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Selective Embryo Abortion Hypothesis Revisited ±
G. Korbecka, P. G. L. Klinkhamer, and K. Vrieling
Institute of Evolutionary and Ecological Sciences, Section Plant Ecology, Leiden, The Netherlands
Received: October 9, 2001; Accepted: February 20, 2002
Abstract: Many plant species abort a large fraction of their em-
otypes with a potential low quality later in life such that an in-
bryos. It has often been suggested that embryos of genotypes
crease in the level of abortion leads to an increase in offspring
that would perform worse later in life are preferentially abort-
quality. In evolutionary theory the hypothesis is important in
ed. Such selective embryo abortion would lead to investment
relation to explanations for low seed to ovule ratios and the
of resources only in the offspring with the highest potential fit-
optimal allocation of resources to male and female reproduc-
ness. Many studies have shown that otherwise viable embryos
are aborted. However, only few manipulative studies have in-
deed shown a correlation between the level of abortion and
The SEA hypothesis is based on the following premises: i)
offspring quality and these studies have been challenged for
plants abort a substantial part of the embryos, ii) otherwise
their experimental design. Molecular techniques open new op-
viable embryos are aborted, iii) the probability of being abort-
portunities to study selective embryo abortion. Non-random
ed depends on the genotype of the embryo. In contrast to
abortion at the level of molecular markers can be observed as a
ample theoretical attention given to the SEA hypothesis (e.g.,
deviation from Mendelian segregation: over- or under-repre-
Kozøowski and Stearns, 1989; Latta, 1995; Burd, 1998),
sentation of markers in the offspring. Subsequently, the over-
there are only a few experimental studies in which all condi-
or under-represented markers can be related to offspring quali-
tions, mentioned above, were considered. The SEA hypothesis
ty later in life. We reviewed the literature on the genetic maps
received a lot of attention in the 1980s (Stephenson, 1981;
of intraspecific crosses of wild plant species and the selection
Wilson and Burley, 1983; Casper, 1988; Lee, 1988; An-
of cultivated species. The level of non-Mendelian segregation
dersson, 1990; Andersson, 1993) but, probably due to diffi-
we found in these maps is high. On average, 11.5% of the tested
culties with the interpretation of the results of experiments in
markers in the genetic maps of wild species and 14.6% in the
which the abortion level was manipulated, empirical research
cultivated ones, show a departure from Mendelian segregation.
on the topic has drastically reduced. Most of these problems
From six studies, providing sufficient data, it was calculated
can now be overcome using molecular techniques. In this pa-
that in 68% of loci segregating in non-Mendelian fashion post-
per we review the work on this hypothesis and discuss the
fertilization selection is involved. We propose that the devia-
possibilities and difficulties that are presented by the use of
tion from Mendelian segregation can be partly explained by se-
molecular methods to shed new light on the topic.
lective embryo abortion. We describe an experimental design
that allows for attributing selective embryo abortion to the
In crossings, SEA shows up as a deviation from Mendelian seg-
non-Mendelian segregation that is found in a genetic map.
regation for some molecular markers. We will review data on
the genetic maps of plants to judge whether there is a potential
Key words: Selective embryo abortion, non-Mendelian segrega-
for SEA to be detected by means of marker segregation analy-
tion, distorted segregation, genetic maps, seed±ovule ratios,
sis. However, SEA is not the only mechanism leading to devia-
tion from Mendelian segregation. We will discuss how we may
distinguish SEA from other mechanisms that include, e.g.,
meiotic drive, gametophytic selection, and seedling death.
Selective embryo abortion (SEA) is the phenomenon that some
Two explanations have been proposed for the selective abor-
genotypes are aborted more frequently than others. The Selec-
tion of particular genotypes: 1. Maternal control, 2. Embryo
tive Embryo Abortion hypothesis proposes that the fitness of a
female plant can be increased by the selective abortion of gen-
Since, potentially, SEA may be maternally controlled, it has of-
ten been discussed as an aspect of female choice together with
pre-fertilization processes, such as selective inhibition of pol-
Georg Thieme Verlag Stuttgart ´ New York
len germination and pollen tube growth (Wilson and Burley,
1983; Marshall and Folsom, 1991). Theoretically, in an-
Selective Embryo Abortion Hypothesis Revisited ± A Molecular Approach
giosperms maternal control can be through the endosperm,
onic viability is often assessed in relation to early-acting in-
the tissue that nourishes the embryos, because it contains
breeding depression. On the basis of information on seed pro-
two copies of the maternal and one copy of the paternal genes,
duction after selfing and outcrossing, the number of so-called
also abortion may be related to an interaction of the maternal
lethal equivalents is estimated. A lethal equivalent is a lethal
and paternal genome. However, Marshall and Folsom (1991)
gene or a number of deleterious genes that make up one lethal
concluded in their review on mate choice in plants that there is
gene. According to Lynch and Walsh (1998), the number of
little evidence to prove that specific maternal mechanisms
lethal equivalents per gamete affecting early embryonic sur-
produce sorting among compatible donors. The problem with
vival varies approximately from 1.7 to 5.0 for conifers and from
the assumption of maternal control is how the link with off-
0.4 to 0.91 for short-lived angiosperms. However, for consider-
spring quality later in life is brought about, in other words:
ing SEA it is essential to make a distinction between lethal and
how can the mother plant ªknowº which embryos will give
deleterious alleles. If abortion results from recessive lethal al-
the highest fitness contribution? Moreover, it is technically
leles, both the level of abortion and the direction of selection
extremely difficult to experimentally test this hypothesis. If
are fixed. The embryos, which possess lethal alleles, will die
changes in the maternal tissue of the seed (nucellus and in-
irrespective of the conditions they encounter during develop-
teguments) precede changes in embryo and endosperm devel-
ment. In such cases it is not likely that the level of inbreeding
opment, this could point to maternal control. If the order of
depression during seed set will be correlated with the level of
changes is the reverse, this would point to embryo competi-
inbreeding depression later in life. This may explain the ab-
tion (Marshall and Folsom, 1991 and refs. therein). As yet
sence of such a correlation in the studies of Husband and
there is very little evidence to decide for either of the two pos-
Schemske (1995) or Koelewijn et al. (1999). On the other
hand, if the alleles on which embryo abortions depend are de-
leterious, embryo abortion may be selective and depend on the
More generally accepted is the idea that SEA is brought about
conditions the embryo encounters. Remington and OMalley
through competition among embryos. Some embryos may be
(2000) studied early acting inbreeding depression in lob-
better competitors for resources than others, either because
lolly pine (Pinus taeda) using information from a genetic map.
they present a larger sink or they may even release chemical
They estimated that in this species 19 loci have moderately
substances which are most probably indole compounds that
deleterious or lethal embryonic effects. Moreover, most of
inhibit the sucrose uptake of siblings (Mohan Raju et al.,
the alleles reducing viability are recessive and for 3 loci over-
1996; Krishnamurthy et al., 1997; Arathi et al., 1999).
dominance was found. There is also another study (Melser et
In this scenario, maternal ªrecognitionº of the embryos is not
al., 1997) suggesting that embryo abortion may not be a
necessary. The mother plant can influence offspring quality in-
result of action of recessive deleterious alleles. On the basis of
directly by controlling the level of resources and thus setting
comparing seed production after selfing and outcrossing in
the selective arena for the embryos. It has even been suggested
E. vulgare (after sufficient amount of pollen was applied),
that endosperm reduces embryo competition since it is more
they found that some individual plants aborted more selfed
frequently observed in the species with multiovulated ovaries
embryos and others more outcrossed ones. Melser et al.
compared to those with uniovulated ones, and it is found more
(1997) concluded that in E. vulgare the effects of the deleter-
often in the species with multiovulated species that experi-
ence less abortion (Uma Shaanker et al., 1996).
One can imagine that embryo abortion may be influenced by a
However, from an evolutionary ecological perspective, the
number of (mildly) deleterious alleles that each by themselves
mechanism leading to SEA is not as interesting as the fact
have only a small effect and are therefore not easily purged
whether or not it can increase offspring quality. The increase
of offspring quality through SEA would mean that embryo
abortion is potentially adaptive. The correlation between the
In the remaining part of the paper we will first present the
abortion level and offspring quality is, under the assumption
more traditional phenotypic approach to study SEA and then
of embryo competition, brought about by genes that control
we will discuss how molecular techniques can be used to
e.g., basic metabolic processes that are important, both during
embryo development and during later life, or by genes that
have pleiotropic effects. Goldberg et al. (1989) summarize
in their review: ªMore than 90 % of the 15000 diverse mRNAs
present in mid-maturation stage embryos are represented in
both cotyledon stage and fully differentiated, mature embryos.
Most of these mRNAs are also present in post-germination
Flowering plants commonly produce more ovules than seeds.
cotyledons and in the mature plant leaf.º The fact that most
In many angiosperm species ovules may not develop into
of the genes that are expressed in embryonic stage are also
seeds due to pollen limitation (Wolfe, 1983; Zimmerman
expressed later in life, gives ample opportunity for embryo
and Pyke, 1988; and see Burd, 1994 for a review) or be-
abortion to have an effect on offspring quality later in life.
cause they are involved in self-incompatibility mechanisms
(Waser and Price, 1991; Seavey and Carter, 1996). How-
Most evidence for the fact that abortion depends on the geno-
ever, even after successful fertilization, a considerable propor-
type of the embryo comes from studies on inbreeding depres-
tion of the ovules fail to produce seed in many species. Wiens
sion. If selfed embryos have a higher chance of being aborted
(1984) estimated that seed±ovule ratio equals, on average,
than outcrossed ones (Montalvo, 1992; Gibbs and Sassaki,
about 85% for annuals and 50 % for perennials. Wiens data are
1998), this suggests that recessive deleterious or lethal al-
based on developing fruits. If ovules in undeveloped fruits are
leles may influence competitive strength of embryos. Embry-
also included, the seed ovule ratios may be even lower. Dissec-
G. Korbecka, P. G. L. Klinkhamer, and K. Vrieling
tions of ovaries showed that a large fraction of embryos are
produced more leaves, and later in life more inflorescences,
aborted, for example in Prunus cerasus (Bradbury, 1929), Ox-
flowers and matured more seeds compared to the treatment
alis magnifica (Guth and Weller, 1986) and Epilobium angu-
after random destruction of ovules (Stephenson and Winsor,
stifolium (Wiens et al., 1987). Some species show extremely
1986). In a study on patterns of seed abortion in P. cocci-
high abortion rates. In Dedeckera eurekensis, the seed±ovule
neus, Rocha and Stephenson (1991) found that ovules at
ratio equals 2.5%, although about 90 % of the ovaries initiate
the basal end of the ovary are more likely to abort, due to the
growth, indicating that fertilization took place (Wiens et al.,
fact that they lag behind in development because they were
1989). In Asclepias speciosa approximately only 3.8% of the
pollinated later, which may result in reduced nutrient avail-
ovaries develop into mature fruits, although 82.4% of them
ability. Destroying the ovules on the stylar end increased the
were fertilized (Bookman, 1984).
probability of seed maturation on the basal end. The progeny
that resulted from this treatment was significantly less suc-
Gymnosperms also abort many seeds. In Pinus sylvestris on
cessful compared to the control treatment with regard to ger-
average 30% seeds are aborted (Karkkainen et al., 1999).
mination time, vegetative growth, flowering time and number
The level of embryo abortion is, however, higher due to poly-
embryony. The most common form is simple polyembryony
with independent fertilizations of more than one archegonium
Is abortion dependent on embryo genotype?
within the same ovule of which usually only one develops into
a seed (Sorensen, 1982; Willson and Burley, 1983; Haig,
Stephenson (1981) and Lee (1988) show in their reviews
that in many plant species the chance for an embryo of being
aborted depends on factors like time of initiation, position
In some cases it has been argued that embryos are not viable
within ovary, resource availability and pollen source. Even if
because of high genetic load, as in the D. eurekensis example
the level of embryo abortion is high and viable embryos are
(Wiens et al., 1989). However, as we will discuss later, even
aborted, abortions do not necessarily depend on the genotype
viable embryos are often aborted at a very high rate.
of the embryo and may not lead to selection. Both single pollen
donor and mixed pollen donor experiments have been used to
Are potentially viable embryos aborted and
study the relationship between abortion rate and genotype.
does abortion increase offspring quality?
The easiest way to detect selection is when each flower of a
In some species with linearly arranged ovules, developing em-
plant receives pollen from a single pollen donor only. One can
bryos in the basal end of the ovary are more likely to abort.
then compare the siring success of different potential fathers
Nakamura (1988) described a successful in vitro culture of
directly, by counting the seeds in the flowers, without the use
embryos from the basal end in Phaseolus vulgaris. In Dalberia
of genetic markers. With this approach, it is unlikely that pol-
sisso, Ganeshaiah and Uma Shaanker (1988) cut off two dis-
len tube competition influences differences among fathers.
tal seeds and implanted the remaining pod in agar to complete
The disadvantage of single pollen donor experiments is that
maturation of the rest of the seeds. This treatment resulted in
competition among the embryos within a flower cannot be de-
an abortion rate in the basal end of the pod as low as in the dis-
tal end of intact, control pods. Both Nakamura (1988) and
Ganeshaiah and Uma Shaanker (1988) did not relate abor-
Bertin (1982) studied the self-incompatible trumpet creeper
(Campsis radicans) and applied pollen of different fathers and
found that the pollen donors that were favoured by particular
To our knowledge, only four papers present evidence that
recipients were usually those whose pollinations resulted in
abortion can increase offspring quality. These experiments
fruit with many and large seeds. Although prezygotic mecha-
compared offspring quality after natural abortion and after
nims were not all properly excluded, the author concluded that
random thinning of the ovaries. In contrast to the first, the lat-
fruit abortion seems to have been more important in donor
ter is not selective. Species of the family of the Boraginaceae al-
selectivity than prezygotic phenomena.
ways produce four ovules in each flower arranged in equal po-
sitions, in a square. Although pollen is not limiting seed pro-
Most single pollen donor experiments aim at comparing abor-
duction, on average there are fewer than four seeds per flower
tion after self- and outcross pollination, or comparing outcross
found in many species of the Boraginaceae (e.g., Cynoglossum
pollination with close and distant donors. Such comparisons
officinale ± Jong and Klinkhamer, 1989; Echium vulgare ±
are interesting, especially because Husband and Schemske
Klinkhamer et al., 1994 and Cryptantha flava (Casper,
(1996) showed that embryo development is one of the most
1988). In Cr. flava (Casper, 1988) and in Cy. officinale (Mel-
important life stages in which inbreeding depression can act.
ser et al., 2001) the random destruction of three ovules in a
flower resulted in doubling of the chance of maturation for the
For the self-compatible Aquilegia caerulea Montalvo (1992)
remaining ovule, compared to a control treatment with all
found that the abortion rates for selfing were, on average, 38%
ovules intact. This shows that in the control treatment a large
higher compared to abortion for outcrossing, while there were
fraction of the aborted embryos was potentially viable. In Cr.
no significant differences in fertilization rate for both pollina-
flava seeds from the control group with natural abortion
tion types. For E. vulgare, Melser et al. (1997) found that in
showed higher emergence and survival during two years of
some individuals self-pollen was relatively more successful
growth (Casper, 1988). Melser and Klinkhamer (2001)
compared to outcrossed pollen, while in others the outcrossed
found that natural abortion resulted in higher offspring sur-
pollen was more successful. Pollen donors did not differ in pol-
vival in Cy. officinale. In Lotus corniculatus, offspring produced
len viability, pollen germination and pollen tube growth.
after natural embryo abortion showed better germination,
Therefore, Melser et al. (1997) concluded that differences
Selective Embryo Abortion Hypothesis Revisited ± A Molecular Approach
in siring success of different pollen donors were most likely
Crushing ovules does not always reduce abortion levels. One
can explain Caspers (1988) and Melser and Klinkhamers
(2001) results by assuming that the resources not used by
Gibbs and Sassaki (1998) found for Dalbergia miscolobium in
the destroyed ovules are allocated to the remaining ovules
the field that 30.0% of crossed flowers and 3.6% of selfed flow-
within the same flower, thereby increasing the chance for mat-
ers developed mature fruits. This difference was mainly caused
uration. If the experimental treatment is applied to only a part
by abortion of selfed embryos because, in the ovules dissected
of the flowers, it is possible that resources that would be used
4±6 days after pollination, embryos were found in similar fre-
by crushed ovules are divided among all ovules of the plant
quency and condition for both treatments.
and not only among those that remained in the hand-thinned
flowers. In such a case, the difference among the treatments
Marshall and Whittaker (1989) studied effects of identity of
would be small and could go undetected. Perhaps this may at
a pollen donor on offspring quality in Raphanus sativus. They
least partly explain the negative results found in two studies
found significant paternal effect on the number of leaves and
on Anchusa officinalis (Andersson, 1990) and Achillea ptarmi-
weight of offspring after eight weeks of growing in a green-
ca (Andersson, 1993). The difficulties in the interpretation of
house. The effects of pollen donor were more pronounced if
results from the experiments discussed above can be avoided
maternal plants were grown in water stress conditions. Their
if a single treatment is applied to a whole plant and the same
results suggest that the processes that sort among potential
genotypes are used in different treatments (Melser et al.,
fathers during pollination, fertilization and seed filling may
Decreased offspring quality after random crushing of ovules may
Multiple donor experiments, where a mixture of pollen from
be an artefact. In experiments based on ovule destruction, in-
different genotypes is applied to a single flower, combined
ferior offspring do not necessarily result from genetic differ-
with paternity analysis, can also provide information about
ences but may be caused by subtle effects of the mechanical
SEA. The advantage of multiple donor experiments is that se-
damage itself. Casper (1988) cautions: ªPrematurely remov-
lection among pollen donors within flowers can be detected.
ing some reproductive structures might upset initial source±
The disadvantage is that, if it is not possible to analyse aborted
sink relationships and thus plant±resource levels, adversely af-
embryos for their paternity, an appropriate method has to be
fecting seed quality. In addition, forcing a flower to distribute
found to separate the effects of pollen tube competition from
resources to an ovule that it normally would not mature might
SEA. Marshall and Ellstrand (1988) carried out a multiple
itself result in an inferior seed.º Moreover, developmental irre-
donor experiment on Raphanus sativus under stress condi-
gularities of the flower can influence the competitive strength
tions. Early water stress can affect both fertilization and early
seed abortion. In contrast, late water stress can only influence
seed abortion. The contribution to the progeny of the three
An experiment, as described above, is therefore not sufficient
pollen donors differed from the control in the late stress treat-
to prove that SEA occurs. The best way to show that SEA can
ment but not after early stress. Apparently, only late abortions
increase offspring quality in ovule destruction experiments is
provide the opportunity to select in this case.
to collect genetic evidence as well. We will therefore discuss
in the remaining of the paper how molecular data can be used
Attributing the abortion rate to the origin of pollen in some
to overcome the problems caused by the traditional approach
gymnosperms is even easier since they have poorly developed
prezygotic selection mechanisms (Willson and Burley,
1983). For example, Karkkainen et al. (1999) determined
the abortion rate in Pinus sylvestris as a proportion of empty
seeds, because seed coat formation in this species is an effect
If embryo abortion is selective, certain alleles will be under-
of pollination. They found that frequency of abortion increases
or over-represented in the offspring, compared to Mendelian
with the proportion of self pollen applied to the flowers. The
segregation. The upswing in molecular methods in the last
proportion of empty seeds ranges from 23% after outcrossing
decade has led to easy access to abundant molecular markers
in almost every organism (e.g., AFLP). Such molecular markers
might be a powerful tool to detect and assess the adaptive
value of SEA. Using molecular markers avoids the limitation
of pollination experiments because selection among offspring
Missing information about the selection among genetically dif-
of a single pollen donor can be detected. Even if the plant is
ferent offspring sired by the same father. Pollination experi-
self-pollinated, selection among embryos may be observed in
ments can show that selective abortion exists only if siring
the loci for which the parent plant was heterozygous. So far,
success of different fathers is compared, either after single
selection among the offspring of a single father has largely
donor pollination or after mixed donor pollination combined
been ignored. This may have caused an under-estimation of
paternity analysis. Moreover, it is necessary to eliminate that
prezygotic mechanisms that may play a role. The big disadvan-
tage of this approach is that a part of post-fertilization selec-
The second advantage of using molecular markers to test the
tion, which may occur among genetically different offspring
SEA hypothesis is that the presence or absence of alleles that
of the same father, cannot be observed. Only molecular tech-
are under- or over-represented in the offspring, compared to
Mendelian segregation, can be related to offspring perform-
ance in later life. This would be a much better way of assessing
the selective advantage of embryo abortion compared to tradi-
G. Korbecka, P. G. L. Klinkhamer, and K. Vrieling
tional methods, because no manipulations of flowers or plants
artificial selection and inbreeding were minimal. We expected
(e.g., destroying ovules) are needed and because selection can
that in genetic maps of cultivated species non-Mendelian seg-
be directly linked to the genotype of the offspring.
regation is found more often because mapping populations are
often derived from crosses between different inbred line vari-
Selection among embryos can be presented at the level of DNA
eties or come from distinct geographical areas (e.g., Loarce et
as a deficiency or excess of certain genotypes among the off-
al., 1996; Jenczewski et al., 1997; Liu et al., 1997; Qi et
spring that successfully went through seed maturation, com-
al., 1998). It may happen that genes from one inbred line/
pared to expected Mendelian segregation. We reviewed genet-
variety do not function properly when combined with genes
ic maps of plants in order to determine the potential for SEA. If
the percentage of molecular markers showing non-Mendelian
segregation found in genetic maps of plants is as low as ex-
Results of the literature survey are presented in Tables 1 and 2.
pected due to chance alone, we have to conclude that SEA is
The percentage of markers showing non-Mendelian segrega-
not an important process. This argument, however, cannot be
tion differs significantly from 5% for the 59 analysed species
reversed. If many markers show non-Mendelian segregation,
(t = 9.143; df = 58; p < 0.001). It ranges from 0.1±40.82 % (aver-
that could be due to SEA but other selective mechanisms can-
age: 14.6) for cultivars (Table 1) and from 0±41.0% (average:
not be excluded. For instance, meiotic drive and gametophytic
selection can also lead to non-Mendelian segregation (Appen-
dix). The difficulty in distinguishing the cause of non-Mende-
The difference in the average percentage of markers showing
lian segregation is a disadvantage of this method. An appropri-
non-Mendelian segregation between cultivated and wild spe-
ate experimental design should be used to study segregation
cies is not significant (F = 1.099; df = 1,57; p = 0.299).
in plants, with different treatments leading to differences in
the level of abortion, as will be discussed later.
Distinguishing between biological phenomena
Is non-Mendelian segregation common in plants?
Sometimes it is argued that sampling error or irreproducibility
Data about non-Mendelian segregation in plants can be found
of the techniques can be responsible for a high percentage of
in genetic maps. In almost all genetic maps of plants we have
molecular markers showing non-Mendelian segregation. Here
reviewed, authors refer to a statistically significant departure
we will consider the importance of those problems.
from Mendelian segregation as distorted segregation, although
they usually do not present any evidence for the presence of
Inconsistent PCR amplification can cause irreproducibility of
segregation distorter genes sensu Lyttle (1991). Lyttle de-
the method and hence a detection of apparently higher non-
fines segregation distorters as genetic elements that exhibit
Mendelian segregation. RAPD is known as a technique that
meiotic drive. That is why, when we consider a statistically sig-
does not always give fully reproducible results (Jones et al.,
nificant departure from Mendelian segregation, we will use
1997). We therefore compared the level of non-Mendelian
the more neutral term: non-Mendelian segregation.
segregation detected in genetic maps using three techniques:
AFLP, RAPD and RFLP. None of the techniques gave significantly
It is common practice to test, by means of a chi square test at a
higher level of non-Mendelian segregation (paired samples
5% significance level, whether or not segregation of a certain
test results for: RAPD vs. RFLP: df = 10, p = 0.433; RFLP vs. AFLP:
marker deviates from the expected ratio. If all markers are in-
df = 4, p = 0.222; RAPD vs. AFLP: df = 4, p = 0.386), although
herited independently, 5% of all markers should show non-
PAGE gels used in AFLP give much higher resolution than agar-
Mendelian segregation, if no selection occurs. However, it is
ose gels used commonly in RAPDs. Note, however, that the
extremely difficult to determine the expected fraction of mar-
tests are based on a small number of comparisons. The con-
kers showing non-Mendelian segregation under the null hy-
stant warning (e.g., Jones et al., 1997) that RAPDs are not
pothesis, that no selection occurs. Firstly, non-Mendelian seg-
fully reproducible may have caused a severe selection against
regation can be over- or under-estimated when judged from
markers giving non-Mendelian segregation previously used in
the number of loci with a significant non-Mendelian segrega-
mapping. Many authors using RAPD markers for the construc-
tion because, in a distorted region of the genetic map, the den-
tion of a genetic map, only include markers which are effi-
sity of mapped molecular markers may differ from the aver-
ciently amplified and exhibit unambiguous polymorphism.
age. Secondly, an unknown percentage of DNA markers is lo-
Jenczewski et al. (1997) write: ªWhen such precautions are
cated in non-functional regions (e.g., not or loosely linked to
taken, RAPD does not induce higher levels of distortion than
functional regions). For such markers, only non-Mendelian
restriction fragment length polymorphisim (RFLP).º Discard-
segregation due to chance is expected. Nevertheless, Tables 1
ing markers before use in mapping, although to a smaller ex-
and 2 provide useful information because, averaged over all
tent, may have happened in these other techniques as well.
species, the first problem should disappear as we have no rea-
Tables 1 and 2 may therefore underestimate the level of non-
son to assume that the density of molecular markers is higher
or lower in the region where selection occurs. The second
problem can only lead to an under-estimation of selection. Un-
Other sources of artefacts can be homoplasy, which is the am-
fortunately, we do not know the quantitative importance of
plification of two fragments of the same length from non-alle-
lic regions, low resolution of agarose-gels, and co-migrating
and overlapping polymorphic fragments. However, we expect
We searched for genetic maps based on intraspecific crosses of
these explanations to have only a minor influence on the level
cultivated and wild species. Wild species were defined in the
of non-Mendelian segregation. Rieseberg (1996) tested the
broadest sense possible. The basic criterion we used was that
homology of 220 RAPD co-migrating fragments in three close-
Selective Embryo Abortion Hypothesis Revisited ± A Molecular Approach
Table 1 Percentage of non-Mendelian segregation found in genetic maps of cultivated species$
No. of loci showing nMS for each type of marker
$ We have searched for the genetic map of cultivated species using the keywords:
nMS: non-Mendelian segregation, BC: backcross, RIL: recombinant inbred lines, BIL:
ªgenetic mapº or ªlinkage mapº and ªplantºin the journal ªTheoretical and Applied
Geneticsº from volume 93 (year 1996) till volume 97 (year 1998). We used Win-
a % of markers showing nMS only in the map (the number of loci that showed nMS
spirs 2.0 to search in the Current Contents database. The search resulted in 222
and that are not linked in the genetic map could not be retrived from the article),
records. Data from 33 out of 222 papers could be included in the table. A paper
b only markers showing nMS given for the probability level p < 0.01 were presented,
was included if the number of loci with significant non-Mendelian segregation for
c the type of markers that showed nMS could not be indentified in a paper,
the genetic map could be calculated. Partial genetic maps and maps based on
d two mapping populations combined together,
doubled haploids or intraspecific cross were not included.
# this category of markers may have included the following markers: isoenzymes,
Many doubled haploid lines are derived from the pollen of one parent. Analysing
minisatellites, microsatellites, IGS, SCAR, CAPS, PCR markers, rDNA, STS, morpho-
these lines yields the segregation directly without the necessity of crossing. After
pollen germination and regeneration of haploid plants, chromosome doubling oc-
* indication of a genetic map that could be used for analysis of distribution of loci
curs spontaneously or it is induced chemically (by colchicine). The plants grow and
with non-Mendelian segregation along linkage groups. This analysis is described
then the material is sampled for DNA analysis. During the germination of pollen
in a chapter: ªdistinguishing between biological phenomena and technical prob-
and while the plants are growing in in vitro culture, selective mortality may occur.
This mortality might explain the relatively high levels of non-Mendelian segregation
found in the doubled haploid offspring (Xu et al., 1997). Since the offspring did
not develop from embryos, the genetic maps based on double haploid populations
were not reviewed in this study. We did not include maps derived from interspe-
cific and intergeneric crosses because, in such wide crosses, chromosome pairing
and other phenomena ± that are not related to selective embryo abortion ± may
G. Korbecka, P. G. L. Klinkhamer, and K. Vrieling
Table 2 Percentage of non-Mendelian segregation found in genetic maps of wild species$$
No. of loci showing nMS for each type of marker
Abbreviations as in Table 1, M.: megagametophytes;
search resulted in 1275 records. We scanned the abstracts of all articles to find ge-
$$ We searched for genetic maps of wild species by means of Winspirs 2.0 in the Cur-
netic maps of intraspecific crosses of wild plant species. The criteria of incuding
rent Contents database until August 2000. We used the same keywords as in the
the data from a genetic map into this review were the same as for cultivated spe-
search for genetic maps of cultivated species, but in all available journals. The
ly related species of sunflowers and found that 91% of frag-
A strong argument for the fact that the non-Mendelian segre-
ments are homologous. This means that artefacts like homo-
gation is not found by chance or sampling error is the repeat-
plasy and wrong scoring due to low resolution of agarose gels
ability of finding skewed markers in the same species in many
may be responsible for only 9% of co-migrating fragments.
crosses, with a different set of parents, or in the same chromo-
However, this number would be much lower if individuals
somal regions. Xu et al. (1997) mapped chromosomes of
from the same mapping population derived from an intraspe-
rice using many types of crosses: inter-subspecific crosses,
doubled haploid and recombinant inbred lines. They detected
a non-Mendelian segregation by means of RFLP in all types of
Moreover, artefacts mentioned above cannot explain why
crosses, ranging from 17% for one of the inter-subspecific
non-Mendelian segregation often occurs in clustered loci. We
crosses, to 70% for one of the doubled haploid populations.
screened the reviewed genetic maps for the distribution of
227 distorted markers were clustered in 17 chromosomal re-
markers showing non-Mendelian segregation. On the basis of
gions, and nine of these regions were associated with segre-
the data from 30 maps (these maps are indicated in Tables 1
gation distortion in more that one population. Repeatability
and 2) we found that 56% of 633 loci segregating in non-Men-
of non-Mendelian segregation in the same region of genetic
delian fashion formed clusters of two or more markers.
Selective Embryo Abortion Hypothesis Revisited ± A Molecular Approach
The difficulty with isolation of embryos and the very small
amount of material may limit the feasibility of this method.
PCR-based techniques, like microsatellites, can be a better al-
ternative to allozyme analysis since they require much a smal-
ler amount of plant material. Hufford et al. (2000) have
shown that aborting embryos of Platypodium elegans can be
successfully genotyped by means of microsatellites. Reusch
(2000) also used microsatellites to genotype developing
embryos in Zostera marina. However, isolation of embryos at
the stage when they are large enough for analysis makes it im-
possible to investigate effects of very early stages of abortion.
When one cannot analyse the aborting embryos for their pa-
ternity, it is rather difficult to judge what was the cause of ob-
served non-Mendelian segregation that is already detected in
a map. An attempt to separate different causes has been made
by Pham et al. (1990), who determined whether selection
before or after fertilization took place on the basis of segrega-
tion analysis of isozyme loci in an F2 generation in several
crosses of rice. They used successive c2 tests for 18 loci in
which non-Mendelian segregation was found. Firstly, the equi-
frequency of alleles (p, q) was tested. Secondly, a c2 test was
made to test if the distribution of genotype frequencies fits
p2:2pq:q2 (based on the observed allele frequencies p and q)
(see Fig.1). Since, for most of the tested skewed loci, the fre-
quency of alleles was not equal and genotype frequencies fit-
ted the p2:2pq:q2 distribution, Pham et al. (1990) conclud-
ed that prefertilization (gametophytic) selection was respon-
sible for non-Mendelian segregation. However, for other loci,
Fig.1 Key for determining whether gametophytic or post-fertilisa-
evidence for post-fertilization selection was found. Guiderdoni
tion selection takes place in a segregating F2 population analysed
(1991) reported similar results for crosses between different
with co-dominant markers (based on Pham, 1990).
We performed such an analysis for the reviewed genetic maps
maps derived from different crosses of the same species was
that reported segregation data for the F2 generation for co-
also reported by Price and Tomos (1997).
dominant markers. We found segregation data for such mar-
kers only in 6 genetic maps (Mukai et al., 1995; Baudracco-
How to distinguish between SEA and other biological
Arnas and Pitrat, 1996; Katzir et al., 1996; Chen et al.,
explanations for non-Mendelian segregation?
1998; Korzun et al., 1998; Vanhala, unpublished data).
Chi square analysis of 56 loci revealed that, in 31 loci, post-fer-
There is a long list of biological explanation for non-Mendelian
tilization selection affecting heterozygotes took place, while in
segregation in plants, it includes, apart from SEA, meiotic
7 loci, zygotic or a combination of selection before and after
drive, gametophytic selection, selective germination and seed-
fertilization occurred. In 15 loci gametophytic selection was
ling death, B chromosomes, cytoplasmic inheritance, endo-
detected. In 3 loci the stage of selection could not be deter-
phytes and chromosomal rearrangements (Appendix). There-
mined by means of subsequent c2 tests. This analysis shows
fore, it is very difficult to separate SEA and other causes of
that post-fertilization selection occurs in the majority of cases
non-Mendelian segregation. Below we will present three ways
(68%) involved in non-Mendelian segregation.
Another method to track down the cause of non-Mendelian
segregation is the analysis of segregation of molecular markers
in reciprocal crosses. Korzun et al. (1998) performed such
Direct evidence for SEA may be presented by molecular marker
crosses in rye (Secale cereale) and found, in one cross, 7 loci
segregation analysis of aborting embryos in comparison to
showing non-Mendelian segregation, while in the other cross
mature seeds. Rigney (1995) performed a successful pater-
such a skewed segregation was found for 9 loci. Only 2 of those
nity analysis for aborting embryos by means of the MDH allo-
loci were common for both crosses and they are potential loci
zyme marker. Rigney (1995) removed embryos that were
in which post-fertilization selection could take place. Asym-
being aborted from a plant and analysed their paternity in
metry of segregation data in reciprocal crosses could be caused
Erythronium grandiflorum. Selfed embryos were more likely
by post-fertilization selection due to an interaction between
to abort than outcrossed ones. Moreover, the progeny fertilized
nuclear and cytoplasmic genes which is different, depending
by nearby donors are aborted more often than those sired by
on which plant is used as a female in a cross, or gametophytic
selection affecting either male or female function of one of the
G. Korbecka, P. G. L. Klinkhamer, and K. Vrieling
parents. The distinction between pre- and post-fertilization
increases offspring quality is still weak. The molecular geno-
selection in the latter case could be made if reciprocal back-
typic approach links SEA to the presence and absence of par-
crosses to both parents are performed. Faris et al. (1998)
ticular alleles, which is why offspring quality can be related to
compared non-Mendelian segregation in 4 such crosses in
specific alleles and, therefore, manipulations, such as crushing
Aegilops tauschii. They attributed nearly the whole observed
non-Mendelian segregation on chromosome 5D to gameto-
phytic selection affecting male function, however, they could
The level of non-Mendelian segregation found in the published
not exclude nuclear±cytoplasmic interaction in one region on
genetic maps suggests that there is ample opportunity to de-
tect SEA. An appropriate experimental design, which we pro-
pose in this paper, would not only detect SEA and provide the
Possible experimental design to test SEA hypothesis
possibility to relate this to offspring quality, but it would also
provide more information about the genetic mechanisms con-
Attributing non-Mendelian segregation, in crosses used to
make genetic maps, to one of the explanations given in the ap-
pendixcan be done in some cases if an experiment is carefully
planned or additional research is conducted. Some of the ex-
planations (other than SEA) for non-Mendelian segregation
We thank Eddy van der Meijden, Tom de Jong, Russell Lande,
can be ruled out by additional studies such as: chromosome
Brenda Casper, Leo Beukeboom, Jan Kozlowski for their com-
counting and observation of pollen germination (Appendix).
ments on the earlier versions of the manuscript. The work
The best way to separate the effect of SEA from other explana-
was supported by Life Sciences Foundation (SLW), which is
tions listed in appendixwould be to find an experimental
subsidized by the Netherlands Organisation for Scientific Re-
treatment with which the level of abortion is manipulated
without influencing other processes. Nutrient stress would be
a good candidate: it is known to influence abortion levels
while there are no reports that it influences e.g., meiotic drive.
If the deviation from Mendelian segregation for certain mo-
Biological explanations for non-Mendelian segregation in
lecular markers is positively correlated with the level of em-
genetic maps of plants. Meiotic drive. Lyttle (1991) de-
bryo abortion this would imply that, indeed, embryo abortion
fines meiotic drive as ªmechanics of meiotic division that
is selective. Using the same genotype (clone) in all treatments
cause one member of a pair of heterozygous alleles or hetero-
could further strengthen the argument because meiotic drive,
morphic chromosomes to be transmitted to progeny in excess
B chromosomes, cytoplasmic inheritance and chromosomal
of the expected Mendelian proportion of 50%º. A number of
rearrangements can be excluded, since the same nuclear genes
meiotic drive systems are described in detail for animals. How-
(chromosomes) are in the same cytoplasmic environments in
ever, little is known about meiotic drive in plants. In most
all nutrient treatments. If clones are grown in the same envi-
flowering plants, megasporogenesis may lead to meiotic drive
ronment, they could possibly also contain the same endo-
because of an obvious asymmetry of meiotic division: only one
of the four haploid cells develops into a functional egg and this
cell may contain preferentially transmitted alleles or chromo-
An alternative experiment would be to compare the segrega-
somes. An example of such a process is the preferential trans-
tion of molecular markers in the offspring coming from two
mission of chromosomal knobs (large clusters of repetitive
treatments performed on self-pollinated clonal replicates of
DNA) on chromosome 10 into viable megaspores in maize
one genotype of a plant. The first treatment would have the
(Buckler et al., 1999). Another example of meiotic drive, al-
ovules randomly crushed, while the control treatment would
though of interspecific origin, is the preferential transmission
not be manipulated. If selective abortion is playing a role, then
of alien chromosomes. Such chromosomes, common in Triti-
it is expected that more loci in the offspring of control plants
ceae, are called ªcuckooº chromosomes (Miller, 1983). Finch
would show non-Mendelian segregation.
et al. (1984) described the effects of one chromosome com-
ing from Aegilops sharonensis in wheat (Triticum aestivum)
The advantages of these two experimental designs are that:
plants. Such monosomic plants have abnormal female and
1. non-Mendelian segregation can be attributed to SEA,
male meiosis, only meiospores containing the alien chromo-
2. it can be established if SEA leads to higher offspring quality,
some develop into normal gametophytes. Only such a cyto-
and linked to the genotype of the offspring,
logical analysis combined with mapping would allow for attri-
3. at least for the control treatment, SEA can be studied in un-
buting non-Mendelian segregation found in the map to meio-
4. non-Mendelian segregation can also be studied among the
Gametophytic selection includes all phenomena that cause
5. it is possible to find markers for SEA that can be used on
differential success of pollen from different donors or pollen
from the same donor but bearing different alleles. Gametophy-
6. major loci controlling SEA can be detected.
tic selection may occur, for example, during pollen germina-
tion and pollen tube growth. Germination of pollen in vitro is
a standard method used to assess both its viability and pollen
tube growth. However, only in a very few cases are such tests
The traditional experimental phenotypic approach to test the
combined with data on segregation of molecular markers (Lin
SEA hypothesis has the disadvantage that the treatment itself
et al., 1992; Sari-Gorla et al., 1992). Often, gametophytic
can be a source of artefacts. That is why the evidence that SEA
selection is assumed to occur on the basis of allele frequencies
Selective Embryo Abortion Hypothesis Revisited ± A Molecular Approach
in the offspring for the loci in which non-Mendelian segrega-
of Smith (1988). Nineteen out of 60 angiosperms showed
tion was found. Under-representation of one of the alleles is
at least occasional biparental inheritance. Less examples (only
then attributed to gametophytic selection in one of the parents
four species) are available for biparental inheritance of mito-
(see e.g., Wagner et al., 1992). Such studies neglect the fact
chondria for two reasons. Firstly, this phenomenon has not re-
that post-fertilization selection affecting homozygotes also in-
ceived much attention (Reboud and Zeyl, 1994). Secondly, it
may occur less often. Species with biparental inheritance of
plastids may have strictly maternal transmission of mitochon-
Selective germination and seedling death. Kuang et al.
(1998) linked non-Mendelian segregation to seedling death
in Pinus radiata. A comparison of the segregation of RAPD mar-
Endophytes. A diversity of organisms, like bacteria and fungi,
kers was made for megagametophytes, for surviving seedlings
are known to live inside and among plant tissues (Carroll,
and those that died within the first month after germination in
1988; Clay, 1988; Hallmann et al., 1997). The DNA from
order to find markers for which segregation was significantly
endophytes may be extracted together with plant DNA and
skewed in opposite directions in both groups. A null allele of
eventually give the same effect as contamination. Cytoplasmic
one locus was over-represented in dead seedlings while it
inheritance and endophytes can potentially be observed as dis-
was strongly under-represented in the seedlings that were still
torted unlinked markers. However, molecular markers for or-
alive. The authors suggested that an allele closely linked to this
ganelle DNA will never be linked to markers for nuclear genes
null allele is responsible for the seedlings death. Moreover, a
and, if there are two polymorphic markers for organelle DNA,
segregation analysis at the same locus for unsown seeds
they will be 100% linked to each other because of a lack of re-
showed that the null allele was over-represented in this stage.
combination. Molecular markers for eucaryotic endophyte
Kuang et al. (1998) gave two possible explanations: selec-
DNA may appear in a map (resulting in more groups than chro-
tion favouring this allele prior to germination or a sampling
mosomes). However, they will never be linked to the markers
error. If the allele responsible for seedling death is indeed
that are known to be developed for plants e.g., morphological
favoured during embryo maturation, this would present a case
opposite to that is predicted by the SEA hypothesis.
Chromosome rearrangements, such as translocation and du-
The elimination of selective seed germination and seedling
plication, are often suggested causes of non-Mendelian segre-
death as the explanation for non-Mendelian segregation found
gation found in genetic maps (e.g., Vaillancourt and Slinkard,
in the map can be done if seed that did not germinate and dead
1992). However, genetic mapping alone is not sufficient to
seedlings are included into the segregation analysis.
link non-Mendelian segregation directly to translocation. Be-
lay and Merker (1998) analysed inheritance of the transloca-
B chromosomes are supernumerary chromosomes that are
tion on chromosome 6B in tetraploid wheat (Triticum turgi-
not essential for growth and reproduction of organisms. They
dum) by cytogenetics. They observed C-banding patterns in
have been described in more than 1000 species of plants (see
the F2 generation derived from two crosses, both with one par-
Jones and Rees, 1982 for a review). B chromosomes can be
ent homozygous for a translocation and one parent homozy-
distinguished from normal (A) chromosomes because they
gous for the lack of translocation. In both crosses, non-Men-
are usually smaller and consist of large amounts of heterochro-
delian segregation was observed. Homozygotes containing 2
matin. Their number may be variable even within the same in-
chromosomes without translocation were over-represented.
dividuals due to nondisjunction in anaphase of mitosis. B chro-
mosomes are inherited in a non-Mendelian fashion which, ac-
cording to Jones (1991), can be caused by their nondisjunc-
tion in female or/and male meiosis, nondisjunction in mitosis
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