spare their
siblings in the later-forming reproductive caste. C.
about 10 days, and during that time it seems to dominate
most aspects of embryonic development.
POLAR BODIES AND THE PLANT’S ENDOSPERM
Parasitoid polyembryonic wasp larvae, the genomic
contortions of scale insects’ bacteriomes, and those par-
early development. Fair, we agree. However we are all
intimately dependent on a similarly strange entity—the
endosperm. The seeds of flowering plants—largely
and humanity. Cereal grains, the endosperm tissues of
domestic grasses, provide about half the world’s calories
plants originate during double fertilization: one spermato-
cyte of the plant pollen fertilizes the ovum while his twin
fuses with two, four, or more syncitial nuclei of the central
cell (part of the female gametophyte). In most taxa—over
70% of those studied embryologically, and likely in the
common ancestor of all angiosperms—these nuclei are
sister to the ovum (Williams and Friedman, 2004; Rudall,
2006). But in onions (Allium cepa; Musial et al., 2005; Fig.
2C), black pepper (Piper nigrum; Kanta, 1962; Madrid and
Friedman, 2009), and many other angiosperms, these
nuclei may descend from two or four distinct meiotic pro-
ducts (Maheshwari, 1948, 1950; Yadegari and Drews,
2004). One central cell nucleus derives from the same
meiotic product as the ovum, but the others descend from
one (or all three) of the polar body nuclei, which are not
segregated by plasma membranes after meiosis (Fig. 1F).
In these plants, the polar bodies’ genomes live on in the
polyploid endosperm—at least until the endosperm is ab-
sorbed by the growing embryo.
Why would some plants call on their polar bodies to
contribute to the endosperm? The evolution of the endo-
sperm is often explained by kin selection (Queller, 1983).
When both nuclei of the central cell are sister to the ovum,
and as the sperm that fertilizes them is the brother of the
sperm that fertilizes the ovum, then the endosperm is
genetically very similar to the embryo (though with an extra
copy of the maternal genome). Because this endosperm is
it may be more likely to sacrifice itself to provision the
embryo, and in angiosperms it has indeed displaced the
female gametophyte from the nutritive role. But when all
four meiotic products of oogenesis contribute nuclei to the
central cell, as in Piper, the endosperm (like the scale
insect’s bacteriome) shares only 40% of its genome with
SO WHAT’S GOING ON?
When coupled with a complete abdication of fitness, the
fraction of the endosperm genome (or extraembryonic
tissue from the parasitic wasp, or the bacteriome of scale
insects) shared with the embryo would confound an expla-
nation based on kin selection. But the polar bodies that
these structures developed from have zero fitness to begin
with. Instead, polar-body-derived nutritive and protective
tissues might be reconceptualized simply as a bizarre form
of maternal provisioning. Selection has favored females
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SCHMERLER AND WESSEL
that co-opt their polar bodies this way because their off-
spring benefit from these tissues. The onion’s endosperm,
the parasitoid wasp’s extraembryonic membrane, and the
scale insect’s bacteriome are not altruistically sacrificing
their fitness; instead, they are manipulated to benefit the
diploid embryo. Nowak et al. (2010) point out in their recent
and controversial paper on the origins of insect eusociality
(the highest level of social organization) that ‘‘descent is
extension of the queen...in each generation. Selection
acts on the traits of the queen and the extrasomatic pro-
jection of her personal genome.’’ Since plant, wasp, and
scale insect polar bodies, even more fundamentally than
Copidosoma’s soldier larvae, will not pass on their genes,
accessories to the germ line. Like ‘‘normal’’ polar bodies,
they are sacrificed to give the embryo a better start in
peting with the diploid embryo, beyond the asymmetrical
fate is determined by more than the absence of apoptotic
mechanisms found in human polar bodies, and instead is a
partitioning of factors that leads to different fates. An alter-
native explanation is that the genome of the oocyte is in
some way different from that of the polar body, leading to
differences in developmental potential. In this regard it is
each case of extended, functional post-fertilization polar
and to low fitness. Since sibling rivalry is all about fitness,
competition between the modified, polar body derivatives
and the embryonic tissues is eliminated. It is, however, not
yet clear mechanistically how this lack of rivalry is commu-
nicated. Sperm undergo meiosis too, but their fates are
strictly as an individual, not as a part of sibling cells in a
developing organism. Improved understanding of the de-
terminants of polar bodies’ developmental fates may offer
insight into the evolutionary forces driving competition and
diseases of pregnancy are apparently due to conflicts
between the genetically distinct tissues of mother and fetus
the differentiation between ovum and polar body is not
necessarily as direct as it seems. Although more limited in
fate than the oocyte and embryo, the polar bodies of these
bizarre examples are capable of developing into complex,
esis. The relationship between meiotic products and their
descendent cell lineages pertains to some of evolution’s
most vexing questions, and polar-body-derived tissues
demonstratethepotential variabilityof thisrelationship.We
thereforeencourageabroader andmorerefinedlook atthe
diversity of polar body development.
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