Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae

Article (PDF Available)inNew Phytologist 173(2):401-14 · February 2007with21 Reads
DOI: 10.1111/j.1469-8137.2006.01905.x · Source: PubMed
Abstract
The self-incompatibility (SI) status of 571 taxa from the Asteraceae was identified and the taxa were scored as having SI, partial SI or self-compatibility (SC) as their breeding system. A molecular phylogeny of the internal transcribed spacer (ITS) region was constructed for 211 of these taxa. Macrophylogenetic methods were used to test hypotheses concerning the ancestral state of SI in the Asteraceae, the gain and loss of SI, the irreversibility of the loss of SI and the potential for partial SI or SC to be terminal states. The ancestral breeding system in the family could not be resolved. Both maximum likelihood and parsimony analyses indicated that transitions among all breeding system states provide the best fit to the data and that neither partial SI nor SC is a terminal state. Furthermore, the data indicated that the loss of SI is not irreversible, although breeding system evolution has been more dynamic in some clades than in others. These results are discussed within the context of evidence for the gain and loss of SI, the evolutionary role of partial SI and methodological assumptions of tests of breeding system evolution.
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Blackwell Publishing Ltd
Macrophylogenetic analyses of the gain and loss of
self-incompatibility in the Asteraceae
Miriam M. Ferrer and Sara V. Good-Avila
Department of Biology, Acadia University, Wolfville, Nova Scotia, Canada B4P 2R6
Summary
The self-incompatibility (SI) status of 571 taxa from the Asteraceae was identified
and the taxa were scored as having SI, partial SI or self-compatibility (SC) as their
breeding system. A molecular phylogeny of the internal transcribed spacer (ITS)
region was constructed for 211 of these taxa.
Macrophylogenetic methods were used to test hypotheses concerning the ances-
tral state of SI in the Asteraceae, the gain and loss of SI, the irreversibility of the loss
of SI and the potential for partial SI or SC to be terminal states.
The ancestral breeding system in the family could not be resolved. Both maximum
likelihood and parsimony analyses indicated that transitions among all breeding
system states provide the best fit to the data and that neither partial SI nor SC is a
terminal state. Furthermore, the data indicated that the loss of SI is not irreversible,
although breeding system evolution has been more dynamic in some clades than
in others.
These results are discussed within the context of evidence for the gain and loss of
SI, the evolutionary role of partial SI and methodological assumptions of tests of
breeding system evolution.
Key words:
ancestral character state reconstruction, evolution of breeding systems,
partial self-incompatibility, self-incompatibility.
New Phytologist
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: 401 414
© The Authors (2006). Journal compilation ©
New Phytologist
(2006)
doi
: 10.1111/j.1469-8137.2006.01905.x
Author for correspondence:
S. Good-Avila
Tel:
+
902 5851798
Fax:
+
902 5851059
Email: sara.good-avila@acadiau.ca
Received:
22 August 2006
Accepted:
24 August 2006
Introduction
In plants bearing genetic self-incompatibility (SI) systems,
self-fertilization and inbreeding are prevented by the gene
products of the S-locus which prevent reproduction between
individuals sharing one or more SI alleles (de Nettancourt,
2001). Because of the prevalence of hermaphroditic species in
the angiosperms and the well-documented deleterious effects
of inbreeding, SI is widely believed to have evolved as a
strategy to avoid self-fertilization and inbreeding (Richards,
1986; de Nettancourt, 2001). At least 68 angiosperm families
have been identified as having some kind of genetic SI system
(de Nettancourt, 2001; Silva & Goring, 2001).
In species with both gametophytic and sporophytic SI, the
male and female components of the S-locus are linked and
transmitted as a single Mendelian character (de Nettancourt,
2001; Silva & Goring, 2001) and are both necessary and
sufficient to cause SI in the correct genetic background (Lee
et al
., 1994; Murfett
et al
., 1994). This has led researchers to
treat SI as a qualitative trait. However, despite the precise
action of S-genes, natural populations of plants often show
broad variation in the SI response, and modifiers weakening
or nullifying SI can be linked or unlinked to the S-locus and
controlled by one or multiple genes that may also be influenced
by the environment (Levin, 1996; Stephenson
et al
., 2000;
Good-Avila & Stephenson, 2002; Stone, 2002). This means
that natural populations of plants may vary from being strictly
self-incompatible to showing intra- or interpopulation
variation in the strength of SI, known as partial or pseudo
self-incompatibility/self-compatibility (PSI hereafter).
After a review of the breeding systems and geographic
ranges of many plant species, Stebbins (1974) concluded that
the transition from SI to predominant self-fertilization was one
of the most common transitions in plant breeding systems. A
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breakdown in SI has been shown to evolve in populations in
which sexual reproduction is limited by mate availability, such
as small or colonizing populations (Levin, 1996; Kunin &
Shmida, 1997; Hiscock, 2000), and macrophylogenetic studies
have identified the independent loss of SI multiple times in
virtually all groups examined (Takebayashi & Morrell, 2001).
Although the common occurrence of a breakdown in SI is well
established, there are at least two aspects of the macro-
evolutionary dynamics of breeding system evolution that are
unresolved: the evolutionary role of PSI, and the irreversibility
of the loss of SI. Firstly, typically, PSI is assumed to be a transient
state between SI and self-compatibility (SC) (Levin, 1996),
but its macroevolutionary role has never been addressed
(Goodwillie
et al
., 2005). In particular, is PSI part of a transition
to SC, a stable or terminal state or likely to revert to SI?
Secondly, macrophylogenetic analyses support the intui-
tion that SI is lost more frequently than gained (Takebayashi
& Morrell, 2001), and Igic
et al
. (2006) recently presented
evidence that the loss of SI is essentially irreversible in the
Solanceae. However, although there are arguments for think-
ing that the loss of SI is irreversible (see Igic
et al
., 2004), it is
not clear how general this conclusion is. A review of seven
macrophylogenetic studies assessing rates of the gain and loss
of SI found support for the gain of SI in three of the studies
(Takebayashi & Morrell, 2001). SI could be regained through
either the
de novo
origination of SI or the restoration of the
ancestral SI system. A broad survey of the number of SI systems
in the angiosperms estimated that new SI systems have evolved
a minimum of 21 independent times (Weller
et al
., 1995;
Steinbachs & Holsinger, 2002) and, indeed, multiple systems
have now been identified within the family Polemoniaceae
(Barrett
et al
., 1996; Kohn
et al
., 1996; de Nettancourt, 2001).
The conditions under which an ancestral SI system could be
restored have not been well explored but include restoration
of a modifier locus (Nasrallah
et al
., 2004) or complementa-
tion of modifiers through hybridization between compatible
ancestors or between a self-compatible and self-incompatible
ancestor (Rick & Chetelat, 1991).
A macrophylogenetic analysis of breeding systems is per-
formed by reconstructing the phylogenetic relationship of a
suite of species and using the character (breeding) states of the
extant taxa to infer past evolutionary processes. Using methods
based on maximum likelihood (ML) and/or parsimony,
one can evaluate variables such as the number of gains or
losses of a trait, the transition rates between character states,
whether trait evolution is punctual or gradual, and the inferred
location of character state changes on the tree topology, and
test hypotheses such as a bias in the rate of gain vs loss or
the irreversibility of trait evolution (Harvey & Pagel, 1991;
Sanderson, 1993; Pagel, 1999a). Collectively, these analyses
provide important information about the (ir)reversibility of
trait evolution, because the location as well as the frequency of
gains/losses is integral to understanding and testing hypotheses
about the evolutionary process.
In this paper, we examine the evolutionary dynamics of the
gain and loss of SI in the Asteraceae, a family known to possess
sporophytic SI, although the gene regulating it is not known
(de Nettancourt, 2001). To do this, we collected DNA
sequence data and SI status information for 193 species (211
taxa) representing most of the tribes in the Asteraceae. We
then employed methods based on both ML (Pagel, 1994,
1999b) and parsimony (Maddison & Maddison, 1989) to ask
the following questions.
What model best describes breeding system evolution in
the family and is there evidence for the gain of SI?
What is the evolutionary role of PSI?
What are the transition rates between character states?
Is there a punctual or gradual mode of trait evolution?
What is the ancestral state of SI (SI, PSI or SC) in the
Asteraceae?
• What is the ancestral character state reconstruction of
breeding traits on the phylogeny and does the loss of SI tend
to occur on terminal branches?
Because of our focus on PSI as well as SC, we refer to the
loss of SI as any forward transition from SI to PSI to SC and
the gain of SI as any backward transition from SC to PSI to SI.
Materials and Methods
Data collection
SI status
We surveyed different databases to obtain infor-
mation from as many species in the Asteraceae as possible
regarding SI status. The SI status was obtained by surveying
published articles concerning the reproductive ecology and/or
systematics of species in the family (database available upon
request). The nomenclatural synonyms for each taxa were
obtained by searching in The International Plant Names Index
(2005). Our final database contained information on the SI
status of 544 species, but 39 of these were part of species
complexes consisting of various subspecies or varieties, and
the final data set consisted of 571 taxa. We scored the SI status
as SI, PSI or SC depending on evidence from pollination and/
or microscope work. Most authors declared a species as self-
incompatible when fruit set after hand self-pollination was
zero or very low (
<
0.05) and/or when they observed no
germination or growth of self-pollen on the stigmatic surface.
Occasionally, fruit set after self- and cross-pollinations was
recorded and the authors did not explicitly state the SI status
of a species, but if fruit set after self-pollination was zero or
very low (
<
0.05), we called it self-incompatible. Authors
reported species as having PSI if they found variation among
individuals or populations in the strength of SI and sometimes
if a breakdown in SI was induced by environmental factors
such as temperature or age. The number of studies describing
PSI as caused by individual, population or environmental
causes was noted. Most authors defined a species as self-
compatible when it set fruit after self-pollination.
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Molecular sequence data and phylogenetic reconstruction
To
test specific hypotheses concerning the gain and loss of
SI, we searched GenBank for DNA sequence data (internal
transcribed spacer (ITS), megakaryocyte associated tyrosine
kinase gene (
matK
) and ribulose-biphosphate carboxylase gene
(
rbcL
)) for the 571 taxa for which we had SI status data. We
obtained data for 211 (193 species) of the 571 taxa for the internal
transcribed spacer (
ITS1
and
ITS2
, 5.8 S) in the nuclear genome.
Differences in the number of taxa within each category between
the phylogenetic (
n
=
211) and full (
n
=
571) data sets were
assessed for significance using a
χ
2
test. A previous phylogenetic
analysis of the Asteraceae using ITS sequence data by Goertzen
et al
. (2003) recognized 15 tribes in the Asteraceae: the proportion
of taxa represented in each tribe in our molecular data set is
presented in Table 1. Of the 211 taxa for which we obtained
sequence data, there were representatives from all four subfamilies
and 11 of the 15 tribes recognized by Goertzen
et al
. (2003),
and five of the 10 subfamilies and 17 of the 36 tribes described
by Panero & Funk (2002) (Table 1). The number of taxa
is greatest in the subfamily Asteroideae (tribes Astereae
+
Heliantheae
sensu lato
) with
c
. 57% of the taxa. This is
probably a consequence of it being the largest subfamily in
the Asteraceae (Bremer, 1994), and it containing two of the
most economically (Heliantheae) and ecologically (Madieae)
important tribes for which breeding system data are available.
The underrepresentation of other tribes can be attributed to
the fact that most of the 36 tribes described by Panero & Funk
(2002) for which we lack data are monotypic or contain only
a few species, and the fact that the species in these tribes are
locally endemic and there are little or no breeding system data.
The 211 ITS sequences were aligned with C
LUSTAL
X
(Thompson
et al.
, 1997) using stepwise alignment by first
aligning species within a genus and then genera within tribes.
Finally, the tribes were aligned with reference to the consensus
sequences obtained by Goertzen
et al
. (2003). This final align-
ment was edited and trimmed using
BIOEDIT
(Hall, 1999),
resulting in a total sequence length of 703 bp. To reconstruct
the phylogenetic relationships among taxa, the best model of
nucleotide substitution was chosen using maximum likelihood
criteria as employed in
MODELTEST
3.07 (Posada & Crandall,
1998). The Tajima & Nei (1982) model of nucleotide substi-
tution with a gamma distribution of mutation rates among
sites (
a
=
1.37) provided the best fit to the data. The phylogeny
was obtained with
MEGA
2 software (Kumar
et al
., 1993), using
minimal evolution as the optimality criterion.
To examine the gain and loss of SI in the Asteraceae, we fol-
lowed the ML methods of Pagel (1997, 1999b) to (a) investi-
gate whether trait evolution was punctual or gradual, which
also results in testing the importance of including the branch
length information, (b) determine the ancestral state of SI in
the Asteraceae, (c) test alternate hypotheses concerning the
nature of character state evolution in the family, (d) recon-
struct the ancestral SI state at all internal nodes on the phylo-
genetic tree, and (e) using the ancestral state reconstruction
count the proportion of transitions occurring on internal
nodes or terminal branches. Additionally, we repeated parts
(c), (d) and (e) using the method of parsimony. The analyses
were performed on rooted trees and, for the ML method,
branch lengths were estimated by the minimum evolution cri-
teria. Trees were rooted with
Chuquiraga oppositifolia
D. Don,
which is a member of the most basal tribe, the Barnadesieae,
in the Asteraceae (Jansen & Kim, 1996; Panero & Funk, 2002;
Goertzen
et al
., 2003), and polytomies were resolved by
setting the branch length subtending them to 0.0000001,
thereby treating them as soft rather than hard. The sensitivity
of the results to changes in the topology was assessed by forc-
ing this tree to have the topology of the tribal relations, as
described by Goertzen
et al
. (2003) or Panero & Funk (2002),
and re-doing each of the analyses described below.
(a) Test of the importance of branch length information for
understanding character evolution (i.e. the mode of evolution).
Given the three character states, SI, PSI and SC, the full model
of character evolution includes six transitions: SI
SC, SI
PSI, PSI
SI, PSI
SC, SC
SI and SC
PSI. ML methods
can be used to infer both the tempo and the mode of character
state changes. The tempo is inferred from the transition rate
estimates themselves, while the mode is inferred from a scaling
parameter,
κ
, which assesses the probability that transitions are
dependent on branch length (Pagel, 1999a). If
κ =
0, trait evolu-
tion is independent of the branch lengths, indicating a punctual
Table 1 Number of species and their relative representation in the
phylogenetic analyses according to the inclusion in the tribes as
described by Panero & Funk (2002) and Goertzen et al. (2003)
Tribe
Species
(n)
% in
phylogenetic
data set
Panero & Funk
(2002)
Goertzen
et al. (2003)
Bardanesiae Bardanesiae 1 100
Mutiseae Mutiseae 5 40
Cichorieae Lactucaceae 124 48
Carduea Carduea 24 54
Arctotae Arctotae 1 100
Anthemidae Anthemidae 23 26
Calendulae Calendulae 15 7
Senecionae Senecionae 12 42
Asterae Asterae 104 15
Gnaphalae Gnaphalae 7 0
Heliantheae 254 42
Helenieae* 22 45
Heliantheae* 100 36
Coreopsidaeae* 41 46
Tageteae* 2 50
Eupatorieae* 14 14
Millerieae* 18 6
Madieae* 57 67
Total 570 38.8
*These 7 tribes belong to Heliantheae in Goertzen et al. (2003)
classification.
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mode of evolution. With
κ
=
1, trait evolution is dependent
on the branch length, indicating a gradual mode of evolution.
The transition rate estimates are calculated as part of the
process of maximizing the overall likelihood of the distribution
of character states given the hypothesis, while the value and
utility (
κ
0) of including the branch length information are
evaluated by comparing the fit of the data to a full model of
character evolution with and without the scaling parameter,
κ
.
The fit of the data to models including or excluding
κ
was
assessed using both the likelihood ratio test (LRT) and the Akaike
information criterion (AIC). For the LRT, the LR statistic
is LR
=
2log
e
[
H
i
/
H
j
], where
H
i
is the smaller of the two like-
lihoods. The LR statistic is
χ
2
distributed with the degrees of
freedom equal to the difference in the estimated parameters when
models are nested. The AIC statistic is AIC
i
=
2log
e
H
i
+
2
K
i
,
where
H
i
is the likelihood for the model and
K
i
is the number
of parameters in the model (Akaike, 1974). To compare two
models, which need not be nested, the difference in AIC between
the two models is calculated as
AIC
i
=
AIC
i
AIC
min
, where
AIC
min
is the smaller AIC of the two compared models.
Burnham & Anderson (2003) suggest that whenever
AIC
i
=
2
the two models are both substantially supported, when
3
<
AIC
i
> 10 the model with the larger AIC has considerably
less support, and when AIC
i
> 10 the larger AIC model can
be excluded. If two models have the same number of parameters,
as can occur when they are not nested, a difference in the –ln
likelihoods of 2 would be equivalent to a AIC
i
of 4.
(b) Ancestral state of SI for the Asteraceae. To determine
the ancestral breeding state for the Asteraceae, we used the
command ‘fossil’ in the program MULTISTATE (Pagel, 2002) to
assign the root node as SI, PSI or SC and then the calculated
the likelihood of the data. Because the three models concern-
ing the hypothetical ancestor were not nested, the models
were compared using AIC
i
as described in (a).
(c) Test of hypotheses concerning the ML model of breed-
ing system evolution. To find the model of breeding system
evolution that maximized the likelihood of the data, we com-
pared the fit of reduced models to the full model + scaling
parameter (as supported by the analyses; see Results) to test
specific hypotheses about the gain and loss of SI. Specifically,
we restricted transitions to test the following hypotheses: Is (1)
PSI or (2) SC a terminal state? (3) Is the loss of SI irreversible,
i.e. do only forward transitions occur (SI PSI SC, or SI
SC)? (4) Is there a bias in the rates of the gain and loss of
SI, i.e. are the rates of forward and backward transitions equal?
Because we found strong evidence that backward transitions
were required to explain the data, we performed a series of
tests to more rigorously examine the importance of the back-
ward transitions. We tried several model building approaches,
but present analyses in which all forward transitions were
allowed and then one or two backward transitions were added
to see if they significantly improved the model. The above
analyses were performed with the aid of MULTISTATE software
(Pagel, 2002) using the LRT and AIC statistics described
above to compare models. In addition, the sum of the forward
(α) and backward (β) transition rates among the three char-
acter states for the best fit model (the full model + the scaling
parameter; see Results) was calculated.
(d) Ancestral state reconstruction. To assign an ancestral
breeding state to the internal nodes, each node was succes-
sively fixed as SI, PSI, SC or unresolved and then the likelihood
of the data given this model was recalculated. If the likelihood
of the data given one particular ancestral state was greater than
2.0 units compared with both other states, the node was set
to that state; otherwise it was set to unresolved (Pagel, 1994,
1999b) (equivalent to a AIC
i
of 4.0; see (a) above).
(e) The proportion of gains/losses at internal nodes and ter-
minal branches. Sanderson (1993) describes how the location
on the topology of inferred gains and losses of a trait contributes
to the evidence for irreversibility. For example, if SI was gained
early and subsequently only lost on terminal branches, this
would provide greater support for the hypothesis of irreversi-
bility. To assess this, we calculated the proportion of changes
falling into each of the six transition categories as a function
of the total number of possible changes at both internal nodes
and on terminal branches. This was done by counting the number
of each type of transition occurring on trees in which the ances-
tral character state was reconstructed by either ML or parsimony
methods and dividing by the total possible number of changes,
210 for internal nodes and 211 for terminal branches.
To assess the importance of the gain of SI by an independent
method, we compared the results of the ML methods with
those obtained using parsimony methods. To do this, we
reconstructed the ancestral SI state at all internal nodes using
parsimony rules on the tree topology (without branch lengths)
as implemented in the program M
ACCLADE (Maddison &
Maddison, 2002) and then calculated the number of steps and
character state changes under different step matrices that corre-
spond to the hypotheses outlined above: (1) PSI terminal; (2) SC
terminal; (3) irreversibile parsimony, and (4) the full model –
equivalent to unordered parsimony. We were unable to test
the hypothesis of equal rates of forward and reverse evolution
using parsimony. Using the reconstruction of ancestral states by
parsimony, we also tabulated the number of transitions occur-
ring at internal nodes and on terminal branches (see (e) above).
Results
Robustness of data set and the phylogenetic tree
The frequency of taxa having SI (65%), PSI (10%) or SC
(25%) as their breeding system in the full data set did not
differ significantly from that in the phylogenetic data set
[χ
2
= 0.60, degrees of freedom (d.f.) = 2, P = 0.7395; Table 2].
Of the 56 species in the whole data set, 60% exhibited
variation in the strength of SI within a population and 40%
variation among populations (not shown). Interestingly, for
the species that exhibited within-population PSI, most authors
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Research 405
found that between 8 and 15% of the individuals were self-
compatible while the remaining were either partially or fully
self-incompatible (not shown).
The minimum evolution tree describing the relationship
among tribes provided generally high bootstrap support for
internal nodes: 38% of the internal nodes had a support equal
to or higher than 75%, and 19% of the internal nodes had
support ranging from 50 to 74% (Fig. 1), which is high for a
family such as the Asteraceae known to have evolved rapidly
in the last 40–50 million years (Devore & Stuessy, 1995).
Both methods recovered five subfamilies: Barnadesioideae,
Mutisioideae, Carduoideae, Cichorioideae and Asteroideae.
The first four subfamilies were paraphyletic and consisted of
the following tribes: Barnadesieae (subfamily Barnadesioideae);
Mutisieae (subfamily Mutisioideae), Cadueae (subfamily
Carduoideae) and Cichorieae and Arctoteae (subfamily
Cichorioideae). The subfamily Asteroideae was monophyletic
and was composed of six tribal groups: (1) Anthemideae, (2)
Calenduleae and its sister Senecioneae, (3) Astereae, (4) Hele-
nieae, (5) Eupatorieae, Tageteae and Madieae and (6) Miller-
ieae, Heliantheae and its sister group Coreopsideae (Fig. 2).
The topology of the trees generally concurred with those of
Goertzen et al. (2003) and Panero & Funk (2002), except in
the position of some paraphyletic tribes (not shown). Here, we
present the results based on analyses of the minimum evolution
tree based on our data but with forcing the topology at the
tribe level to concur with that presented in Goertzen et al.’s
(2003), because their tree was also based on ITS but included
more species (288 species) and was highly similar to our
original tree. However, we use the nomenclature of the tribes
as described by Panero & Funk (2002) (listed in Table 1). All
three topologies gave identical conclusions and only influenced
the absolute value of, for example, likelihood scores, showing
that the choice of topology did not affect our results.
Table 2 The proportion (and number) of self-incompatibility (SI),
partial SI (PSI) and self-compatibility (SC) taxa in the entire data set
and that used for the phylogenetic analyses
Entire data set Phylogenetic data subset
SI PSI SC Subtotal SI PSI SC Subtotal
0.63 0.10 0.27 1.0 0.65 0.10 0.25 1.0
(361) (56) (154) (571) (137) (22) (52) (211)
Fig. 1 Condensed minimum evolution tree
depicting the relationships among tribes of
the 211 taxa using internal transcribed spacer
(ITS)1, ITS2 and 5.8 S DNA. The values
subtending the nodes or on branches
represent the bootstrap value for each node
(see text for details). The size of each triangle
is proportional to the number of species
pertaining to each tribe and the branch
length.
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Research406
(a) Test of the mode of evolution of SI
The fit of our data to the full model was significantly
improved based on either the LRT or AIC criterion by the
inclusion of the scale parameter κ (Table 3). The κ value was
small (c. 0.12), suggesting that trait change was punctual –
occurring quickly and then followed by a long period of
stasis.
(b) Ancestral state of SI status in the Asteraceae
The maximum likelihood test to determine whether SI, PSI
or SC was the most likely ancestral state for the family could
not resolve what the most likely ancestral state was: the
likelihoods for the three models were very close and the
difference in AIC was not greater than 2 units for any model
(AIC
SI
= 340.38; AIC
PSI
= 340.36; AIC
SC
= 340.84).
(c) Models of evolution of SI
The first four reduced models had a lower fit to the data than
the full model, using both the LRT and the AIC criterion
(Table 4). We can infer from this that (1) neither SC nor PSI
is a terminal state, and (2) including only forward transitions
or setting the rate of forward transitions equal to that of
backward transitions provides a significantly poorer fit to the
data than the full model. This indicates that the loss of SI is
Fig. 2 Rates of forward () and backward () transitions between
self-incompatibility (SI), partial SI (PSI) and self-compatibility (SC)
reconstructed under the full model of evolution by (a) maximum
likelihood and (b) unordered parsimony.
Table 4 Likelihood, likelihood ratio test (LRT) and difference for the Akaike information criterion (AIC
i
) test for nine hypotheses concerning
the evolution of self-incompatibility (SI) in the Asteraceae
Model
number Transitions included Hypothesis d.f.
–ln
likelihood LRT AIC
i
Parsimon
y
steps
1 All six Full model 163.03 55
2 SI PSI SC, PSI SI and SI SC SC terminal 2 196.83 67.6 63.1 88
3 SI SC PSI, SC PSI and SI PSI PSI terminal 2 171.36 15.94 13.2 57
4 All six, but constraints on rates Forward = backward transition rate 3 174.6 23.14 17.1
5 SI PSI SC and SI S C Irreversibility (forward transitions only) 3 207.80 89.5 83.1 104
6 All forward + PSI SI Forward + one backward 2 197.48 68.9 64.9
7 All forward + SC SI Forward + one backward 2 169.49 12.9 8.9
8 All forward + SC PSI Forward + one backward 2 196.83 67.6 64.1
9 All forward + SC SI and PSI SI Forward + two backward 1 169.72 13.3 11.8
The likelihood ratio test of each reduced model (numbers 2–9) nested in the full model is χ
2
distributed and evaluated with the degrees of
freedom (d.f.) indicated. When AIC
i
> 10 the model with the larger AIC can be rejected (see text for details).
Likelihood ratios > 3.84 for 1 d.f., 5.991 for 2 d.f., or > 7.84 for 3 d.f. indicate a significant difference between the full and reduced models.
PSI, partial self-incompatibility; SC, self-compatibility.
Table 3 Likelihood, likelihood ratio test (LRT) and difference in the
Akaike information criterion (AIC
i
) test comparing the full model of
evolution of self-incompatibility (SI) status with and without the
branch scaling parameter (κ)
Model –ln likelihood d.f. LRT AIC
i
Full 187.0359
Full + κ 163.0318 1 48.0081 46.008
A likelihood ratio > 3.841 indicates that the scaling parameter has a
significant affect on the model.
d.f., degrees of freedom.
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org New Phytologist (2007) 173: 401414
Research 407
not irreversible and that at least some backward transitions are
required to explain the data. The relative importance of the
backward transitions is tested in models 69 (Table 4). This
shows that no single reverse transition is sufficient to provide
as good a fit to the data as the full model but that inclusion of
the transition from SC to SI shows the greatest improvement
in the likelihood. The transition rate estimates for the best fit
model of character state evolution using ML are shown in
Fig. 2. Keeping in mind that these are the instantaneous
transition rates over the whole tree (and are not probabilities),
this underscores that mating system evolution in the Asteraceae
is very dynamic. The total value of the forward transition
rates, α, is 0.76 and that of backward transitions, β, is 0.52,
giving a relative rate of the loss of SI of α/(α + β) = 0.59.
(d) Ancestral state reconstruction: overall patterns of
gain and loss of SI on the phylogeny
The phylogenetic tree describing the reconstruction of the
ancestral breeding states using ML methods (Fig. 3) reveals
that the ancestral state of some internal nodes could not be
resolved (grey solid lines) and others were identified as either
SC or PSI (grey dashed lines). However, of the resolved
branches, there are clear differences in the number of gains
and losses of SI in each tribe. For example, several clades are
predominantly SI such as (a) the genus Coreopsis L. (Coreopsidae,
node A; Fig. 3a), (b) the Madieae clade (Silversword alliance
node F; Fig. 3a), (c) the Calycadenia DC clade (node E; Fig. 3a),
and (d) members of the genus Helianthus L. (node D) and the
genus Sonchus L. (node N; Fig. 3b). In these clades the loss of
SI is more frequent than its gain and tends to occur on
terminal branches. Other clades exhibit mixtures of SI, PSI
and SC and many changes in the breeding system are inferred
to have occurred. For example, (a) the tribes Astereae,
Senecioneae and Cardueae (Fig. 3b) are dominated by SC and
PSI and the closely related tribe Cardueae (Fig. 3b) has all
three character states approximately equally represented, and
(b) the basal members of the tribe Cichorieae are also
dominated by SC or PSI as exemplified by members of the
genera Cichorium (node L; Fig. 3b) and Lactuca (node M;
Fig. 3b). Striking examples of the gain of SI are inferred: (a)
in a section of the Heliantheae, the Encelia Adans. alliance
(node C; Fig. 3a), (b) in the Coreopsidae because the ancestral
genus, Bidens L., is SC (node B; Fig. 3b), (c) in the genus
Malacothrix in the tribe Cichorieae (node K; Fig. 3b), (d) at
multiple locations within the tribes Asteraceae, Senecioneae,
Cardueae and Cichorieae (L, M, and N) and (e) in the genus
Lasthenia in the tribe Helenieae (node G; Fig. 3a).
Reconstructing the ancestral state of SI using parsimony
rules and four different models of character state change
revealed that parsimony methods also strongly prefer models
in which both gain and loss of SI can occur (supplementary
material Fig. S1, available online, and Table 4). A step matrix
of unordered parsimony is parallel to the ML full model and
required the fewest number of inferred changes, 55 steps, of
all the models examined (Table 4). The transition rates of this
model are, overall, quite similar to those found under ML
(Fig. 2b). The number of steps required to reconstruct the
ancestral states assuming only forward changes (irreversible
parsimony) was 104. Constructing parsimony step matrices
that are parallel to the ML models of PSI or SC as a terminal
state required 57 or 88 steps (Table 4). This suggests that
parsimony methods agree with those based on ML in that the
full/unordered model is best, except that parsimony finds that
PSI may be a terminal state, probably because parsimony
reconstructs transitions to PSI only on terminal branches.
(e) The proportion of gains/losses at internal nodes
and terminal branches
Between 5 and 13% of the internal or terminal branches
showed a shift in breeding system based on ML or parsimony
ancestral character state reconstructions (Table 5). These
changes indicate that there are no transitions from partial SI
to SC (losses) or to SI (gains) inferred via parsimony (see also
Fig. S1). In addition, ML infers that the loss of SI is twice as
frequent on internal than terminal branches and occurs from
SI to partial SI and from partial SI to SC while parsimony
infers 2–4 times more losses on terminal than internal
branches and infers them as occurring from SI to SC and SI
to partial SI. Finally, ML infers slightly more gains of SI on
terminal than internal branches but three times more gains
than losses on terminal branches while parsimony infers that
2.5 times more gains occur on terminal than internal
branches. ML calculates these gains as occurring from SC to
SI and from partial SI to SI while parsimony infers them as
Table 5 Proportion of transitions occurring at internal nodes and
on terminal branches using either maximum likelihood (ML) or
parsimony ancestral character state reconstruction for the evolution
of self-incompatibility (SI) in Asteraceae
Transition
Internal nodes Terminal branches
ML Parsimony ML Parsimony
SI SC 0.0000 0.0143 0.0000 0.0427
PSI SC 0.0143 0.0000 0.0095 0.0000
SI PSI 0.0190 0.0048 0.0047 0.0237
Total loss 0.033 0.0191 0.0142 0.066
SC SI 0.0190 0.0190 0.0474 0.0332
SC PSI 0.0000 0.0095 0.0000 0.0284
PSI SI 0.0190 0.0000 0.0000 0.0000
Total gain 0.038 0.0285 0.0474 0.062
Total changes 0.071 0.0476 0.0616 0.128
The proportion of changes occurring for each transition were
estimated using the total of possible changes at internal nodes (210)
or on terminal branches (211).
PSI, partial self-incompatibility; SC, self-compatibility.
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Research408
Fig. 3 Reconstruction of the ancestral state of self-incompatibility (SI) in the Asteraceae using maximum likelihood and the criteria indicated in
the text. Character states of internal and terminal branches: solid, SI; dashed, partial SI (PSI); dotted, self-compatibility (SC). Grey solid lines,
branches for which the ancestral state was uncertain (SI, PSI or SC equally probable); grey dashed lines, either SC or PSI. Letters indicate genera
or alliances with more than three taxa represented in the phylogeny: (a), (A) Coreopsis, (B) Bidens, (C) Encelia, (D) Helianthus, (E) Calycadenia,
(F) silversword, (G) Lasthenia; (b), (H) Solidago, (I) Senecio, (J) Centaurea, (K) Malacothrix, (L) Cichorium, (M) Lactuca and (N) Sonchus.
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org New Phytologist (2007) 173: 401414
Research 409
Fig. 3 continued
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Research410
occurring from SC to SI and from SC to partial SI. Thus,
ML suggests that the loss of SI is greater on internal nodes and
the gain of SI greater on terminal branches, while parsimony
reconstructs both greater loss and greater gain on terminal
branches. The slight differences in the transitions described in
the internal/terminal branch analyses (Table 5) compared with
the transition rate estimates (Fig. 2) are caused by the former
being based on the changes assigned by the ancestral state
reconstruction (i.e. changes that were justified by the 2 log
likelihood criterion for a single node) while the latter were based
on the full probabilistic model of character state evolution.
Discussion
Our literature survey of the breeding systems of 571 species in
the Asteraceae revealed that the majority of plants in the
Asteraceae are self-incompatible (63%), but a significant
proportion are either partially self-incompatible (10%) or
self-compatible (27%). Analyses of the patterns of gain and
loss of SI by both ML and parsimony indicate that breeding
system evolution has been very dynamic and is best described
by a model in which transitions among all character states are
allowed to occur. In particular, we can reject two slightly
different tests of irreversibility: that the rate of forward is not
equal to the rate of backward transition, and that the number
of backward transitions is zero. Ancestral character state
reconstruction by both ML and parsimony showed that
breeding system evolution has been more dynamic in some
clades than others, but that gains and losses of SI have
occurred on both internal and external branches, providing
stronger evidence that the loss, or partial breakdown, of SI is
not irreversible in the Asteraceae.
The use of ML methods to study character evolution pro-
vides the opportunity to examine the mode of evolution and
to investigate whether including branch length information
improves the fit of the data to the model of character evolution.
Our analyses indicated that breeding system evolution in the
Asteraceae is punctual and that including a scaling parameter,
κ, to describe this evolution significantly improves the fit of
the data. The finding that breeding system changes occur soon
after speciation suggests that they may have a role in speciation:
a finding that is not surprising, and a hypotheses that could
be further examined using ML-based phylogenetic models.
Although the SI status of the ancestor of the family could
not be resolved by ML methods, the finding that 63% of
extant species have SI suggests that it is an ancient breeding
system in the family, as other authors have argued (Richards,
1986; Lane, 1996). An inspection of Fig. 3 (or the supple-
mentary material Fig. S1 using parsimony) shows that, while
the basal group in the family, the Barnardisioneae, is self-
incompatible the other basal tribes, the Mutiseae and Cichorieae,
are not predominantly self-incompatible and the ancestral
character states for the family tend to be reconstructed as SC,
PSI or uncertain. Thus, while the phylogeny gives some
support to the hypothesis that the family is ancestrally self-
incompatible or partially self-incompatible, many species in
the subfamilies Cichorioideae and Carduoideae must have
subsequently lost SI.
Before we discuss the implications of these results, it is
worth discussing some of the assumptions of the methods
used to generate them. Firstly, both methods assume that the
phylogeny reflects the true topology for the family (Harvey &
Pagel, 1991). We are confident that the relationships within
tribes reflected the true topology because most internal nodes
below the level of subtribes had bootstrap support higher than
80%. The internal nodes that had lower bootstrap values were
those for which the true phylogenetic relationships remained
unresolved. However, when we employed the topologies of
either Goertzen et al. (2003) or Panero & Funk (2002), the
main results were identical, giving further statistical support
to our conclusions. Secondly, Pagel’s ML method (Pagel,
1994, 1999b) assumes that forward and backward transitions
are equally probable (unless one imposes a restriction that
α = β) and then calculates the likelihood of the data given a
model. Pagel (1999a) tested the assumption of steady-state
character evolution using a bacteriophage data set and con-
cluded that the assumption was reasonable, but if differential
transition rates across the tree are a result of differences in
birth or death rates of self-incompatible or self-compatible taxa
this may be more problematic (Adam Richman, pers. comm.).
Thirdly, Takebayashi & Morrell (2001) noted that, in
studies that use ML methods to infer rates of the gain and loss
of SI, the proportion of forward to total transitions (α/
(α + β)) tends to be equal to the proportion of selfing (or self-
compatible) species in the data set. The authors propose that
ML estimators of α and β may be more sensitive to topolog-
ical information when larger phylogenetic data sets are used.
We found that the proportion of forward to total transitions
was 0.59 while the proportion of SC + partial SI taxa was
0.35; this suggested that our analyses were more sensitive to
the topological information, perhaps because of the inclusion
of four times more taxa compared with those reviewed by
Takebayashi & Morrel (2001) (211 vs 2560).
Fourthly, the ability to detect a difference in the rate of gain
vs loss of a character trait and to test for irreversibility depends
on the size of the phylogeny, when the trait is first gained and
the overall rates of gain and loss of the trait (Sanderson, 1993).
Sanderson (1993) concluded that the power of the test for
both hypotheses was generally low. General conditions for
improving the power of the test were provided when the ana-
lyses were performed on large phylogenies in which rates of
both the gain and the loss of traits were high and the first trait
gain occurred deep on phylogeny. The data presented here
indicate that we appear to have these conditions: SI appears
early on some deep internal nodes and the overall rates of
character state change are high, and there is evidence that SI
was lost preferentially on internal branches and then gained
on terminal branches.
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org New Phytologist (2007) 173: 401414
Research 411
Lastly, Igic et al. (2006) showed that using only the charac-
ter states of extant taxa to infer the ancestral character states
can lead to spurious results. Using the trans-genetic polymor-
phism of S-alleles to set internal nodes as SI, they showed that
the loss of SI is essentially irreversible in the Solanaceae and
that they would have spuriously concluded it was not irrevers-
ible without the inclusion of the SI ‘fossil’ data. We were not
able to include SI ‘fossil’ data in our data set (because the S-
locus is unknown in the Asteraceae), but have assessed the
location as well as the frequency and importance of transitions
to provide stronger evidence for the reversibility of SI in the
Asteraceae.
The breakdown of SI
Although the Asteraceae exhibit a high proportion of species
with SI, an important fraction of the species (37%) exhibit a
partial or complete breakdown of SI. Our ML results indicated
that the relative rate of forward to backward transitions was
0.59 and that the breakdown of SI occurred approximately
twice as frequently on internal nodes compared with external
nodes, and in virtually all tribes. The evolutionary transition
from SI to either PSI or SC will depend on the genetic
mechanisms controlling the breakdown of SI and the strength
of selection for self-fertility (Levin, 1996; Good-Avila &
Stephenson, 2002). A breakdown of SI is known to be caused
by at least three possible mechanisms: (1) mutations at the S-
locus, (2) the influence of unlinked modifier loci and (3)
polyploidization or S-gene duplication (de Nettancourt,
2001; Stone, 2002). Firstly, mutations at the S-locus that
inactivate the S-gene products typically cause self-fertility in
mutant individuals (Porcher & Lande, 2005). Depending on
the nature of the mutant, the number of S-alleles, the selfing
rate and levels of inbreeding depression, populations are
expected to evolve to SI or SC (Charlesworth & Charlesworth,
1979). Because the gene regulating S is unknown in the
Asteraceae, the role of S-linked mutations in the dissolution
of SI is difficult to assess, but mutations at the S-locus are
believed to have resulted in the appearance of the SC taxon
Stephanomeria exigua Gottlieb ssp. coronaria (Greene) Gottlieb
from its SI ancestor Stephanomeria exigua Nutt. (Brauner &
Gottlieb, 1987) and the breakdown of SI in Carthamus
flavescens L. (Imrie & Knowles, 1971).
Secondly, if a breakdown in SI is caused by an unlinked
modifier locus, it is more difficult for SC to completely invade
a self-incompatible population (Porcher & Lande, 2005).
However, if variation at an unlinked modifier locus causes
PSI, PSI may be evolutionarily stable (Vallejo-Mar’n &
Uyenoyama, 2004). If modifiers of SI are caused by multiple
unlinked modifiers, as found in Campanula rapunculoides L.
(Good-Avila & Stephenson, 2002), then PSI may exhibit
even broader conditions for stability if polymorphism in
modifiers of SI is similar to polymorphism in alleles promot-
ing selfing vs outcrossing (Latta & Ritland, 1993). Indeed,
several detailed crossing studies in the Asteraceae have found
evidence that PSI is caused by variation in unlinked modifier
loci [Senecio squalidus L. (Hiscock, 2000); Aster furcatus Bur-
gues ex Britton & A. Brown. (Reinartz & Les, 1994) and
Chrysanthemum L. (Ronald & Ascher, 1975)]. Experimental
studies have identified several unlinked modifiers of the S-
locus (Hancock et al., 2003) potentially explaining why many
SI species exhibit some variation in the degree of SI in
response to environmental or genetic background conditions
(reviewed in Levin, 1996; Stephenson et al., 2000).
Thirdly, polyploidization may cause a breakdown of SI. A
recent review of the effect of polyploidy on the breakdown of
SI in angiosperms concluded that polyploidy in species with
gametophytically controlled SI can result from competitive
inhibition between heteroallelic pollen but that, overall, there
is no strong association between polyploidy and a complete
loss of SI in angiosperms, especially for species with sporo-
phytically controlled SI (Mable, 2004). An analysis of the
coevolution of the breeding system with polyploidy in the
Asteraceae confirms that there is no overall support for a loss
of SI after polyploidization (M. M. Ferrer and S. V. Good-
Avila, manuscript in preparation). In sum, there is some evi-
dence that the loss of SI may be caused by S-linked mutants
or modifier loci in the Asteraceae but not by polyploidization.
Is there evidence that the breakdown in SI is associated with
island or small population effects? Baker (1955) predicted that
founder effects during island colonization should select for
the breakdown of SI as a result of a predicted reduction in the
number of S-alleles and compatible mates in founder popula-
tions. However, there is not strong support for this hypothesis
in the Asteraceae. There are four groups of island species rep-
resented in our data set: the Madieae (Hawaiian silverswords)
and members of the genus Bidens colonized Hawaii, members
of the genus Malacothrix colonized islands off southern
California and the genus Sonchus reached the Canary Islands.
Two of these exhibit a breakdown of SI with island coloniza-
tion – the Bidens and Malacothrix genera (Williams, 1957;
Davis, 1986; Sun & Ganders, 1986; Sun & Ganders, 1988)
– while two do not – the Hawaiian silverswords (Carr & Pow-
ell, 1986) and island members of the genus Sonchus (Kim
et al., 1999). We suggest that one possible influence of the dif-
ferential response of these groups to island colonization may
be correlated to the evolution of life histories in the groups:
the silverswords and many species of Sonchus are long-lived
perennials, while many species of Bidens and Malacothrix are
annual or short-lived perennials (M. M. Ferrer and S. V.
Good-Avila, manuscript in preparation).
The gain of SI
Perhaps the most surprising finding of this study is the
evidence that the loss of SI is reversible. The finding that SC
can revert to PSI or SI in the Asteraceae could be explained by
several factors, including (1) de novo generation of SI systems
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Research412
and (2) the retention of genes involved in mate recognition.
Firstly, in a parsimony analysis of the number of independent
gains and losses of SI in the angiosperms, Weller et al. (1995)
concluded that SI systems have evolved independently at least
21 times. In this light, it is interesting that one of the broadest
macrophylogenetic studies of the evolution of SI was carried
out in the Polemoniaceae (Barrett et al., 1996) and multiple
origins of SI were needed to explain the phylogeny. Although
this was considered unlikely at the time, recent studies reveal
the presence of multiple SI systems in the Polemoniaceae:
gametophytic SI occurs in Phlox L. (Levin, 1993), Sporophytic
SI in Linanthus Benth (Goodwillie, 1997), and heterostylous
SI in the genus Aliciella Brand. (M. Tommerup and M. Porter,
unpublished). The analyses presented here also suggest that a
de novo origin of SI is possible in the subfamily Asterideae
within the tribes Astereae or Senecioneae or within the tribe
Cichorieae, because most of the basal members in Lactuca
(node m; Fig. 3a) or the sister clade Malacothrix (node k;
Fig. 3a) are partially self-incompatible or self-compatible and
yet the derived members of the Malacothrix clade and the entire
derived Sonchus clade (node n; Fig. 3a) are self-incompatible.
Secondly, a gain of SI could occur because the ancestral SI
system is restored. If the partial or complete breakdown of SI
is caused by an S-linked mutation, S-allele diversity is expected
to erode, making the restoration of SI more difficult (Igic
et al., 2004), although the relative timescale of the erosion of
S-allele diversity to, for example, speciation is unknown.
However, if SI is lost as a result of unlinked modifier alleles it
could theoretically be regained through selection or comple-
mentation of modifier loci after hybridization. There is experi-
mental evidence that SI can be restored via these pathways.
Studies in the self-compatible plant Arabidopsis thaliana (L.)
Heynh. identified remnants of the Brassicaceae SI systems:
three female-linked (S-locus receptor kinase gene (SRK))
S-alleles have been identified (Shimizu et al., 2004) and SI was
restored to one strain by trans-genetically inserting functional
copies of the female (SRK) and male (S-locus Cys-rich gene
(SCR)) S-alleles (Nasrallah et al., 2004). In addition, there is
evidence that SI can be restored or maintained through
hybridization. Restoration of SI was achieved by crossing two
self-compatible races of Lycopersicon hirsutum HBK in Peru
(Rick & Chetelat, 1991) and hybrid individuals of two self-
incompatible species of Rorippa (Brassicaceae) maintain SI
(Bleeker, 2004). These experiments show that SC is not
always irreversible and suggests that the role of hybridization
and gene flow in the evolution of SI warrants further study.
Our analyses indicate that the total rate of loss of SI is as
high as or higher than the rate of gain of SI, and yet 65% of
the species in the family are SI. This implies that there has
been selection to restore SI, as suggested by the relatively high
rates of the gain of SI on terminal branches. Although there
will be diverse factors determining the final mating system of
any species, these results are consistent with the hypothesis
that species that lose SI continue to act as outcrossers. There
is evidence that species that lose SI adopt other breeding
systems such as dioecy (Miller & Venable, 2000) or maintain
temporal or spatial separation of the reproductive functions
that both encourage outcrossing and reduce interference
between male and female functions (Routley et al., 2004). In
the Asteraceae, many self-compatible taxa exhibit mixed
mating systems; outcrossing rates in Bidens species in Hawaii
range from 0.425 to 0.881 (Sun & Ganders, 1988), in H. annus
they range from 0.6 to 0.91 (Ellstrand et al., 1978), and in
Prionopsis ciliata DC they were found to have a mean of 0.57,
while only a few self-compatible species have been found to
predominantly self-fertilize, such as Tragopogon mirus Ownbey
(0.07) (Soltis et al., 1995). Partially self-incompatible species
have also been found to be predominantly outcrossing,
with Rutidosis leptorrynchoides Hook showing an outcrossing
rate of 0.82 (Young et al., 2002) and Flourensia cernua DC an
outcrossing rate of 1.00, despite wide variation in strength of
SI among individuals (Ferrer et al., 2004).
The evolutionary role of PSI
Our survey of the literature found that 10% of the species
in the Asteraceae are partially self-incompatible, although
this number is probably a minimum estimate (Levin, 1996).
Interestingly, the majority of these species exhibited within-
population variation in the degree of SI in which between 10 and
15% of the population was fully self-compatible, something
that may indicate the frequency of mutations causing a
weakening of SI or an evolutionary strategy. However, the
results of our macrophylogenetic analyses were somewhat
ambivalent concerning the evolutionary role of PSI. The ML
analyses indicated that SI can lead to PSI which can lead to
SC, especially on internal branches, while SC can revert to PSI
or SI, especially on terminal branches. This result could be
caused by the presence of PSI among species designated as
self-compatible, or by the restoration of PSI in self-compatible
species. However, the parsimony analyses indicated that PSI
is a derived state only in terminal taxa. In either case, the only
evidence that PSI is maintained over longer evolutionary periods
is presented in the tribes Asterae, Calenduleae and Senecioneae,
where ML reconstructed PSI as the most probable state at several
deep internal nodes. Therefore, our analyses suggest that PSI
may be an important component of both the maintenance and
breakdown of SI in the Asteraceae, but its full evolutionary
role requires further theoretical and empirical study.
In conclusion, we have found evidence that the evolution
of the breeding system has been dynamic in the Asteraceae
and that SI can be regained. We suggest that the difference
between the results presented here and those obtained by Igic
et al. (2006) may also be attributed to differences in the
genetic basis, physiology and population dynamics of SI
between sporophytic SI in the Asteraceae and gametophytic
SI in the Solanaceae. We surveyed 571 species in the Asteraceae
and 218 in the Solanaceae and found that the proportion of
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org New Phytologist (2007) 173: 401414
Research 413
self-compatible to self-incompatible species is essentially reversed
in the two families: 27% of the species in the Asteraceae are
SC and 73% PSI or SI, while in the Solanaceae 67% are SC
and 33% SI or PSI, although the two families are relatively
closely related and of similar age (Wikström et al., 2001).
Unravelling the mechanisms responsible for differences in the
evolution and breakdown of SI between families is also
undoubtedly influenced by many additional factors such as
growth habit, life-span, apomixis, clonality and latitude. These
coevolutionary dynamics will be explored in future studies.
Acknowledgements
We thank Adam Richman, Joshua Kohn, Marcy Uyenoyama
and Sam Vander Kloet for helpful comments on a previous
version of this manuscript. This research was funded by post-
doctoral fellowship support to MMF from the Organization
of American States (OAS) and by a research grant to SG-A
from the National Sciences and Engineering Research Council
(NSERC) of Canada.
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Supplementary Material
The following supplementary material is available for this
article online:
Fig. S1 Reconstruction of the ancestral state of self-
incompatibility (SI) in the Asteraceae using parsimony as
indicated in the text. Character state of internal and terminal
branches: solid, SI; dashed, partial SI (PSI); dotted, self-
compatibility (SC). Grey solid lines, branches for which the
ancestral state was either SI or SC; grey dashed lines, uncertain
(SI, SC or PSI). Letters indicate genera or alliances with more
than three taxa represented in the phylogeny: (a) Coreopsis,
(b) Bidens, (c) Encelia, (d) Helianthus, (e) Calycadenia, (f)
silversword, (g) Lasthenia, (h) Solidago, (i) Senecio, (j)
Centaurea, (k) Malacothrix, (l) Cichorium, (m) Lactuca and
(n) Sonchus.
This material is available as part of the online article from:
http://www.blackwell-synergy.com/doi/abs/10.1111/j.1469-
8137.2006.01905.x
(this link will take you to the article abstract).
Please note: Blackwell Publishing is not responsible for the
content or functionality of any supplementary materials supplied
by the authors. Any queries (other than missing material)
should be directed to the corresponding author for the article.
    • "In addition, some species in Kalanchoe are known to be polyploid (Baldwin 1938), a characteristic that can break self-incompatibility mechanisms and provide opportunities for the evolution of selffertilization (Chawla et al. 1997). The low frequency of nonherkogamous plants in the SDTFvr may indicate the early stages of a microevolutionary shift in the breeding system of K. pinnata in a similar manner to the many self-incompatible to self-compatible transitions observed in other angiosperms (Barrett 2002; Igic et al. 2004; Mast et al. 2006; Ferrer and Good-Avila 2007). Further Table 3. Life-stage transition matrix of Kalanchoe pinnata based on simple time-stage population matrix models (Leslie 1945; Lefkovitch 1965), parameterized based on both field and glasshouse experiments and observations. "
    [Show abstract] [Hide abstract] ABSTRACT: Ecological invasions are a major issue worldwide, where successful invasion depends on traits that facilitate dispersion, establishment, and population growth. The nonnative succulent plant Kalanchoe pinnata, reported as invasive in some countries, is widespread in remnants of seasonally dry tropical forest on a volcanic outcrop with high conservation value in east-central Mexico where we assessed its mating system and demographic growth and identified management strategies. To understand its local mating system, we conducted hand-pollination treatments, germination, and survival experiments. Based on the experimental data, we constructed a life-stage population matrix, identified the key traits for population growth, weighted the contributions of vegetative and sexual reproduction, and evaluated management scenarios. Hand-pollination treatments had slight effects on fruit and seed setting, as well as on germination. With natural pollination treatment, the successful germination of seeds from only 2/39 fruit suggests occasional effective natural cross-pollination. The ratios of the metrics for self- and cross-pollinated flowers suggest that K. pinnata is partially self-compatible. Most of the pollinated flowers developed into fruit, but the seed germination and seedling survival rates were low. Thus, vegetative propagation and juvenile survival are the main drivers of population growth. Simulations of a virtual K. pinnata population suggest that an intense and sustained weeding campaign will reduce the population within at least 10 years. Synthesis and applications. The study population is partially self-compatible, but sexual reproduction by K. pinnata is limited at the study site, and population growth is supported by vegetative propagation and juvenile survival. Demographic modeling provides key insights and realistic forecasts on invasion process and therefore is useful to design management strategies.
    Full-text · Article · Jun 2016
    • "In fact, in other Asteraceae taxa, bottleneck effects may have caused the breakdown of SI, as a result of a predicted reduction in the number of S-alleles and compatible mates, especially in highly colonizing, annual or short-lived perennials [44,484950 . However , loss of SI is reversible in Asteraceae [44], and the re-establishment of SI systems may be facilitated when the number of mates rises and the selection against rare taxa decreases. According to our results, brushing increased seed set in C. seridis, which highlights the important but not essential role of pollinators despite self-compatibility. "
    [Show abstract] [Hide abstract] ABSTRACT: Hybridization between tetraploids and their related diploids is generally unsuccessful in Centaurea, hence natural formation of triploid hybrids is rare. In contrast, the diploid Centaurea aspera and the allotetraploid C. seridis coexist in several contact zones where a high frequency of triploid hybrids is found. We analyzed the floral biology of the three taxa to identify reproductive isolation mechanisms that allow their coexistence. Flowering phenology was recorded, and controlled pollinations within and between the three taxa were performed in the field. Ploidy level and germination of progeny were also assessed. There was a 50% flowering overlap which indicated a phenological shift. Diploids were strictly allogamous and did not display mentor effects, while tetraploids were found to be highly autogamous. This breakdown of self-incompatibility by polyploids is first described in Centaurea. The asymmetrical formation of the hybrid was also found: all the triploid intact cypselae came from the diploid mothers pollinated by the pollen of tetraploids. Pollen and eggs from triploids were totally sterile, acting as a strong triploid block. These prezygotic isolation mechanisms ensured higher assortative mating in tetraploids than in diploids, improving their persistence in the contact zones. However these mechanisms can also be the cause of the low genetic diversity and high genetic structure observed in C. seridis.
    Full-text · Article · Oct 2015
    • "These results also imply that the sharing of selfing/outcrossing morph variation among the eight focal species is unlikely due to the retention of an ancestral polymorphism, and the consistent rejection of their monophyly (Table 2 ) further supports this view. Unidirectional transitions from outcrossing to selfing are commonly reported in flowering plants [3, 18–20, 24, 26, 28] but see [25, 27]. However, this is one of few studies to estimate a time-calibrated transition rate to selfing based on a discrete-state character. "
    [Show abstract] [Hide abstract] ABSTRACT: Background The transition from outcrossing to selfing has long been portrayed as an ‘evolutionary dead end’ because, first, reversals are unlikely and, second, selfing lineages suffer from higher rates of extinction owing to a reduced potential for adaptation and the accumulation of deleterious mutations. We tested these two predictions in a clade of Madagascan Bulbophyllum orchids (30 spp.), including eight species where auto-pollinating morphs (i.e., selfers, without a ‘rostellum’) co-exist with their pollinator-dependent conspecifics (i.e., outcrossers, possessing a rostellum). Specifically, we addressed this issue on the basis of a time-calibrated phylogeny by means of ancestral character reconstructions and within the state-dependent evolution framework of BiSSE (Binary State Speciation and Extinction), which allowed jointly estimating rates of transition, speciation, and extinction between outcrossing and selfing. Results The eight species capable of selfing occurred in scattered positions across the phylogeny, with two likely originating in the Pliocene (ca. 4.4–3.1 Ma), one in the Early Pleistocene (ca. 2.4 Ma), and five since the mid-Pleistocene (ca. ≤ 1.3 Ma). We infer that this scattered phylogenetic distribution of selfing is best described by models including up to eight independent outcrossing-to-selfing transitions and very low rates of speciation (and either moderate or zero rates of extinction) associated with selfing. Conclusions The frequent and irreversible outcrossing-to-selfing transitions in Madagascan Bulbophyllum are clearly congruent with the first prediction of the dead end hypothesis. The inability of our study to conclusively reject or support the likewise predicted higher extinction rate in selfing lineages might be explained by a combination of methodological limitations (low statistical power of our BiSSE approach to reliably estimate extinction in small-sized trees) and evolutionary processes (insufficient time elapsed for selfers to go extinct). We suggest that, in these tropical orchids, a simple genetic basis of selfing (via loss of the ‘rostellum’) is needed to explain the strikingly recurrent transitions to selfing, perhaps reflecting rapid response to parallel and novel selective environments over Late Quaternary (≤ 1.3 Ma) time scales. Electronic supplementary material The online version of this article (doi:10.1186/s12862-015-0471-5) contains supplementary material, which is available to authorized users.
    Full-text · Article · Sep 2015
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