Polyploidy and Self-Fertilization in Flowering Plants
Author(s): Brian C. Barringer
Source: American Journal of Botany, Vol. 94, No. 9 (Sep., 2007), pp. 1527-1533
Published by: Botanical Society of America, Inc.
Stable URL: http://www.jstor.org/stable/27733324
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American Journal of Botany 94(9): 1527-1533. 2007.
Polyploidy and self-fertilization in flowering plants1
Brian C. Barringer2
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, New York 14853 USA
Mating systems directly control the transmission of genes across generations, and understanding the diversity and distribution
of mating systems is central to understanding the evolution of any group of organisms. This basic idea has been the motivation for
many studies that have explored the relationships between plant mating systems and other biological and/or ecological
phenomena, including a variety of floral and environmental characteristics, conspecific and pollinator densities, growth form,
parity, and genetic architecture. In addition to these examples, a potentially important but poorly understood association is the
relationship between plant mating systems and genome duplication, i.e., polyploidy. It is widely held that polyploid plants self
fertilize more than their diploid relatives, yet a formal analysis of this pattern does not exist. Data from 235 species of flowering
plants were used to analyze the association between self-fertilization and ploidy. Phylogenetically independent contrasts and
cross-species analyses both lend support to the hypothesis that polyploids self-fertilize more than diploids. Because polyploidy
and self-fertilization are so common among angiosperms, these results contribute not only to our understanding of the relationship
between mating systems and polyploidy in particular, but more generally, to our understanding of the evolution of flowering
plants.
Key words: angiosperms; comparative analysis; flowering plants; inbreeding depression; mating systems; phylogenetically
independent contrasts; polyploidy; self-fertilization.
The diversity and distribution of mating systems in plants
have been of longstanding interest, and it is widely
acknowledged that mating systems can profoundly influence
the evolutionary trajectories and long-term success of taxa
(Darwin, 1859, 1876; Stebbins, 1950, 1957; Grant, 1981,
Lande and Schemske, 1985; Barrett and Eckert, 1990; Barrett
et al, 1996; Barrett, 2003). Because mating systems are
influenced and molded by environmental and genetic factors
(Barrett and Eckert, 1990; Barrett, 2003), they are not simply
static descriptors of a taxon's life history, but are, rather,
dynamic and evolving traits in and of themselves (Barrett and
Eckert, 1990). For these reasons, a thorough understanding of
the evolution of plant mating systems and the patterns of their
distributions is clearly fundamental to an understanding of the
evolution of flowering plants.
Some of the most persistent questions surrounding the
evolution of plant mating systems are those that address the
evolution of self-fertilization. In the absence of pollen
discounting (the reduction due to selfing in the number of
pollen grains available for outcrossing [Harder and Wilson,
1998]), selfing is advantageous because a selfing individual
will pass on two copies of its genome for every copy passed on
by an outcrossing individual (Fisher, 1941). This "cost of
1 Manuscript received 14 September 2006; revision accepted 20 July
2007.
The author thanks M. Geber for providing encouragement and
constructive criticism during all phases of this work. Thanks also to S.
Barrett and C. Eckert for sharing their selfing rate data, to J. Bellemare and
I. Lovette for helping with the comparative analyses, and to R. Harris for
helping with the figures. S. Balcomb, M. Noor, S. Otto, and several
anonymous reviewers provided comments that improved previous
versions of this manuscript. This work benefited from discussions with
J. Anderson, E. Baack, S. Barrett, J. Bellemare, C. Eckert, J. Doyle, L.
Evanhoe, K. Flinn, J. Fox, S. Gardescu, M. Geber, R. Harris, R. Harrison,
B. Husband, K. Liddicoat, I. Lovette, B. Mable, P. Marks, K. Mills, D.
Moeller, S. Murphy, M. Park, J. Ramsey, S. Reilly, M. Vellend, and F.
Vermeylen.
2 E-mail: bcb24@cornell.edu, phone: 607-254-4282, fax: 607-255
8088
outcrossing" provides a 50% fitness advantage to selfing
variants in otherwise outcrossing populations, and unless
counteracted by some other selective force, will translate to
increased population selfing rates (Fisher, 1941; Charles worth
and Charlesworth, 1979). In addition, self-fertilization may be
advantageous as a reproductive assurance mechanism (Steb
bins, 1950, 1957; Grant, 1981; Pannell and Barrett, 1998;
Morgan and Wilson, 2005) or as a means of fixing co-adapted
gene complexes (Lande and Schemske, 1985).
In contrast to phenomena that might favor the evolution of
selfing are a variety of factors that may select for outcrossing,
such as pollen discounting (Harder and Wilson, 1998),
temporal and spatial variation in environmental conditions
(Maynard-Smith, 1978; Lande and Schemske, 1985), and
tradeoffs in the allocation of energy to male and female
functions resulting in gender specialization (Charnov et al,
1976; Brunei, 1992; Thomson, 2006). In addition, inbreeding
depression (the reduction in fitness of inbred relative to
noninbred individuals) is often hypothesized to be strong
enough to overcome the selective cost to outcrossing (Charles
worth and Charlesworth, 1979, 1987; Lande and Schemske,
1985; Husband and Schemske, 1996, 1997). If inbreeding
depression leads to a 50% fitness reduction in selfed progeny
relative to outcrossed siblings, selfing may no longer be
advantageous (Charlesworth and Charlesworth, 1979, 1987;
Lande and Schemske, 1985; but see Holsinger, 1988). Despite
the detrimental effects of inbreeding and the potential benefits
of outcrossing, high levels of self-fertilization have evolved
repeatedly in many groups (Stebbins, 1950; Johnston and
Schoen, 1996).
The transition from outcrossing to selfing in plants is
correlated with many biological and ecological phenomena,
including a variety of floral and environmental characteristics,
conspecific and pollinator densities, growth form, parity, and
genetic architecture (Darwin, 1876; Stebbins, 1950, 1957;
Grant, 1956, 1981; Charlesworth and Charlesworth, 1979;
Wyatt, 1984; Lloyd, 1992; Barrett et al., 1996; Pannell and
Barrett, 1998; Morgan, 2001; Barrett, 2003; Morgan and
Wilson, 2005; Scofield and Schultz, 2006). In addition to these
1527
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1528 American Journal of Botany [Vol. 94
examples, a potentially important though poorly understood
association is the relationship between self-fertilization and
genome duplication, i.e., polyploidy. Polyploids are organisms
with more than two sets of chromosomes (Grant, 1981; Soltis
et al., 2004), and, although relatively rare in most groups of
animals (Otto and Whitton, 2000; Mable, 2004b; but see Legatt
and Iwama, 2003), polyploidy is common in flowering plants
(Soltis et al., 2004). The relationship between polyploidy and
self-fertilization in plants has been of interest for many years,
because it is widely held that polyploids have higher selfing
rates than their diploid relatives (Stebbins, 1950; Mable,
2004a). There are several nonmutually exclusive reasons why
polyploidy might be associated with increased levels of selfing
in plants: first, polyploidy may facilitate the evolution of self
fertilization because it results in a breakdown of self
incompatibility (SI) systems in many groups of plants,
especially those whose SI systems are gametophytic (Bateman,
1952; Barrett, 1987; Mable, 2004a). Because SI systems reduce
or eliminate the ability to self-fertilize, it follows that some
polyploids may have increased levels of selfing compared to
their diploid relatives whose SI systems remain intact. Second,
the ability to self-fertilize may facilitate the evolution of
polyploidy. Newly arisen polyploids (i.e., neopolyploids) are
likely to co-occur with their diploid progenitors (Levin, 1975;
Jackson, 1976; Ramsey and Schemske, 1998), and because
intercytotype crosses often result in offspring with low fitness
(Levin, 1975; Ramsey and Schemske, 1998), minority
cytotypes are expected to experience negative frequency
dependent selection, a phenomenon referred to as minority
cytotype disadvantage (Levin, 1975). The ability to self
fertilize should reduce the effects of minority cytotype
disadvantage by eliminating the need for a cytoplasmically
compatible mate, and for this reason it may be that selfing taxa,
on average, successfully produce more polyploids than do
outcrossing taxa (Grant, 1956, 1981; Stebbins, 1957; Levin,
1975; Ramsey and Schemske, 1998). Finally, some theoretical
work predicts that polyploids may exhibit less inbreeding
depression than diploids, owing to the presence of multiple
gene copies and the associated reduction in the rate of
formation of homozygotes (Lande and Schemske, 1985). The
relationship between polyploidy and inbreeding depression is
complex, however, and levels of inbreeding depression in
polyploids have been shown to depend on many additional
factors, including the level of dominance of deleterious al?eles,
the number and lethality of genes involved, and the age of the
polyploid in question (Ronfort, 1999; Pannell et al., 2004;
Rausch and Morgan, 2005). Indeed, some studies predict that,
under some circumstances, polyploids might exhibit greater
inbreeding depression than their diploid relatives (Busbice and
Wilsie, 1966; Bennett, 1976; Ronfort, 1999). In addition,
polyploids differ in regard to the behavior of their chromo
somes during cell division, and although autopolyploids
(polyploids that possess only homologous chromosomes)
may effectively mask deleterious al?eles better than diploids,
?z//opolyploids (polyploids that possess homeologous chromo
somes) are expected to have chromosomal behavior similar to
that of diploids and may not exhibit increased tolerance to
inbreeding (Bever and Felber, 1992; Ronfort, 1999; Soltis and
Soltis, 2000; Comai, 2005). To date, theoretical work has
concentrated on autopolyploids, however, and no formal
theoretical explorations of inbreeding depression in allopoly
ploids exist (Pannell et al., 2004; but see Lande and Schemske,
1985). Comparative data on inbreeding depression in closely
related polyploid and diploid taxa are few (Ramsey and
Schemske, 2002; Pannell et al., 2004), but at least two studies
indicate lower inbreeding depression in autopolyploids relative
to diploids (Husband and Schemske, 1997; Rosquist, 2001).
The ability to increase levels of selfing without suffering the
detrimental consequences of inbreeding depression should
select for increased selfing rates among polyploids.
Despite increasing interest in the evolution of both
polyploidy and plant mating systems, surprisingly few studies
have carefully evaluated whether polyploids do, in fact, self
fertilize more than diploids (Ramsey and Schemske, 1998;
Mable, 2004a). Among homosporous ferns, polyploids do tend
to self-fertilize more than diploids (Soltis and Soltis, 1987,
1990; Masuyama and Watano, 1990), and very limited support
for this trend in gymnosperms also exists (B. C. Barringer,
unpublished data). Whether this pattern holds across the
angiosperms remains unknown, however, despite many
anecdotal examples (e.g., Stebbins, 1950; Grant, 1956, 1981).
One way to answer this question would be to compare the
mating systems of polyploid angiosperms and their immediate
progenitor taxa (i.e., sister-taxon comparisons); the relation
ships between polyploids and their progenitors are often
unknown, however, and selfing rates for those groups in which
such relationships are known have generally not been estimated
(Husband and Schemske, 1997). Both Stebbins and Grant
describe several genera (e.g., Amsinckia, Bromus, Clarkia,
Gilia, Microseris) wherein polyploids self more than diploids
(Stebbins, 1950; Grant, 1956, 1981), and others have since
documented this trend within specific groups (Ross, 1981;
Husband and Schemske, 1997; Cook and Soltis, 2000; Quarin
et al., 2001; T?te and Simpson, 2004; Guggisberg et al., 2006).
The opposite pattern occurs among diploid and polyploid
species of Tragopog?n (Asteraceae) (Cook and Soltis, 1999),
however, and although polyploidy might generally be associ
ated with a loss or breakdown of gametophytic SI systems, a
recent review failed to find a widespread association between
polyploidy and self-compatibility, especially among taxa with
sporophytic or heteromorphic SI (Mable, 2004a). Finally,
although polyploidy has resulted in a breakdown of SI in the
genus Lycium (Solanaceae), this may have led to an increase in
inbreeding depression as rates of self-fertilization increased,
which facilitated selection for higher outcrossing rates among
polyploids via the evolution of gender dimorphism (Miller and
Venable, 2000).
Here I examine the association between ploidy and self
fertilization using data from 235 species of flowering plants for
which levels of self-fertilization have been estimated. I report
results from two separate analyses of these data: (1)
phylogenetically independent contrasts (PICs), which control
for phylogenetic relationships among taxa, and (2) an analysis
that does not control for phylogeny but instead treats each
species as an independent data point (i.e., cross-species
analysis). In each analysis I ask whether polyploids have
higher levels of self-fertilization than diploids. Annuals,
herbaceous perennials, and woody perennials differ in their
average rates of self-fertilization (Barrett and Eckert, 1990;
Barrett et al., 1996). Accordingly, these three life-history
categories are represented by an additional independent
variable (along with ploidy) in the second analysis (cross
species analysis). In addition, the relationship between
polyploidy and self-fertilization might differ among major
groups of angiosperms; therefore, in both analyses the
monocotyledons, rosids, and asterids were analyzed on their
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September 2007] Barringer?Polyploidy and selfing in plants 1529
?M
40
!'S
I20
0
Dip. Poly. Dip. Poly. Dip. Poly,
ann. ann. h. per. h. per. w. per. w. per.
Fig. 1. Numbers of taxa represented in the data set by diploid annuals
(Dip. ann.), polyploid annuals (Poly, ann.), diploid herbaceous perennials
(Dip. h. per.), polyploid herbaceous perennials (Poly. h. per.), diploid
woody perennials (Dip. w. per.), and polyploid woody perennials (Poly. w.
per.).
own in addition to the analysis of the entire data set. Although
within-family comparisons might be a more informative and/or
biologically meaningful way to analyze angiosperm life-history
data, most families included in this study lack variation in
ploidy (among those species represented in the data set),
making within-family comparative analysis impossible.
MATERIALS AND METHODS
Selfing rate and ploidy database?Selfing rate estimates for angiosperm
taxa were compiled from the primary literature. S. C. H. Barrett and C. G.
Eckert provided a database of selfing rates from studies published through 1995
(S. C. H. Barrett, University of Toronto, and C. G. Eckert, Queen's University,
personal communication). I gathered additional data on selfing rates published
since 1995 (through March 2006) using the Science Citation Index Expanded
(ISI Web of Knowledge, Web of Science, Science Citation Index Expanded,
1900-2007) online science literature database. Only levels of selfing measured
in natural populations (i.e., occurring in their natural habitat and range) were
included. Because most studies report population outcrossing rates, the selfing
rate for a given study population is equal to 1 ? /, where t is the outcrossing
rate. For studies reporting estimates of t > 1 (which may occur if multiple loci
are used and one or more assumptions of the model used to estimate
outcrossing rates are violated [Ritland and Jain, 1981]), the selfing rate was set
to zero. For some taxa, levels of self-fertilization have been estimated for
multiple populations and/or for the same population during multiple years. If
multiple estimates of t were available for a species, I used the mean value of the
estimates in my analyses.
Chromosome numbers for most taxa were obtained from the Missouri
Botanical Garden's Index to Plant Chromosome Numbers (http://mobot.mobot.
org/W3T/Search/ipcn.html) or the Chromosome Atlas of Flowering Plants
(Darlington and Wylie, 1955). For a few species (6%), taxon-specific literature
was consulted for chromosome counts not reported in these sources. Because
information on ploidy does not exist for most species, I inferred relative ploidy
levels for individual taxa by comparing basal chromosome numbers for a given
genus (Darlington and Wylie, 1955) to those reported for the species in
question (sensu Mable, 2004a). Darlington and Wylie (1955) defined basal
chromosome numbers as the largest common denominator of all published
chromosome counts for a given genus. Taxa with chromosome numbers that
are two times the basal number are treated as diploids, while those with more
than two times the basal number are treated as polyploids.
The complete data set (Appendix SI, see Supplemental Data accompanying
the online version of this article) contains 235 species of flowering plants from
LU,
126 genera and 58 families (Cronquist, 1981, 1988; APG Angiosperm
Phylogeny Group, 2003), and includes 170 diploids and 65 polyploids. There
are 74 annuals, 82 herbaceous perennials, and 79 woody perennials in the data
set. The numbers of diploids and polyploids in each of the three life-history
categories are shown in Fig. 1.
Statistical analyses?Selfing rate data were arcsine (y/y) transformed
before analysis to better meet assumptions of normality/equal variance.
Normality was assessed using Minitab (version 13.1, Minitab Inc., State
College, PA, USA) and a Ryan-Joiner normality test (r = 0.9819, P = 0.0710).
Homogeneity of variance was assessed using Minitab and a Levene test (L =
1.127, P = 0.341). For all analyses, results from the analysis of nontransformed
data were qualitatively the same.
Analysis 1 (phylogenetically independent contrasts)?Because plant mating
systems are distributed nonrandomly with respect to phylogeny (Barrett and
Eckert, 1990), PICs were constructed to control for phylogenetic relations
among taxa (Felsenstein, 1985). The MacClade software package (Maddison
and Maddison, 1992) was used to build a phylogenetic tree (MacClade file
available from the author on request) containing all of the 235 species in the
data set, based on the Davies et al. (2004) phylogeny of flowering plants.
Taxon-specific literature was used to resolve relationships within families, but
several genus- and species-level polytomies remain in the finished tree, owing
to a lack of available data for some groups. The Comparative Analysis by
Independent Contrasts (CAIC) software package (Purvis and Rambaut, 1995)
was then used to identify and calculate PICs for four different trees: (1) the
entire tree containing all 235 species, (2) a tree that included monocotyledons
only (43 species), (3) a tree that included rosids only (92 species), and (4) a tree
that included asterids only (77 species). All branch lengths were set equal;
results from the analysis of trees for which branch lengths had been estimated
using the algorithm described by Grafen (1989) were qualitatively the same.
CAIC uses one of two different models to calculate PICs: CRUNCH (if all
variables in the analysis are continuous) or BRUNCH (if the analysis includes
one or more categorical variables) (Purvis and Rambaut, 1995). Because ploidy
is categorical, the BRUNCH model was used. When performing PICs, CAIC
automatically investigates potential violations in the assumptions of regression
analysis (http://www.bio.ic.ac.uk/evolve/software/caic/assumptions.html); no
violations were found.
Analysis 2 (cross-species analysis)?Shifts between outcrossing and selfing
as well as changes in ploidy are very common among angiosperms (Barrett et
al., 1996; Soltis et al., 2004), and because mating systems and ploidy are
evolutionarily labile (relative to rates of speciation), phylogenetic correction
may not be necessary (Felsenstein, 1985; Westoby et al., 1995; Barrett et al.,
1996; Ricklefs and Starck, 1996; Price, 1997; Larson and Barrett, 2000;
Rheindt et al., 2004) (see Discussion). In addition, levels of self-fertilization
among flowering plants correlate strongly with life history; annuals tend to self
more than herbaceous perennials, which in turn have higher selfing rates than
woody perennials (Barrett and Eckert, 1990; Barrett et al., 1996). Therefore, for
the cross-species analysis, I included both ploidy and life history (and their
interaction) as independent variables in a two-way analysis of variance
(ANOVA) using PROC GLM in SAS (SAS Institute, 1999-2001). As in
analysis 1, the monocotyledons, rosids, and asterids were analyzed separately in
addition to the overall analysis, which included all 235 species in the data set.
RESULTS
Analysis 1 (phylogenetically independent contrasts)?The
CAIC program identified 32 PICs from among the 235 species
represented in the complete phylogeny, and the mean contrast
value is significantly greater than zero, indicating that
polyploids tend to have higher levels of selfing than their
diploid relatives (AT = 32 contrasts, P = 0.0011) (Table 1, Fig.
2). When analyzed on their own, monocotyledons (N = 9
contrasts, P = 0.0274) and rosids (N = 11 contrasts, P =
0.0013) also exhibit higher levels of selfing among polyploids
than among diploids. In contrast, the asterids provide no
support for the hypothesis that polyploidy is associated with
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1530 American Journal of Botany [Vol. 94
Table 1. Phylogenetically independent contrasts. Positive contrast
values indicate higher selfing rates among polyploids relative to
diploids.
Analysis No. contrasts No. positive
All species 235 32 22 0.0011
Monocotyledons only 43 9 7 0.0274
Rosidsonly 92 11 10 0.0013
Asterids only 77 7 3 0.6255
increased levels of self-fertilization (N = 7 contrasts, P ?
0.6255).
Analysis 2 (cross-species analysis)?When all 235 species
are treated as independent data points, polyploids have
significantly higher levels of selfing than diploids (N = 235,
P = 0.0001) (Table 2). Results from the other three cross
species analyses are similar: monocotyledons (N = 43, P =
0.0067), rosids (N = 92, P = 0.0143), and asterids (N = 77, P =
0.0112). In addition, life history correlates strongly with selfing
rate in all four cross-species analyses, with annuals having
higher levels of selfing than herbaceous perennials, which in
turn have higher levels of selfing than woody perennials. The
interaction between ploidy and life history was nonsignificant
for all four analyses. The distribution of selfing rates for all six
possible combinations of ploidy and life history are shown in
Fig. 3, and the least-squares mean selfing rates for diploids and
polyploids and for annuals, herbaceous perennials, and woody
perennials are shown in Tables 3 and 4, respectively.
DISCUSSION
This study is the first to analyze the relationship between
polyploidy and self-fertilization in flowering plants in a
phylogenetic context using quantitative estimates of selfing
rates from natural populations. As indicated by phylogeneti
cally independent contrasts and cross-species analysis, poly
Between species Between genera Between families
Fig. 2. Differences in levels of self-fertilization between diploids and
polyploids for each of the 32 phylogenetically independent contrasts,
arranged in three groups according to node depth (between species,
between genera, and between families). For a given contrast, a positive
value indicates higher levels of selfing in polyploids relative to diploids,
while a negative value indicates the reverse. For each group, a solid line
indicates the mean contrast value.
Table 2. Analysis of variance on the effects of ploidy, life history, and
their interaction on selfing rate in the cross-species analysis.
Analysis Type HI SS
All species
Ploidy 1
Life history 2
Ploidy X life history 2
Error 229
Monocotyledons only
Ploidy 1
Life history 1
Ploidy X life history 1
Error 39
Rosids only
Ploidy 1
Life history 2
Ploidy X life history 2
Error 86
Asterids only
Ploidy 1
Life history 2
Ploidy X life history 2
Error 71
1.25
4.33
0.22
18.65
0.98
0.82
0.11
4.64
0.37
0.88
0.12
5.11
0.60
1.07
0.06
6.27
15.30
26.61
1.35
8.21
6.90
0.96
6.26
7.43
0.96
6.78
6.08
0.34
0.0001
<0.0001
0.2607
0.0067
0.0122
0.3333
0.0143
0.0011
0.3855
0.0112
0.0037
0.7130
ploid angiosperms tend to have higher rates of self-fertilization
than their diploid relatives. This trend is not apparent in the
asterids when PICs are used, but there are only seven PICs in
the ?stend phylogeny, and the lack of power in this analysis
may be exacerbated by a relatively low level of phylogenetic
resolution among the asterids than among the other phyloge
netic trees used in this study. Polytomies can reduce the
validity and power of CAIC, and cross-species analysis can be
more powerful than PICs when a phylogenetic tree is fairly
unresolved (Purvis and Rambaut, 1995). In addition, although
studies suggest that polyploidy is generally associated with a
Fig. 3. Levels of self-fertilization for diploid annuals (Dip. ann.),
polyploid annuals (Poly, ann.), diploid herbaceous perennials (Dip. h.
per.), polyploid herbaceous perennials (Poly. h. per.), diploid woody
perennials (Dip. w. per.), and polyploid woody perennials (Poly. w. per.).
For each group, the central bar indicates the median value, the filled circle
indicates the mean value, the shaded box represents the interquartile range,
and the dashed line indicates the total range.
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September 2007] Barringer?Polyploidy and selfing in plants 1531
Table 3. Least-squares means of selfing rates in the cross-species
analysis for diploids and polyploids. Values in parentheses indicate
standard errors. For each data set used, means were significantly
greater for polyploids than for diploids (Tukey-Kramer honestly
significant difference, for a = 0.05).
Analysis Diploids Polyploids
All species 0.36 (0.02) 0.53 (0.04)
Monocotyledons only 0.41 (0.07) 0.76 (0.10)
Rosids only 0.43 (0.03) 0.60 (0.06)
Asterids only 0.33 (0.05) 0.54 (0.06)
breakdown in gametophytic SI systems (Mable, 2004a), there
is no evidence for a ploidy-dependent breakdown of SI in the
Asteraceae (S. Good-Avila, Acadia University, personal
communication). Of the 77 taxa analyzed in the asterid clade,
29 (38%) belong to the Asteraceae, and this may further
explain the lack of evidence for increased selfing rates among
polyploid asterids.
Selfing rates appear to evolve rapidly relative to rates of
speciation in flowering plants (Barrett et al, 1996), and floral
traits associated with selfing (e.g., small petal size, simulta
neous maturation of pollen and receptivity of stigma, and close
spatial proximity of anther and stigma) often differ among
subspecies and populations (Wyatt, 1984). For example, the
two subspecies of Clarkia xantiana have markedly different
breeding systems (Runions and Geber, 2000), and both C.
exilis and C. tembloriensis have high variation in selfing rates
among populations (Vasek and Harding, 1976; Holtsford and
Ellstrand, 1989). Both genetic and environmental factors
contribute to the evolution of mating systems in plants (Barrett
and Eckert, 1990; Barrett, 2003), and rates of self-fertilization
are known to change rapidly (relative to rates of speciation) in
response to a changing environment (Stebbins, 1950, 1957;
Grant, 1981; Schemske and Lande, 1985; Barrett and Eckert,
1990; Barrett et al., 1996; Barrett, 2003). Because plant mating
systems are so evolutionarily labile, it could be argued that
controlling for phylogenetic relations among taxa may be
unduly conservative in this study. Indeed, a similar argument
might be applied to changes in ploidy because chromosome
number varies among populations of many species (Grant,
1981; Otto and Whitton, 2000; Soltis et al, 2004) and changes
in chromosome number are not necessarily related to speciation
events. Because life-history traits are often phylogenetically
constrained (Mazer, 1990; Peat and Fitter, 1994; Moles et al,
2005), however, it is possible that phylogenetic inertia of traits
not included in this study could contribute to differences in
selfing rates and/or differences in ploidy. This possibility
justifies controlling for phylogenetic relationships among the
taxa analyzed here.
As shown in Table 2, the effect of the interaction between
ploidy and life history on levels of self-fertilization was
nonsignificant in all four of the cross-species analyses,
indicating that the relationship between ploidy and self
fertilization does not depend on life history. Annuals,
herbaceous perennials, and woody perennials all tend to have
increased selfing rates among polyploids relative to diploids.
As can be seen in Fig. 3, however, levels of self-fertilization
range widely in all categories regardless of ploidy or life
history, suggesting that selective forces not considered in this
study influence the evolution of self-fertilization. In agreement
with previous studies (Barrett and Eckert, 1990; Barrett et al.,
Table 4. Least-squares means of selfing rates in the c
analysis for annuals, herbaceous (herb.) perennials (per.
perennials. Values in parentheses indicate standard erro
superscripts within rows indicate means that differ si
(Tukey-Kramer honestly significant difference, for a =
Analysis Annuals Herb. per. Woody
All species 0.64 (0.04)a 0.43 (0.03)b 0.2
Monocotyledons only 0.74 (0.10)a 0.43 (0.07)b na
Rosids only 0.66 (0.06)a 0.55 (0.06)a 0.
Asterids only 0.61 (0.06)a 0.41 (0.07)a-b 0
Note: na = not applicable
1996), selfing rates are negatively associated with li
and this trend is apparent in both polyploids an
Annual species have higher selfing rates than p
Among perennials, herbaceous species self more tha
long-lived woody species. This result is cons
theoretical expectations that short-lived species
to self-fertilize more than long-lived species, owing
for reproductive assurance in the former (Stebbins
the cost of seed discounting (decreasing levels of
seed production due to increased levels of self-fert
the latter (Lloyd, 1992; Morgan et al., 1997). The
reasons why outcrossing rates might be higher in
species as well. For example, long-lived species (e.g.
shrubs) are often larger than short-lived species (e
and because plant cells are not differentiated in
somatic and germ cell lineages, mutations that o
mitosis can contribute to the genetic load carried b
Because larger plants are expected to have a greater
mitotic cell divisions between germination and the
of gametes (relative to smaller plants), this m
profound inbreeding depression and strong selec
selfing (Morgan, 2001; Scofield and Schultz, 2006
Polyploids are known to undergo diploidization
by which their chromosomal behavior reverts back t
diploid, owing to a variety of phenomena such a
genomic rearrangements, gene silencing and/or los
evolution of novel functions by one or mor
duplicated genes (Wendel, 2000; Wolfe, 2001; So
2004). Though some taxa treated as polyploids in
may behave cytogenetically as diploids, the met
ensure that such taxa have undergone a relative
polyploidization event because they were com
congeners possessing at least half as many chro
The assumption then is that the evolution of self-f
might be associated with polyploidization regard
current cytogenetic behavior of a given taxon.
Allopolyploids may not differ from diploids in
inbreeding depression (Bever and Felber, 1992; Ronf
Soltis and Soltis, 2000; Comai, 2005), and if
inbreeding depression contributes to the evolution
selfing rates among polyploids, it would be of intere
whether this pattern occurs in both alio- and autopol
is more prevalent in one group relative to t
Unfortunately, the category of ploidy is not kno
majority of polyploids included in this study, and w
and autopolyploids differ in terms of their relation
self-fertilization remains unknown. Autopolyploids
thought to be quite rare (Grant, 1981), but there
evidence that they are much more common in n
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1532 American Journal of Botany [Vol. 94
initially believed (Soltis et al., 2004). Because most theoretical
and empirical work has focused on autopolyploidy and its
effects on the evolution of self-fertlization (e.g., Husband and
Schemske, 1997; Ronfort, 1999; Rausch and Morgan, 2005),
the results presented here suggest that either autopolyploids are
indeed more common (at least among those polyploids
represented in the data set) or that the association between
self-fertilization and polyploidy does not differ between allo
and autopolyploids.
Conclusions?In agreement with other studies (e.g., Cook
and Soltis, 2000; Quarin et al, 2001; T?te and Simpson, 2004;
Guggisberg et al., 2006), the data support the hypothesis that
polyploid angiosperms have, on average, higher rates of self
fertilization than their diploid relatives. Of continued interest
are the evolutionary and ecological phenomena that underlie
this pattern, and they are likely both numerous and varied. The
ability to self-fertilize may increase the likelihood that newly
arisen polyploids can establish successful populations, and
selfing taxa may give rise to successful polyploid lineages
more often than do outcrossing taxa. Decreased levels of
inbreeding depression in polyploids might also help to explain
why polyploids have higher rates of self-fertilization than
diploids. The relationship between ploidy and inbreeding
depression is complex, however, and has been shown to
depend on many factors, including the number and lethality of
deleterious al?eles, the degree of dominance among al?eles and
epistasis among loci, and the age of the polyploid in question
(Ronfort, 1999; Pannell et al., 2004). More empirical studies
that compare mating systems and inbreeding depression in
closely related polyploids and diploids are needed to further
address these issues. In addition, auto- and allopolyploids may
differ in their response to inbreeding. Accordingly, models that
compare and explore further the evolution of inbreeding
depression in polyploids and diploids?especially those that
differentiate between neopolyploids vs. older polyploids and
autopolyploids vs. allopolyploids?will be of value.
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