Download The evolution of self-incompatibility when mates are

Review
The evolution of self-incompatibility
when mates are limiting
Jeremiah W. Busch and Daniel J. Schoen
Department of Biology, McGill University, 1205 Docteur Penfield, Montreal, QC H3A 1B1, Canada
Self-incompatibility (SI) is a genetic barrier to inbreeding
that is broadly distributed in angiosperms. In finite
populations of SI plants, the loss of S-allele diversity
can limit plant reproduction by reducing the availability
of compatible mates. Many studies have shown that
small or fragmented plant populations suffer from mate
limitation. The advent of molecular typing of S-alleles in
many species has paved the way to address quantitatively the importance of mate limitation, and to provide
greater insight into why and how SI systems breakdown
frequently in nature. In this review, we highlight the
ecological factors that contribute to mate limitation in
SI taxa, discuss their consequences for the evolution and
functioning of SI, and propose new empirical research
directions.
The multi-faceted perils of rarity
Small populations often face instability owing to demographic and environmental fluctuations that increase the
probability of local extinction [1]. When such populations
are composed of self-incompatible (SI) plants, limitation in
the numbers of genetically compatible mates can contribute to population decline. In this paper, we review theory
and data pertaining to mate limitation in finite populations of SI species, and consider the effects of mate
limitation on the evolutionary stability of SI. We suggest
that the use of molecular approaches for typing diversity
at the S-locus (‘S’ denotes self-sterility) will provide tools
for addressing questions about the importance of mate
limitation in SI taxa. By combining traditional ecological
approaches for studying mating systems with the application of molecular biological approaches, a deeper understanding of the generality of limited mate availability
can be gained, as well as the mechanisms by which this
inbreeding barrier has been lost.
Mate limitation in SI taxa
SI systems have long been studied by plant evolutionary
biologists because they strongly influence the distribution
of genetic variation in populations [2,3]. SI probably
evolved early during the diversification of angiosperms,
and is found in nearly half of all flowering plant species [4].
Despite the variation among SI systems, most share one
fundamental property: SI is controlled by a linked cluster
of genes collectively known as the ‘S-locus’, and individual
plants that share recognition alleles at this locus are
incapable of successfully producing offspring [5]. In homomorphic gametophytic or sporophytic SI systems, mate
Corresponding author: Busch, J.W. ([email protected]).
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recognition occurs when maternal S-alleles match those
expressed in the haploid or diploid life stages of pollen
parents, respectively. In heteromorphic SI systems, incompatibility prevents matings between individuals of the
same floral morph, although matings between morphs
can occur. Regardless of the specific type of SI system,
sexual reproduction within populations is dependent upon
the number and distribution of alleles at the S-locus. In the
next two sections, we discuss factors that exacerbate the
negative fitness consequences of mate limitation in small
populations of SI taxa, including reductions in the number
of S-alleles, population fragmentation, local pollen dispersal and limited pollinator availability.
Reduced population size, S-allele diversity and mate
limitation
Population size is an important determinant of the amount
of genetic variation. Theory has shown that in effectively
large populations, many S-alleles should be maintained by
negative-frequency-dependent selection, and surveys of
allelic variation have supported this hypothesis [3,6,7]
(Figure 1). In the model, it is assumed that there is
sufficient compatible pollen available to plants to ensure
that all ovules are fertilized. In moderately sized or small
populations, however, variation at the S-locus can be lost
owing to genetic drift. This is an important change in
population-genetic structure because the total number of
S-alleles maintained in a group of breeding individuals can
strongly influence the seed production of individual plants.
When compatible mates are limiting, not all ovules are
fertilized, and seed production per plant will be greatest for
the rarest S-locus genotypes; this has been termed ‘fecund-
Glossary
Allee effect: positive correlation between population growth rate and
population density; for example, as can occur when individual reproductive
success declines at low population densities owing to difficulty in encountering mates. An Allee effect can lead to extinction below a crucial threshold
density.
Genetic drift: random fluctuations in allele frequency across generations in
finite populations. The expected change in the frequency of an allele caused by
random sampling is inversely proportional to the population size.
Inbreeding depression: reduced offspring fitness as a result of breeding
between related parents. Inbreeding depression is a major force maintaining SI
systems in plants.
Negative frequency dependent selection: mode of selection whereby the
relative fitness of an allele or genotype decreases (increases) as it becomes
more (less) prevalent in the population. Because this mode of selection favors
variants when they are uncommon, it is synonymous with ‘rare advantage’.
Pseudo self-compatibility (PSC): quantitative variation in the strength of the
self-incompatibility (SI) response, such that matings between plants sharing
active S-alleles produce some seed.
1360-1385/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2008.01.002
Review
Trends in Plant Science
Vol.13 No.3
Figure 1. Numbers of S-alleles maintained in populations with gametophytic SI under three different mutation rates per generation (108, 103, 106). Unbroken lines
represent the case where only 25 alleles can be generated by mutation. Broken lines represent the case where an infinite number of S-alleles are possible. The number of
alleles expected in populations with sporophytic SI is similar when alleles act codominantly [8]. Reproduced, with permission, from Ref. [3].
ity selection’ [8]. A clear example of this phenomenon is the
low seed production of the common morph in distylous
Hottonia palustris, which was especially pronounced in the
smallest of populations examined [9].
Some studies suggest that in small or low density
populations, mate limitation causes extreme variation
among plants in seed production [10,11] (Figure 2a–c).
Direct manipulation to reduce S-allele number in experimental Raphanus sativus populations led to pronounced
declines in seed production in small populations with high
inbreeding coefficients [12]. Population studies of Hymenoxys herbacea found a tight relationship between the size
of natural populations and the average mate-compatibility
[13]. Surveys have examined patterns of mate-compatibility and seed production in natural populations of
Cochlearia bavarica and Ranunculus reptans, two
restricted European endemics. These experiments found
a collapse in the average fruit set in populations with fewer
than one-hundred individuals [14,15]. The endemic species
Rutidosis leptorrhynchoides has experienced strong
habitat fragmentation in southeastern Australia over
the past 100 years. In the smallest of populations, allozyme
allele diversity in the pollen pool of R. leptorrhynchoides
was found to be a reduced subset of the diversity of
parental genotypes, suggesting that mate limitation occurs
simply because not all individuals donate gametes through
pollen [16].
The stochastic loss of S-alleles in small populations will
also cause an increase in population structure (FST) at the
S-locus [17,18]. In a metapopulation where individual
populations have lost S-locus diversity, interpopulation
crosses should more often alleviate mate limitation compared to crosses between plants from the same population.
Interpopulation crosses were used to determine whether
seed production could be rescued in populations of C.
bavarica, R. reptans and R. leptorrhynchoides [19–21]. In
each of these endemic species, interpopulation crosses led
to increased fruit and seed set, and this effect was greatest
in populations that were the smallest or had the lowest
levels of genetic variation, as estimated using neutral
markers [19,20]. Patterns of seed production have also
been studied in remnant prairie patches of Echinacea
angustifolia [22]. Lower levels of fertilization were
observed in areas of the population with the lowest local
densities. A model incorporating the effects of habitat
fragmentation and stochastic loss of S-alleles showed that
bottlenecks of several hundred or fewer plants might have
caused the levels of mate limitation observed in small local
patches of E. angustifolia [22].
Pollinator activity and the strength of mate limitation
realized within populations
The amount by which seed production declines in small
populations can also depend upon the activity of pollinators. In theory, if SI plants are capable of continually
sampling the pollen pool until they encounter a compatible
pollen grain (i.e. because they receive many visits from
pollinators), these plants will compensate for lost reproductive opportunities caused by mating with plants sharing the same S-allele(s) [23]. Complete reproductive
compensation is expected in populations of SI plants in
which pollinators are abundant and bring about transfer of
pollen between many individuals. If, however, flowers are
visited by few pollinators, then they might receive pollen
from one or a few pollen donors [24]; because few S-alleles
would be sampled in the process, cross-incompatibility is
probable (Figure 2d–f). Pollen limitation of seed set is a
common phenomenon in populations of SI plants [25], and
smaller or less dense populations have been shown to
attract fewer pollinators [26–28]. Lower levels of pollinator
service in small populations and the resulting effects on
individual seed production is a specific manifestation of the
Allee effect (see Glossary) [29,30]. Although declines in
pollinator visitation in small or low density natural populations are generally expected to exacerbate mate limitation in SI species [31], a recent study found that elevated
pollinator activity in small populations did, in fact, attenuate the effects of limited S-allele diversity [13].
Because field and theoretical studies demonstrate that
both the size of natural populations and the level of polli129
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Trends in Plant Science Vol.13 No.3
Figure 2. Distributions of mean fruit set in 250 simulated populations possessing a sporophytic SI system with codominant allele expression. (a–c) In each trial, the
mutation rate to new alleles is m = 0.0001 and populations of size N = 250 (a), 50 (b) and 25 (c) plants. (d–f) The number of pollinator visits was varied in populations of 100
individuals, with 3 (d), 2 (e) or 1 (f) visits per flower; in cases of multiple visits per flower, the pollinator could visit a different pollen donor each time with probability 1/N. In
each simulation trial, populations were enabled to attain the quasi-equilibrium number and frequency distribution of S-alleles expected before assessing fruit-set
distributions.
nator activity can influence mate limitation, it will be
important for future investigators to account for variation
in both S-allele diversity and pollinator activity in studies
aimed at understanding the ecology of mate limitation in
SI populations.
Evolutionary consequences of mate limitation
Mate limitation lowers individual reproductive output and
increases the probability of population extinction [29].
Once populations have lost a sufficient number of S-alleles
and individual seed production declines, per-capita population growth rates should fall. Under these conditions,
natural selection should favor new mutations that disable
or modify the SI reaction because these alleles will have
higher intrinsic rates of increase. Below, we discuss the
potential evolutionary pathways taken by populations that
can experience the selective loss of SI, either through the
evolution of pseudo self-compatibility (PSC) or self-compatibility (SC).
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Population declines and the possibility of extinction
Low individual seed production in mate-limited populations can endanger population persistence. If the population suddenly declines in size, few S-alleles will survive
the bottleneck, and extinction can be inevitable unless preexisting SC mutations spread and ‘rescue’ reproduction.
This ‘filtering’ mechanism was originally invoked to
explain the evolution of SC on islands, where a single
SC seed can establish a new population following colonization [32–34]. There is compelling evidence to suggest that
precipitous population declines do, in fact, occur in natural
populations. Populations of the endangered lakeside daisy,
Hymenoxys acaulis var. glabra, were monomorphic at the
S-locus and were incapable of producing fruit [35]. Complete or nearly complete losses of S-allele diversity require
catastrophic bottlenecks, which are possible in populations
inhabiting a fragmented landscape. Less severe bottlenecks are probably more likely to occur in nature, although
these will also cause S-alleles to be lost from populations
Review
owing to genetic drift [22]. Population declines of varying
severity were implicated in limiting the seed production of
individuals in populations of Aster furcatus, a restricted
endemic [36]. In some of these populations, the majority of
individuals produced little or no fruit, suggesting the
nearly complete loss of allelic diversity at the S-locus.
The evolution of PSC
Quantitative variation in the strength of the SI response is
a phenomenon that has long been recognized in various SI
systems [37–40]. In other words, the SI response of a plant
can be ‘leaky’, such that it exhibits PSC. PSC can be caused
by S-allele products that are expressed at low levels in
flowers [41], the action of one or several modifiers that
influence the efficacy of the SI reaction [38], or be associated with post-pollination mechanisms such as floral
abscission and fruit abortion [23]. A common indicator of
PSC in species with SI systems is the production of small
fruits with few or small seeds following natural or enforced
self-pollination, or the weakening of the SI response in
older flowers [40,42,43]. PSC mechanisms seem to be widespread among species with SI systems (for a review, see
[37]). This is perhaps not too surprising because modifiers
of S-allele expression can enable selfing once opportunities
for outcrossing have elapsed; in fact, delayed selfing should
nearly always be favored by natural selection because it
enables for the ‘best of both worlds’ (i.e. plants outcross first
and self if no other pollen is available [44,45]). Recent
theoretical papers have confirmed this idea, showing that
quantitative variation in SI might reflect an evolutionary
stable mating strategy in the face of variable pollen delivery [23,46].
The emerging picture from research into the multiple
losses of SI in the genus Arabidopsis supports the idea that
PSC can be an evolutionary transition to high levels of selffertilization. There is marked variation among individuals
and populations in the strength of the SI response in
Arabidopsis lyrata var. lyrata in North America [47].
Populations that have experienced the loss of SI are genetically less variable [48]. In this species, there does not seem
to be a strong indication that the loss of SI occurs more
frequently in smaller populations – it does seem, however,
that the recent history of post-glacial colonization was
important. The historical chain of events that seem to have
led to the loss of SI and the evolution of self-fertility in A.
thaliana is similar to that invoked in the case of A. lyrata,
although there is more information on the genetic modifications that have disabled SI in A. thaliana. The loss of SI
might have started with the weakening of the incompatibility response in older flowers [43], which would be
selectively favored during the post-glacial colonization of
habitats by this weedy plant [47]. Moreover, it seems that,
within this species, there were several independent losses
of the SI reaction [49–51], and the loss of variation at the
S-locus has been gradual [52]. In support of this idea, the Slocus pseudo-genes of A. thaliana are still extremely variable in comparison to the genomic average [53]. Taken
together, these independent pieces of evidence suggest that
natural selection, facilitated by a lack of mates during
colonization, might have led to the gradual fixation
of multiple, independent mutations that weakened or
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disabled the SI system throughout the geographic range
of A. thaliana.
Selective spread of non-functional S-alleles enabling SC
It has often been suggested that SI systems breakdown
when non-functional S-alleles (causing SC) invade natural
populations and are swept to fixation [49,54,55]. In many
natural systems, it might be possible for both PSC and SC
mutations to be present in populations [47,56,57–59]
because both will be selectively favored under conditions
of mate limitation. However, even in populations that do
not experience mate limitation, SC mutations should equilibrate at some intermediate frequency dictated by the
level of inbreeding depression and rate of selfing [54]. With
mate limitation, SC mutations should be quickly driven to
high frequencies unless inbreeding depression is extreme
[23,46]. Given the widespread occurrence of pollen limitation of seed set, one would expect that there should be
many observations of SC mutations that have been fixed by
natural selection, thereby disabling the SI mechanism.
Interestingly, although there have been indications of a
low frequency of SC individuals within natural populations
of SI plants [47,56–63], as well as direct genetic evidence of
SC mutations segregating at low frequency in populations
or cultivars [64–68], there is also evidence that the loss of
SI might not always be caused by the rapid fixation of SC
mutations at the S-locus [47,53].
Theory makes specific predictions regarding the specific
kinds of SI-disabling mutations that should be recruited
Box 1. Demography, mate availability and dominance
S-alleles studied in three plant families with independent evolutionary histories (Asteraceae, Brassicaceae and Convulvaceae) are
organized into complex dominance hierarchies. In a dominance
hierarchy, alleles of the same class act codominantly, but are
dominant to those below them in the hierarchy (e.g. if S2 and S3 are
dominant to S1, then a cross between S1S2 and S1S3 will produce
seed). Hierarchies have been shown to consist of six [70], four [86],
three [87] or two classes of alleles [71]. In some species, the
hierarchy is the same for the expression of S-alleles in the pistil and
the pollen [70], whereas in other species the dominance relationships are asymmetrical in pistils and pollen [71]. A recent theoretical
treatment has made it clear that the number of classes in a
dominance hierarchy and the interactions among alleles might be
the result of both selection and demographic history of a species
[77].
Theory suggests that it is difficult for recessive alleles to be
maintained in finite populations because they are not rescued from
loss owing to genetic drift when rare [6]. The vulnerability of
recessive S-alleles to extinction can cause classes of the dominance
hierarchy to disappear in species with small effective population
sizes [77]. Bottlenecks might have caused the loss of all but two
dominance classes in Brassica, where S-alleles exhibit shallow
genetic divergence; by contrast, there are four classes of the
dominance hierarchy in Arabidopsis, in which S-alleles are extremely divergent from each other [88], which is consistent with
historically large population sizes [89]. Interestingly, when mate
limitation occurs, recessive S-alleles are more likely to be retained in
effectively small populations because they will be passed on more
frequently than dominant alleles via seeds and pollen [77]. Mate
limitation might, therefore, contribute to the retention of S-alleles in
the most recessive class in small populations. The evolution of
population-specific dominance interactions in Senecio squalidus is
another example in which the architecture of the S-allele dominance
hierarchy might respond to natural selection caused by local mate
limitation [74,75].
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Box 2. Neutral genomic variation and S-allele diversity
The variation found at neutral loci should reflect the balance of
mutation and genetic drift. Putatively neutral nuclear genetic markers
(e.g. allozymes, non-coding sequences and microsatellites) can
provide estimates of effective population size (u = 4Neu), which will
reflect recent historical bottlenecks or fluctuations in overall number.
Using microsatellite loci in populations of the Corsican endemic
Brassica insularis, a recent study examined both S-allele diversity and
estimated parameters describing genetic variation (Figure I) [71].
Estimates of microsatellite heterozygosity and effective population
size were markedly reduced in the smallest population (Punta Calcina;
Table I). Interestingly, positive inbreeding coefficients across microsatellite loci indicated departures from random mating even in three
of the larger populations; this might be the result of many recessive Salleles that are broadly distributed throughout the range of the
species. Indeed, each of the two recessive S-alleles in this species are
distributed in at least four of the studied populations, whereas alleles
with more codominant expression are restricted to fewer locales.
It is also evident from this study that populations must be small (and,
therefore, that genetic drift must be strong) so as to promote the loss of
S-alleles. The Punta Gobaghiola and Punta Calcina populations have
approximately three- to fourfold reductions in effective size compared
with the other studied populations. However, S-allele diversity seems
to have declined only in Punta Calcina, which currently harbors 80
plants, of which about half were flowering. Interestingly, Punta Calcina
harbors a single recessive S-allele at high frequency (ranging from 45–
90%, depending upon details concerning assumptions about inferring
homozygous S-locus genotypes). A shift in this population toward one
high frequency recessive allele is consistent with mate limitation of
reproduction in Punta Calcina.
Figure I. Populations of Brassica insularis on the island of Corsica in which Slocus and neutral genetic diversities were estimated. Populations shown in black
were studied; unstudied populations are shown in white.
Table I. Estimates of population-genetic parameters in Brassica insularisa,b
Population
Teghime
Caporalino
Inzecca
Punta Gorbaghiola
Punta Calcina
Population size
2000
1500
500
300
80
% flowering
17
27
55
70
56
S-allele # (range)
18 (15–19)
24 (19–31)
15 (11–31)
16 (12–16)
8 (5–19)
HE
0.58
0.63
0.48
0.50
0.22
FIS c
0.217 *
0.158 *
0.003
0.147 *
0.045
Q
10.48
8.43
6.25
2.38
1.08
a
Reproduced, with permission, from Ref. [71].
Expected heterozygosity (HE), the scaled effective population size parameter u = 4Neu, and inbreeding coefficients (FIS = 1 (HO/HE)) (where HO is observed heterozygosity) were estimated using 11 microsatellite markers.
c
Asterisks denote significant departures from random mating.
b
when SC is favored. In particular, mutations that disable
the pollen component of recognition should have the highest rates of increase when they appear in natural populations; such mutations reduce mate limitation through
both pollen and seed if they enable self-fertilization [69]. By
contrast, mutations that disable maternal recognition do
not alleviate mate limitation as a pollen parent, although
they do enable self-fertilization. Molecular investigations
into the genetic basis of SC mutations have found support
for the occurrence of mutations that disable pollen function
[62,64–66], maternal function [60,64–67] or both [61]. Perhaps the most compelling generality from these studies is
that there are often several independent mutations conferring SC within a single species. Although it is clear that
132
SI systems are lost recurrently, there is a need to determine whether mate limitation plays a role in this repeated
evolutionary trend at the population level.
Recessive S-alleles in sporophytic SI systems
In sporophytic (as opposed to gametophytic) SI systems,
there is the further possibility for a unique evolutionary
response to mate limitation and limited S-allele diversity.
In these systems, some alleles have recessive phenotypes.
If two mates are heterozygous for the same recessive Sallele, they can still produce offspring; this enables recessive S-alleles to be found at relatively high frequencies in
natural populations. Empirical studies of S-allele diversity
in nature and in cultivars have found evidence in favor of
Review
the hypothesis that mate limitation can cause populations
to experience shifts toward a higher frequency of recessive
alleles [69]. For instance, in the small populations at the
western and eastern edge of the species range of Ipomoea
trifida, there are fewer S-alleles maintained, and the
relative frequency of the most recessive S-allele is nearly
double that observed in larger, more geographically central
populations [70]. In another study, the smallest population
of the Corsican endemic Brassica insularis maintained few
alleles, with the most common one being recessive [71].
Work on the Oxford ragwort (Senecio squalidus) also
suggests that bottleneck-induced losses of S-allele diversity drive shifts toward recessive alleles [72–75], although
the selective enrichment of recessive alleles has also been
invoked to explain increased mate availability in introduced populations of Senecio inaequidens [76]. In general,
there has been much recent progress in our understanding
of the forces influencing the evolution of dominance in
sporophytic SI systems [77] (Box 1).
Empirical research directions
Molecular approaches to studying S-locus diversity are
likely to be useful for addressing how and why mate
limitation occurs in natural SI populations and its evolutionary consequences. Recent identification of the
proteins involved in SI has made it possible to employ
S-allele variation as a direct tool to study the functioning of
mating systems in populations of a growing number of wild
species in the Brassicaeae (Arabidopsis [78], Capsella [79]
and Leavenworthia [80]) and the Solanaceae (Petunia [62],
Solanum [41] and Witheringia [63]). These species might
serve as models for understanding the strength of mate
limitation, and the spread of mutations that weaken or
disable SI. Below, we propose several exemplary experiments that we believe will further our understanding of
mate limitation as a selective force in SI populations.
Are most SI populations mate-limited?
The generality of mate limitation in SI species is an
important issue. It is possible that it is important only
in geographically restricted species or in populations that
have become fragmented. By determining the S-locus genotypes of individuals via direct amplification of S-linked
loci, it should be possible to relate variation in S-allele
diversity to reproductive success. Once mate limitation has
been quantified, it should then be possible to relate this
phenomenon to potential explanatory variables (e.g. population size, stability, isolation and/or loss of pollinator
service, etc.). These experiments could provide a starting
point for identifying threats to the persistence of individuals and populations, particularly in SI species with
restricted ranges [19–21].
How important are historical bottlenecks in causing
mate limitation?
Population genetic theory suggests that population size
crashes limit S-allele diversity and cause mate limitation.
Identification of populations for the study of mate limitation can be facilitated by acquiring estimates of the effective population size using neutral genetic markers; this
measure encapsulates fluctuations in the recent demo-
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Vol.13 No.3
graphic history [47,71,75]. If mate limitation has caused
a shift toward greater amounts of mating between
relatives or self-fertilization in a leaky SI system, estimation of population mating system parameters and
Box 3. Natural selection of SC mutations via pollen and seed
Once one identifies a mutation causing SC, it should be possible to
study the evolutionary forces acting on it. This is a potentially
important approach because it could enable investigators to
measure directly how natural selection operates on the strength of
SI. Although we might expect transient positive (negative) selection
on S-alleles as they fluctuate below (above) their deterministic
equilibria, persistent positive selection on a SC mutation might be
expected for two reasons. First, SC alleles have a natural transmission advantage through paternal function because SC pollen grains
should, in theory, not be recognized by functional S-alleles. Second,
if mate limitation is restricting the seed production of maternal
plants with functional S-alleles, then SC genotypes should enjoy a
seed benefit because they enable self-fertilization.
The relative fitness advantage of a SC mutation via either of these
pathways can be quantified if one genotypes individuals at the Slocus using PCR-based amplification of specific S-alleles [78]. For
example, assume that the population contains n alleles (S1, S2,. . .,
Sn), which occur at frequencies ( p1, p2,. . ., pn) in the parents. In the
absence of selection via male function, the frequency of any given Sallele in the pollen pool should be equal to its relative frequency
among the parent plants in the population. Thus, for a focal Sgenotype (e.g. S1S2) one can calculate the observed frequency of the
nth S-allele in the progeny and compare it to that expected in the
absence of selection ( p 0nðexpectedÞ ):
p 0nðexpectedÞ ¼
pn
1 p1 p2
If the nth allele is a SC mutation that is spreading because it avoids
rejection by functional S-alleles, then one should observe a greater
number of these alleles transmitted to progeny via pollen than
expected in the absence of selection ( p 0nðobservedÞ > p 0nðexpectedÞ ; Figure
I). It is easier to show that the nth S-allele confers a selective
advantage through seeds. Natural selection of an S-allele via a seed
advantage is implicated whenever the average seed production of
the nth haplotype is significantly greater than the average seed
production of all haplotypes (Figure II).
Figure I. Test of positive selection on an S-allele through pollen.
Figure II. Test of positive selection on an S-allele through seeds.
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inbreeding coefficients should also reflect departures from
patterns expected under random mating [48]. A recent
study of B. insularis (Box 2) provides an excellent example
of this approach because it used highly variable microsatellite markers to infer historical population sizes and to
motivate future studies of a population that might be
experiencing mate limitation [71].
Does mate limitation drive the loss of SI in natural
populations?
Although the recurrent loss of SI systems has often been
invoked as a major evolutionary trend in angiosperms [81],
our ability to understand the population-level mechanisms
that underlie such losses has increased in the past decade. It
will be important to determine whether mate limitation
selects against SI genotypes by studying plant species where
the evolution of PSC or SC has occurred recently. Recent
breakdown of SI, where SI and SC (or PSC) genotypes cooccur in the same population, provides an important opportunity to compare seed production of both SI and SC (PSC)
genotypes directly [47,56,57,59], and, therefore, gives investigators the ability to implicate natural selection in the
evolution of the mating system. For example, a study of
Solanum carolinense identified a ‘leaky’ S-allele causing
PSC [41]. Given this evidence and the ability to amplify
the allele directly, it should now be possible to determine
whether this allele enjoys a selective advantage in natural
populations, and to determine whether selection is strongest
in populations experiencing mate limitation (Box 3).
Traditional approaches, such as the genetic analysis of
hybrids and phylogenetic studies of mating system transitions, have advanced our understanding of the evolutionary paths taken between SI and SC. For example, the
historical chain of events involved in the evolution of
PSC or SC has been illuminated by creating experimental
hybrids between plants from closely related SI and SC
species [79]. This approach recently implicated a mutation
causing delayed selfing in the loss of SI in A. thaliana [43].
However, it can sometimes be difficult to identify the
mutation(s) causing the initial loss of SI because all of
the genes in this signaling pathway should evolve neutrally once the SI system ceases to function [82]. Phylogenetic studies have provided, and will continue to provide,
important insights into the loss of SI because these studies
continue to provide valuable information on the minimum
number of times SI has been lost, as well as the ecological
correlates that might have favored or disfavored the maintenance of inbreeding barriers [54,82–85]. Direct studies of
selection on S-alleles should complement these approaches
by implicating the selective processes that disable SI systems or stabilize mixtures of SI, PSC and/or SC genotypes
at the population level.
Acknowledgements
We thank Boris Igic, Mario Vallejo-Marin and two anonymous reviewers
for helpful comments. J.W.B. was supported by a McGill University
Tomlinson Fellowship and D.J.S. acknowledges the support from an
NSERC Discovery Grant.
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